Book HB 37-1

Journal of the Brazilian Association for Horticultural Science Volume 37 number 1 ISSN 0102-0536 January-March 2019 THE BRAZILIAN ASSOCIATION Assistant Editor Francisco Antônio Passos FOR HORTICULTURAL Mirtes F Lima ABH, a convite da Horticultura SCIENCE Brasileira UFRPE Embrapa Hortaliças - Brasília R. Manoel de Medeiros s/n Itamar R Teixeira Dois Irmãos Executive and Editorial Coordination UEG - Anápolis 52171-900 Recife-PE Sieglinde Brune Tel (81) 3320 6000 Jackson Kawakami www.abhorticultura.com.br Associate Editors UNICENTRO - Guarapuava [email protected] Ana Cristina PP de Carvalho Jean Carlos Cardoso President Embrapa Agroindústria Tropical - UFSCar - Araras Roberto de Albuquerque Melo Fortaleza Jesus G Töfoli UFRPE - Recife Antonio T Amaral Júnior Instituto Biológico - São Paulo UENF - Campos dos Goytacazes Vice-President José Magno Q Luz Jackson Kawakami Arminda M de Carvalho UFU - Uberlândia Embrapa Cerrados - Brasília UNICENTRO - Guarapuava Juliano Tadeu V de Resende Carlos Alberto Lopes UNICENTRO - Guarapuava 1st Secretary Embrapa Hortaliças - Brasília Julio Carlos Polimeni de Mesquita Leandro SA Gonçalves Francisco Bezerra Neto UEL - Londrina IPA - Recife UFERSA - Mossoró Marina C Branco 2nd Secretary Geraldo Milanez de Resende Embrapa - Secretaria de Pesquisa e Rene de Paula Posso Embrapa Semiárido - Petrolina Desenvolvimento - Brasília Banco do Brasil - Campinas Gilmar Paulo Henz Moysés Nascimento Embrapa-Secretaria de Inteligência UFV - Viçosa 1st Treasurer e Relações Estratégicas - Brasília Gabriel Alves Maciel Patrícia AA Marques Maria do Carmo Vieira ESALQ - Piracicaba IPA - Recife UFGD - Dourados Renata SB Gomes 2nd Treasurer Marinice O Cardoso Embrapa Cocais - São Luiz Thiago Leandro Factor Embrapa Amazonia Ocidental - Manaus Renato Fernando Amabile APTA - Campinas Embrapa Cerrados - Brasília Scientific Editors EDITORIAL COMMITTEE Adriano do N Simões Rhuanito S Ferrarezi University of Florida - USA Horticultura Brasileira UFRPE - Serra Talhada SGAS, Ed. Athenas, Bl. B, s/ 102/103 Vagner Augusto Benedito CEP - 70390-020, Brasília-DF Anderson F Wamser Samuel Roberts Noble Foundation E-mail: [email protected] EPAGRI - Caçador - USA Tel.: (61) 3202 0507 André Luiz Lourenção Valter R Oliveira Editor-in-chief IAC - Campinas Embrapa Hortaliças - Brasília Paulo Eduardo de Melo Catariny C Aleman Wagner F da Mota Embrapa, Gerência de Relações UFV - Viçosa UNIMONTES - Janaúba Estratégicas Internacionais - Brasília Derly José H da Silva Waldemar P Camargo Filho UFV - Viçosa IEA - São Paulo Hortic. bras., Brasília, v.37, n.1, January-March 2019 1

Horticultura Brasileira is indexed by AGRIS/FAO, AGROBASE, CAB, JOURNAL CITATION REPORTS, SciSearch®, Directory of Open Access Journal (DOAJ), TROPAG Scientific Eletronic Library Online: http://www.scielo.br/hb www.horticulturabrasileira.com.br Horticultura Brasileira, v. 1 n.1, 1983 - Brasília, Sociedade de Olericultura do Brasil, 1983 Quarterly F o r m e r t i t l e s : V. 1 - 3 , 1961-1963, Olericultura. V. 4-18, 1964-1981, Revista de Olericultura. Not published: v. 5, 1965; 7-9, 1967-1969. Composition Periodicity until 1981: Annual. João Bosco Carvalho da Silva from 1982 to 1998: Biannual English revision from 1999 to 2001: Four-monthly Carlos Francisco Ragassi from 2002 on: Quarterly Printed copies From 2005 on: Sociedade de Olericultura do Brasil is called Associação Brasileira de Horticultura 80 copies ISSN 0102-0536 Journal partially sponsored by: 1. Horticulture - Periodics. 2. Olericulture - Periodics. I. Associação Brasileira de Horticultura. CDD 635.05 2 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Volume 37 number 1 January-March 2019 Journal of the Brazilian Association for Horticultural Science ISSN 0102-0536 CONTENTS EDITOR'S LETTER 5 ERRATA Strawberry breeding in Brazil: current momentum and perspectives 6 André Ricardo Zeist; Juliano Tadeu V de Resende COVER ARTICLE 7 RESEARCH Reaction of wild Solanaceae rootstocks to the parasitism of Meloidogyne javanica 17 Jéssica Cardoso; Luiza Tonelli; Talita S Kutz; Fernanda D Brandelero; Thiago O Vargas; Rosangela Dallemole-Giaretta Pulse drip irrigation and fertigation water depths in the water relations of coriander 22 Valentin Ruben O Zamora; Manasses M da Silva; Geronimo F da Silva; José Amilton Santos Júnior; Dimas Menezes; Sirleide Maria de Menezes Phenology and agronomic components of first and second-cycle strawberry 29 André R Zeist; Juliano TV de Resende; Renato B Lima Filho; André Gabriel; Juliane M Henschel; Israel FL da Silva Selection of squash “Menina Brasileira” carrying the allele “Bush” with high yield potential 35 Mariane G Ferreira; Gabriella Q de Almeida; Herika P Pessoa; Fançoise D Dariva; Felipe de O Dias; Carlos Nick Resistance of processing tomato genotypes to leafminer (Tuta absoluta) 40 Diego M Dias; Juliano TV de Resende; André R Zeist; André Gabriel; Matheus H Santos; Nathalia C Vilela Vermicompost and biochar substrates can reduce nutrients leachates on containerized ornamental plant production 47 José M Alvarez; Claudio Pasian; Rattan Lal; Rafael López; Manuel Fernández Potential of aqueous extracts of basidiomycetes to control root-knot nematodes on lettuce 54 Caroline N Wille; Cesar B Gomes; Elisandra Minotto; José S Nascimento Salicylic acid: resistance inducer to two-spotted spider mite in strawberry crop 60 Renata Favaro; Juliano Tadeu V Resende; André Gabriel; André R Zeist; Ely Cristina N Cordeiro; Jorge Luís Favaro Júnior Reaction of strawberry cultivars to root-knot and root-lesion nematodes 65 Daniele de Brum; Priscila Monalisa Marchi; Michel A Gonçalves; Fernanda F Cruz; Luis Eduardo C Antunes; Cesar B Gomes Growth promotion and productivity of lettuce using Trichoderma spp. commercial strains 69 Fabíola T Pereira; Jessica B de Oliveira; Paulo Henrique PC Muniz; Gustavo Henrique S Peixoto; Roberli R Guimarães; Daniel Diego C Carvalho Phenotypic stability of strawberry cultivars based on physicochemical traits of fruits 75 André Gabriel; Juliano TV de Resende; André Ricardo Zeist; Luciane V Resende; Nathalia CV Resende; Ricardo Antônio Zeist SCIENTIFIC COMMUNICATION Growth of sweet pepper plants submitted to water tensions in soil and potassium silicate doses 82 Alexandre Igor A Pereira; João de Jesus Guimarães; João Victor Costa; Fernando S de Cantuário; Leandro C Salomão; Roberta C de Oliveira; José Magno Q Luz Hortic. bras., Brasília, v.37, n.1, January-March 2019 3

Journal of the Brazilian Association for Horticultural Science Potato cultivar BRS F63 Camila has higher yield at lower plant spacing 89 Vlandiney Eschemback; Jackson Kawakami; Aline M Genú; Dioni Stroparo 95 Yield, frying quality, plant vigor, and maturity of potato clones 101 Giovani Olegario da Silva; Arione da S Pereira; Agnaldo DF Carvalho; Fernanda Q Azevedo 106 Physiological differences of 'Crocantela' lettuce cultivated in conventional and hydroponic systems 112 Priscila F de Souza; Marcelo Borghezan; Julia Zappelini; Lara R de Carvalho; Joseph Ree; Jorge L Barcelos-Oliveira; Rosete Pescador Tomato progenies selection in Rondônia, Brazil Maria José Marques; Juliana de Fátima Vizú; Danilo F da Silva Filho; César Augusto Ticona-Benavente Physiological characterization of plant growth in sweet potato Marcos Aurélio M Ferreira; Valter C Andrade Junior; Altino JM Oliveira; Evander A Ferreira; Orlando G Brito; Lidiane R Silva 4 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Dear all, Here it goes, Horticultura Brasileira, volume 37. Our cover wants to draw your attention to our colleagues’, Zeist & Resende, paper dealing with the current situation and perspectives of breeding strawberries in Brazil. Worth mentioning that two decades ago, Brazilians found fresh strawberries for very short periods of the year, coming from, perhaps, not more than half a dozen production spots, with high prices matching the scarce offer. Fortunately, that is no longer, by far, the situation. We start a year in which a few changes will be progressively implemented in the journal, in our efforts to keep Horticultura Brasileira updated with the last advances in scientific publishing, as well as with the requirements of publishers and databases. As we mentioned in our last letter, it all has to do with transparency, reliability, and promptness in scientific publication. This way, we can assure that your results will continue to impact the horticultural science and technology. We start by requiring an ORCID code from all authors of our papers. Horticultura Brasileira is pleased to work with you for one more year! See you in the next issue, Paulo Melo, editor in chief Hortic. bras., Brasília, v.37, n.1, January-March 2019 5

DOI - http://dx.doi.org/10.1590/S0102-053620190119 Errata We apologize for the wrong registration of author’s names, on the article cited below, published in volume 36 number 3, July to September 2018, page 408-413: LIMA, TJL; GAZAFFI, R; CECCHERINI, GJ; MARCHI, L; MARTINEZ, M; FERREIRA, CG; SALA, FC. 2018. Volume of cells on trays influences hydroponic lettuce production. Horticultura Brasileira 36: 408-413. DOI - http://dx.doi.org/10.1590/ S0102-053620180320 The following author’s names associated to DOI http://dx.doi.org/10.1590/S0102-053620180320 were incorrectly grouped: Where the names were registered as: Luana Marchi; Marcela Martinez And grouped as: Camila G Ferreira; Fernando C Sala The author's names must be individualized. 6 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Cover article ZEIST, AR; RESENDE, JTV. 2019. Strawberry breeding in Brazil: current momentum and perspectives. Horticultura Brasileira 37: 007-016. DOI - http:// dx.doi.org/10.1590/S0102-053620190101 Strawberry breeding in Brazil: current momentum and perspectives André Ricardo Zeist 1ID; Juliano Tadeu V de Resende 2ID 1Universidade do Oeste Paulista (UNOESTE), Presidente Prudente-SP, Brazil; [email protected]; 2Universidade Estadual de Londrina (UEL), Londrina-PR, Brazil; [email protected] ABSTRACT RESUMO Brazil depends almost entirely on imported strawberry cultivars, Melhoramento genético do morangueiro no Brasil: which burdens production costs and results in the use of genotypes atualidades e perspectivas with less adaptation to the Brazilian cropping conditions. To reverse this scenario, it is necessary to strengthen strawberry breeding in O Brasil depende quase que na totalidade de cultivares de Brazil. Otherwise, the country will remain dependent on imported morangueiro importadas, o que resulta em custos mais altos para os cultivars and producers will continue to be required to collect produtores e menor adaptação dos genótipos às condições brasileiras royalties. In this context, public institutions in Brazil, such as the de cultivo. Para reverter este cenário, é necessário maior enfoque State University of the Midwest Paraná (UNICENTRO), have been ao melhoramento do morangueiro no Brasil; caso contrário, o successfully conducting strawberry breeding programs, with the país continuará dependente de cultivares importadas, o que obriga objective of launching cultivars in the short term. Crosses between o pagamento de royalties. Em vista dessa situação, instituições the cultivars in use in the country, with the subsequent development públicas do Brasil, como a Universidade Estadual do Centro-Oeste and selection of seedlings, have shown to be the way to generate do Paraná, vêm conduzindo programas de melhoramento genético national genotypes better adapted to the tropical and subtropical do morangueiro com sucesso, com o objetivo de lançar cultivares climate conditions of Brazil. In this work, in addition to the main em curto prazo. Cruzamentos entre as cultivares em uso no país, com results obtained so far by the UNICENTRO strawberry breeding a posterior obtenção e seleção de seedlings, têm demonstrado ser o program, we report information on strawberry origin, taxonomy caminho para gerar genótipos nacionais mais bem adapatados às and phylogenetic description, genotype sensitivity to photoperiod, condições de clima tropical e subtropical do Brasil. Neste trabalho, breeding history in Brazil, and objectives, methods, and techniques além dos principais resultados obtidos até então pelo programa de employed by the current strawberry breeding in Brazil. melhoramento genético do morangueiro da Universidade Estadual do Centro-Oeste, são apresentadas informações referentes à origem, descrição taxonômica e filogenética, sensibilidade dos genótipos ao fotoperíodo, histórico do melhoramento genético no Brasil, objetivos do melhoramento e métodos e técnicas de melhoramento do morangueiro empregadas no Brasil. Keywords: Fragaria x ananassa, intraspecific crosses, breeding Palavras-chave: Fragaria x ananassa, cruzamentos intraespecíficos, program, review. programa de melhoramento genético, revisão. Received on November 20, 2018; accepted on March 13, 2019 Strawberry is the most cultivated and (468,248 t), Egypt (464,958 t), and of Florida. The dependence on foreign consumed small fruit in the world Turkey (415,150 t). In the same year, genetic materials and nurseries results in (Tazzo et al., 2015). Its regular use in Brazil harvested approximately 155,440 increases in the strawberry production daily meals increases the consumption tons of strawberries in 4,300 hectares, costs in Brazil (Fagherazzi et al., 2017a) of antioxidants and other substances resulting in an average yield of 36.1 t ha-1 due to expenses in the importation of important to improve human health (Fagherazzi et al., 2016b). seedlings and payment of royalties own (Andrianjaka-Camps et al., 2017; to property right agreements. In addition, Michalskaa et al., 2017). In Brazil, The main strawberry cultivars imported seedlings generally only arrive strawberries come mainly from small used in Brazil come from breeding in Brazil on the end of April, in detriment farms and there is an increasing trend in programs carried out in the United to producers of regions where climatic both the cultivated area and production States. The leading materials are conditions allow cropping seasons to in recent years (Witter et al., 2012; cultivars Oso Grande, Camarosa, begin in March. Finally, there are the Richter et al., 2018). Figures from Aromas, Diamante, Camino Real, risks associated with the possibility of 2016 (FAO, 2018) show China as the Albion, Monterey, San Andreas, introducing pathogens and pests along world largest producer, with more Palomar, and Portola, developed at the with seedlings. than 3.7 million tons, followed by the University of California; and cultivars United States (1,420,570 t), Mexico Dover, Sweet Charlie, and Florida Speeding up the Brazilian strawberry Festival, developed at the University breeding programs is the most effective Hortic. bras., v.37, n.1, January-March 2019 7

AR Zeist & JTV Resende strategy to reduce the dependence of and Russia), F. viridis and F. vesca Staudt (2009) grouped the strawberry imported cultivars. Local breeding (most common in the European gardens) species based on different ploidy would be in the position of offering (Darrow, 1966). levels (diploid, tetraploid, hexaploid, high-quality genetic material, well octoploid). adapted to the Brazilian conditions, to Strawberry cultivation gained the strawberry chain. However, most momentum in Europe from 1600 due Different ploidy levels make it of the Brazilian strawberry breeding to the introduction of two species, F. difficult to clarify the phylogeny of programs are currently stagnant or virginiana and F. chiloensis, brought from Fragaria. Federova (1946) presented the at a low pace. The development of America (Darrow, 1966; Zawadneak et first genomic formula (AABBBBCC) Brazilian cultivars may also attract al., 2013). In 1764, the botanist Antoine and, Senanayake & Bringhurst new farmers, contribute to prevent rural Nicolas Duchesne formed a strawberry (1967), the second (AAA’A’BBBB), exodus and strengthen family-based collection with specimens coming from later revised by Bringhurst (1990) farming systems. Nevertheless, the all over Europe. Such collection served (AAA’A’BBB’B). More recent studies, development of new cultivars adapted to the studies that ended up revealing based on sequences of nuclear and to the tropical and subtropical climate that the F. chiloensis plants grown in chloroplast genes and morphological of Brazil demands the commitment of Europe produced only female flowers. characteristics, suggest the genomic professionals from several sub-areas Therefore, fruit production took place formula YYY’Y’ZZZZ/YYYYZZZZ, of agronomic knowledge, once it only when F. chiloensis had neighbor in which the contribution of two to requires the assessment of tolerance to plants from other species. It was also four diploid species to the octoploid pathogens and pests and the evaluation observed that the casual cross between species is noticed. This proposition of plant morphological and productive F. chiloensis and F. virginiana resulted supports the allopolyploid origin of characteristics and fruit physicochemical in very aromatic fruits, remembering the the hexaploid F. moschata and of the traits. pineapple, which botanists denominated octoploids F. chiloensis, F. iturupensis, Fragaria x ananassa (Darrow, 1966). and F. virginiana (Rousseau-Gueutin Productivity in strawberry is This species quickly spread throughout et al., 2009). influenced mainly by the interaction Europe and, later, to the other continents. between temperature and photoperiod, The diploid sources of the octoploid soil conditions, and the incidence of The precise introduction of genome are still unclear, but F. vesca, pests and pathogens. Such a combination strawberry in Brazil is unknown. Non- F. mandshurica, and F. iinumae are makes the identification of promising official information suggests that the the most likely candidates (Hummer & materials in the early stages of the commercial-scale planting began around Hancock, 2009; Rousseau-Gueutin et breeding program into a challenge. 1950, in the states of São Paulo, Minas al., 2009; Tennessen et al., 2014). The Additional difficulties the Brazilian Gerais, and Rio Grande do Sul and octoploid genome has an estimate of strawberry breeding programs face are expanded in the following decade with 698 Mb or 80% of the quadruplicated the uneven seedling germination, the the launching of cultivar Campinas. size of the diploid genomes (* 200 Mb need to accumulate desirable traits into Darrow (1966) and Zawadneak et each) (Hirakawa et al., 2014). F. vesca single genotypes and to produce clones al. (2013) report comprehensive is the species most studied among the free from pathogens and pest arthropods. information on strawberry history, parents of the cultivated strawberry and origin, and genealogy. is also the species most used as a genetic Strawberry origin model for the Rosaceae family, as it has Strawberry cultivation started in Taxonomic description and a relatively small genome (Shulaev et Sec. XIII, in France, by transplanting phylogenetics al., 2011). wild-caught Fragaria vesca plants to gardens with ornamental purposes. Strawberry belongs to the genus Genotype sensitivity to Soon, it was realized that the fruits were Fragaria (Cronquist, 1988) along photoperiod tasty, and then the French and English with more than 45 described species. royalties strawberry started consuming However, only 20 species occur in In general, three factors influence and appreciating it (Duschesne, 1766; nature currently (Hancock et al., 2008; the most the strawberry response to Darrow, 1966). From 1500, strawberry Marodin et al., 2018). photoperiod: genotype, temperature, cultivation became increasingly popular and exposure of the seedlings to the all over Europe. The first strawberry The cultivated strawberry, Fragaria cold (Stewart & Folta, 2010). Darrow botanical illustration dates back to x ananassa, is an octoploid, with seven (1936), in his first studies on this 1485, from the Mainz Herbarium basic chromosomes (2n = 8x = 56) subject, observed that most of the Herbariuse (Germany). At the end of (Hancock et al., 2008).After several years genotypes produced more flowers under the 18th century, the literature on botany of study, Staudt (2009) systematized photoperiods ranging from 9.5 to 13.5 and natural sciences already included four important characteristics to the hours, considering 12 hours as optimal. several strawberry species, such as F. strawberry taxonomic classification: However, recent studies showed that moschata (most common in England number of chromosomes; stolon the most abundant flowering occurs branching; sexual expression and other in photoperiods ranging between 8 8 crossing mechanisms, and pollen grain and 12 hours (Stewart & Folta, 2010). morphology. Using these characteristics, Hortic. bras., Brasília, v.37, n.1, January-March 2019

Strawberry breeding in Brazil: current momentum and perspectives According to Darrow (1966), the used in Brazil are Aroma, Diamond, released national genotypes capable of first cultivated octoploid genotypes Pacific, Selva, Seascape, Albion, competing in yield with the imported flowered under short days, although Portola, Monterey, and San Andreas. cultivars, widely used in Brazil. there was considerable variation in Currently, Brazilian farmers prefer these the sensitiveness to the photoperiod cultivars. However, considering the Breeding objectives and in the required number of hours of Brazilian edaphoclimatic variability, it light. As breeding programs advanced is imperative that the local strawberry The success of a strawberry breeding and hybridizations were carried out, breeding develop both short- and program depends on a number of as well as more detailed studies neutral-day cultivars. factors, and the definition of objectives appeared, genotypes setting flowers and goals is fundamental for saving time with photoperiods of up to 14 hours Strawberry breeding in Brazil and resources. In general, strawberry were also considered as of short days breeding programs should pursue (Faedi et al., 2002). Strawberry breeding had its first meeting the demands, from farmers to impulse in England in the early XVIII consumers, and keeping updated with the Although floral induction requires century, expanding to France, Germany, constant changes in production systems. short photoperiods, if short days persist, and the United States later (Zawadneak To develop new strawberry genotypes they may delay the development of the et al., 2013). In Brazil, the Agronomic with high agronomic performance and previously initiated buds if compared to Institute of Campinas (IAC) was the nutritional quality of fruits is a laborious longer photoperiods (Durner & Poling, pioneer in strawberry breeding, starting and complex process (Mezzetti et al., 1987). Therefore, strawberries are short- in 1941, followed by the Experimental 2018). day plants for floral induction, but long- Station of Pelotas, now Embrapa Clima day for flower and fruit development. Temperado, in 1950. These programs Several objectives of the Brazilian Examples of short-day cultivars planted developed and used several materials strawberry breeding programs are in Brazil are Milsey Tudla, Cartuno, obtained from the importation of common to any crop, such as increased Sweet Charlie, Big Bear, Camarosa, seedlings and achenes from breeding productivity in local conditions and Gaviota, Ventana, and Camino Real. programs in the United States. resistance to pests and diseases. However, there are some characteristics There are also strawberry plants The Brazilian breeding programs that are almost specific to strawberries, with no sensitivity to photoperiod. were decisive to increase strawberry such as fruit color, reduced number of F. virginiana subsp. glauca, which productivity and importance in the runners, and a few canopy traits, among flowers in summer and autumn, was country. The IAC program launched others. Brazilian strawberry breeding the first species in which researchers the cultivars Campinas (IAC 2712), programs should tackle the following observed this behavior (Darrow, 1966). Guarani (IAC 5074), Monte Alegre aspects to develop genotypes able to Breeding programs evaluated and (IAC 3113), and Princesa Isabel (IAC exceed or to perform as good as the incorporated a large number of F. 5277); while Embrapa’s launched Santa imported cultivars: virginiana subsp. glauca genotypes Clara, Konvoy-Cascata, and Vila Nova in the 1930s and 1940s. The greatest (Oliveira & Bonow, 2012). However, 1. To increase or maintain crop yields impact of F. virginiana subsp. glauca from the 1990s, improved cultivars to guarantee farmers’ profitability; over strawberry breeding occurred developed by foreign programs were in the 1970s, at the University of successfully introduced in the Brazilian 2. To incorporate or increase the California, when researchers used a producing regions and replaced the level of resistance/tolerance to pests single accession of the species from the national cultivars planted at that time. and pathogens to reduce the need Wasatch Mountains in Utah to introgress for spraying protection products and the flowering habit into the cultivars then Currently, the cultivars most decrease quantitative and qualitative in use (Bringhurst & Voth, 1984). The used in Brazil come from American losses in the field and post-harvest; strawberries derived from this single breeding programs, which implies source constituted the majority of the great dependence and vulnerability to 3. To increase plant adaptation to cultivars planted in California in 1999, the local strawberry chain (Fagherazzi the Brazilian tropical and subtropical called neutral day cultivars (Hancock et al., 2017a,b). In recent years, a few conditions, as well as to different soil et al., 2005; 2008). The characteristic Brazilian institutions, such as Embrapa types and cropping systems; had a simple and dominant inheritance Clima Temperado, the State University in this case and was incorporated with of Santa Catarina, the Federal University 4. To incorporate into cultivars only three backcrosses (Bringhurst & of Lavras, the State University of characteristics to make harvests easier, Voth, 1978). Midwest Paraná, the State University like fruit production far from the center of Londrina, and the University of of the canopy; Neutral-day cultivars are more Oeste Paulista (the last two, from 2019) tolerant to heat and have longer started developing new strawberry 5. To increase the water and nutrient harvesting periods, but are more difficult genotypes, well adapted to the Brazilian uptake and use efficiency and to to propagate and develop fewer runners. soil and climatic conditions. However, introgress genes of tolerance to abiotic Examples of neutral-day cultivars so far the Brazilian programs have not stresses; Hortic. bras., Brasília, v.37, n.1, January-March 2019 6. To extend the cropping season to the summer (neutral day cultivars) to allow for harvesting in unusual periods 9

AR Zeist & JTV Resende with added-value; the 80’s from the cross between cultivars (Marodin et al., 2018). Several Germany and Jundiaí, Princesa Isabel populations of F. chiloensis from United 7. To improve fruit sensorial has good productive characteristics, States and Chile have large fruits, which acceptance, which is dependent on good such as high yield, earliness, and large makes it easier to bred materials with physical-chemical quality, especially fruits (Castro et al., 2003). Currently, large fruits and high yielding potential, intense red color and high contents of the imported cultivars outyield those or even high production of crowns and soluble solids and aromatic volatiles; developed by the Brazilian breeding runners (Hancock et al., 2005; Luby et programs. al., 2008). Therefore, an alternative to 8. To produce uniform fruits, the success of the Brazilian breeding preferably above 20 grams, to reduce The Center for Agronomic Sciences programs may be the introduction of F. labor costs and increase consumers’ of the State University of Santa chiloensis genotypes as donor parents acceptability; Catarina (CAV-UDESC) introduced 15 for gains in fruit size. strawberry genotypes from Italy in 2013 9. To increase fruit firmness to reduce (Fagherazzi et al., 2017a). Cultivars Resistance and tolerance to damage during harvesting, packaging, Jonica [obtained from the natural pathogens distribution, and commercialization; pollination of cultivars Rosalinda x Demetra (Irvine x Tudla)] and Pircinque Pathogens pose challenges to 10. To improve the fruit nutritional (obtained from the cross between strawberry production worldwide, quality, which should be relatively cultivars Ventana x Nora) still stand resulting in increased costs due to yield stable despite the edaphic conditions out, yielding more than 500 g plant-1. losses and to the need for spraying and climatic zones, that must have a However, these two cultivars, along protection products. Strawberry significant impact on human health; with all those widely cultivated today cultivars with some level of multiple in Brazil, do not have a genetic base resistances to pathogens could contribute 11. To develop cultivars that meet directed to the Brazilian soil and climatic significantly to mitigate difficulties the requirements of both the fresh conditions. Recent studies show that the (Nellist, 2018). Therefore, breeding for and processing markets, with fruits hybridization of different strawberry disease resistance has a high priority displaying physical and chemical genotypes followed by local selection, in many breeding programs worldwide characteristics peculiar to each segment, as the pioneer Brazilian strawberry (Kennedy et al., 2013, Pincot et al., and; breeding programs did (Camargo et al., 2018; Nellist, 2018). 1968), may result in the development 12. To address global issues of more productive and better-adapted In Brazil, the main diseases affecting related to the environment, agriculture cultivars (Barth, 2017, Galvão et al., strawberry are fungi: anthracnosis sustainability, food safety, and quality, 2017, Vieira et al., 2017). (Colletotrichum gloeosporioides, C. which are all challenging aspects to fragariae and C. acutatum), common strawberry breeding in Brazil and Crosses between cultivars Camarosa leaf spot (Mycosphaerella fragariae), elsewhere. and Aromas resulted in high yielding leaf scorch (Diplocarpon earliana), hybrids, with large fruits, meeting leaf blight (Dendrophoma obscurans), Productivity commercial standards in the south of crown rot (Pestalotiopsis sp.), powdery Minas Gerais state (Galvão et al., 2017). mildew (Sphaerotheca macularis), The productive potential of a In addition, crosses Dover x Aromas Verticillium wilt (Verticillium dahliae), strawberry genotype depends on the and Camarosa x Aromas resulted in root rot (Rhizoctonia spp., Fusarium size and number of fruits. The ideal 28.6% hybrids with total fruit mass sp., Sclerotium rolfsii, Phytophthora cultivar should produce large fruits, superior to Aromas, and 9.5 and 14.3% spp.), red stele (Phytophthora spp), in shapes that meet the consumers’ hybrids superior to cultivar Camarosa, Rhizoctonia rot (Rhizoctonia spp.), requirements. Large fruit is the recessive respectively (Galvão et al., 2017). In the mold-gray (Botrytis cinerea), and phenotype (quantitative genes) in most screening of populations in Guarapuava, Rhizopus rot (Rhizopus spp.). Some cultivars currently used in Brazil. The Paraná state, hybrids from the cross bacterial diseases, such as the leaf number of crowns per area has also between cultivars Camarosa and Aromas spot (Xanthomonas fragariae) and been associated with yield (Cocco et also stood out in terms of yield (Barth, viruses, such as Strawberry mottle al., 2011). However, the genetics behind 2017). Thus, cultivars Camarosa and virus, Strawberry crinkle virus, and the number of crowns per area has not Aromas bear a high concentration of Strawberry mild yellow edge virus received much attention. favorable genes for breeding strawberry (Antunes et al., 2016), are also relevant. for high productivity under the Brazilian Strawberry yields in Brazil increased soil and climatic conditions. One of the main reasons for the low after the release of cultivar Campinas, level of resistance of the cultivars used from IAC, in 1955 (Castro et al., There are two main ways to increase in Brazil to a large number of pathogens 2003). Cultivar Campinas resulted from productivity through plant genetics and is the narrowing of the genetic basis to crossing the North American cultivars physiology: to increase the efficiency privilege production characteristics. Donner and Tahoe (Camargo et al., of photoassimilate production of or Until then, strawberry breeding has been 1968) and was the leading strawberry to change the dry matter partitioning carried out in several countries, paying cultivar in the main Brazilian producing states for more than 30 years. Cultivar Hortic. bras., Brasília, v.37, n.1, January-March 2019 Princesa Isabel is another Brazilian material that stands out. Launched in 10

Strawberry breeding in Brazil: current momentum and perspectives special attention to the increase in fruit (Qin et al., 2008; Luby & Shaw, 2009). value of the human diet by incorporating number and size (Mezzetti et al., 2018). However, the nutritional value and the into it many nutritional and bioactive In addition, the genetic development antioxidant properties are becoming compounds, such as minerals, vitamin of the foreign cultivars obviously did increasingly relevant, as health concerns C, folate, and phenolic substances not consider the variability of the local are gaining ground (Singh et al., 2011; (Giampieri et al., 2012). This aspect pathogens. As an example, the imported Mezzetti et al., 2016). supports the increase in the number of cultivars are all susceptible to the crown fruit characteristics one should look at anthracnosis (C. fragariae) and to the Pulp firmness and resistance to when breeding strawberries for benefits fruit black spot (C. acutatum) (Oliveira mechanical damage are key aspects on human health (Mezzetti et al., 2016; & Antunes, 2016), except for cultivar for the strawberry breeding. The 2018). Fruit quality should be always Sweet Charlie. The hybridization ideal fruits have the least possible as important as yield and resistance to between imported cultivars (highly damage during handling and transport, pathogens in strawberry breeding. productive) and local genotypes (better preserving their organoleptic qualities adapted) is an interesting approach to for the longest period. The University Classical breeding methods, as develop new genotypes well adapted to of California (UC) breeding program well as molecular-assisted breeding, the pathogenic and productive Brazilian gained more than 47% in fruit firmness are effective in increasing the contents soil and climatic conditions. Local and appearance. Even then, there is of specific bioactive compounds genotypes can be Creole varieties and hypothetically more variability still (Giampieri et al., 2018) and may cultivars developed decades ago by the available for these characteristics (Shaw result in substantial advances in the breeding programs of IAC and Embrapa. & Larson, 2008). years to come. The environmental and crop management influence over The genetic resistance to pathogens The inheritance of the intensity of fruit chemical properties and firmness can be lost after a few years of growing fruit color is partially dominant and, and other agronomic components resistant plants in the field (Nellist, according to Santos (1999), shows are also relevant (Fan et al., 2011). 2018). In general, resistance durability heritability around 81%. However, the Therefore, one should never leave depends on the virulence pressure of a genetic correlation between internal behind the importance of the genotype x pathogen under cropping conditions, and external color is low, indicating environment interaction when breeding the genetic diversity of pathogenic that different genes control these strawberries (Gabriel et al., 2018), isolates, and the possible changes in characteristics (Marodin et al., 2018). especially considering the demand for pathogenicity that may occur over Nonetheless, classical breeding methods genotypes well adapted to the diversity time. Pyramiding or stacking resistance are effective to achieve the ideal internal of Brazilian soil and climatic conditions. genes in a single cultivar, including, red and external dark red. when available, both major and minor Methods and techniques of genes, with greater and smaller effect, Taste and aroma result from the strawberry breeding used in Brazil respectively, and even stacking genes association of several factors, such as of smaller selection impact (Poland the presence of soluble acids and solids, In strawberries, breeders can exploit & Rutkoski, 2016), can result in for example. Aroma has quantitative all the genetic variance produced in a durable resistance. The combination of inheritance and 41% heritability cross, be it additive, dominant or epistatic, lower- and higher- or mid-effect genes (Santos, 1999). The inheritance of the since strawberries allow asexual (clonal) has already shown to be effective in chemical characteristics affecting taste reproduction. Nevertheless, parents increasing genetic resistance (Brun et is not well elucidated yet (Whitaker should have good genetic divergence to al., 2010). et al., 2011). However, Sone et al. avoid inbreeding, which often results in (2003) concluded that the inheritance vigor loss and a decrease in productivity The use of molecular markers and of vitamin C contents is quantitative, (Gil-Ariza et al., 2009; Galvão et al., genomic studies to track large number although they also observed partial 2017). Hybridization between cultivars of genes tend to increase the efficiency dominance in some progenies of crosses is the predominant strawberry breeding of breeding programs (Shiraev et al., within F. x ananassa. Singh et al. (2011), method in Brazil (Camargo et al., 1968; 2011; Hirakawa et al., 2014; Whitaker et working with cultivars Ofra, Chandler, Galvão et al., 2017), resulting in the al., 2017). However, gene pyramidation Festival, and Camarosa, observed high development of genotypes with high is still a time-consuming process that heritability (80%) for ascorbic acid performance for the desired phenotypic involves multiple crosses when it and carotenoid contents and positive characteristics. After the crosses, comes to the resistance to strawberry correlation of phenol content and thousands of genotypes, represented pathogens. contents of ascorbic acid, carotenoid by one or two plants originating from and anthocyanin, and even with yield. seedlings or runners from the mother Fruit quality Thus, phenol contents may be effective plant are grown, in general, in the as biochemical markers to identify high- augmented blocks design, and screened. Pulp firmness and resistance to yielding genotypes that simultaneously Genotypes selected in this first step are damage and fruit color, flavor, shape, contain high levels of antioxidants. usually cloned and reassessed, now aroma, and texture are the main traits in complete blocks at random, with related to fruit quality in strawberry Strawberry fruits play an important role in strengthening the nutritional 11 Hortic. bras., Brasília, v.37, n.1, January-March 2019

AR Zeist & JTV Resende an adequate number of replications and crosses are easily carried out in the and the pericarp are impermeable to (at least two blocks) and plants per field or in the greenhouse. Open flowers water. Therefore, dormancy-breaking plot (approximately ten plants). Those in the male parent are collected in the treatments should precede sowing. genotypes that confirm their potential in field in the morning and packaged in There are several methods to break the this second step pass to a new cloning paper bags. If they do not release enough dormancy. Seed immersion in sulfuric and evaluation stage, now in multi-year pollen, flowers are heated with an acid for 35 to 40 minutes has been and multi-environmental trials to assess incandescent lamp to given temperature showing satisfactory germination results adaptability and stability. In this third limits (28 to 30oC), so that anther (Galvão et al., 2014). stage, each genotype is represented by dehiscence occurs. Flower emasculation at least 40 plants divided into several in the female parent is carried out using Approximately two months after plots (Marodin et al., 2018). The results tweezers to remove stamens, chalice, achene germination, preferably in of this last stage define the final selection and corolla in a single operation. This air-conditioned chambers, seedlings of the superior genotypes to be released procedure must be carried out with present two to three true leaves. At to the market (Chandler et al., 2012; extreme care, so as not to damage the this stage, seedlings are transplanted Zawadneak et al., 2013). Alternatively, pistil. To perform the artificial cross, the to containers containing substrate the selected hybrids can undergo further pollen-donor flowers are agitated over and transferred to greenhouses, with and successive crosses to increase the the pistil of the female parent’s flower, controlled temperature and humidity frequency of favorable alleles. so that stamens softly touch the stigma. for acclimatization. After 75-day In general, to each pollen-recipient acclimatization, plants can be vernalized It is also possible to carry out self- flower, a dehiscent flower is used. After (30 days at 2 to 3oC) and then planted crosses for two to three generations, artificial pollination, the pollinated and evaluated in experimental trials, followed by crossing the best progenies flower is identified and, if necessary, according to the objectives of the to restore vigor and productivity, protected to avoid damage from insect- breeding program. exploring the specific combining ability pests or birds. (Marodin et al., 2018). The method may Background and status of the be useful, although the resulting hybrids Strawberries obtained from crosses strawberry breeding program of are seldom better than those obtained by should be harvested as they reach the the State University of the Midwest crossing cultivars. growth and development peak. After Paraná (UNICENTRO) harvesting, fruits are crushed and sieved Traditional breeding has already and the viable seeds are separated from In the last ten years, UNICENTRO achieved many significant results the pulp, washed and placed to dry in has been developing research with for several strawberry agronomic an oven with air circulation at 28oC. strawberries. From 2013, UNICENTRO characteristics (Mezzetti et al., 2018). Upon drying, achenes are transferred to began to carry out strawberry breeding However, classic breeding is laborious sterilized containers and stored in cold in an intensive way, aiming to obtain and time-consuming. The genetic conditions, at 4oC. Strawberry achenes cultivars with high yielding potential transformation of strawberries has have physical dormancy, once the testa and good postharvest and sanitary observed major advances since the characteristics, superior to the cultivars first transgenic strawberry appeared in 1990 (Marodin et al., 2018). Therefore, Table 1. Genealogy of twelve hybrid populations generated by crossing seven Fragaria x genetic engineering and biotechnology ananassa cultivars. Guarapuava, UNICENTRO, 2019. are alternatives to classic breeding, as they offer the possibility of introducing Population Parent Population Parent a single or a few genes controlling 1 ♀♂ 7 heterozygous traits directly into the Dover Aromas ♀♂ strawberry genome, resulting in the development of new improved materials Sweet Aromas faster than traditional breeding (Qin et al., 2008; Whitaker et al., 2017; Charlie Mezzetti et al., 2018). 2 Oso Aromas 8 Milsei Tudla Aromas Crossing techniques The crossing techniques used to breed Grande strawberries vary among institutions. Here, we describe the main procedures 3 Camarosa Aromas 9 Milsei Tudla Sweet adopted by the Strawberry Breeding Charlie Program of the State University of the 4 Dover Sweet 10 Camarosa Sweet Midwest Paraná (UNICENTRO). Charlie 11 Charlie 12 Festival Aromas The strawberry floral structure does 5 Oso Milsei Flórida not pose difficulties to hybridization, Grande Tudla Oso Grande Sweet Charlie 12 6 Festival Sweet Flórida Charlie Note: ♀= female parent; ♂= male parent. Hortic. bras., Brasília, v.37, n.1, January-March 2019

Strawberry breeding in Brazil: current momentum and perspectives planted today in Brazil. genetic characteristics, and helped in the phytosanitary characteristics, such Prior to the effective start of the selection of elite hybrids. The studies of as correlation matrices; genotypic, Morales et al. (2011,2012) oriented the phenotypic and residual variance and breeding program, Morales et al. mating combinations used in breeding, covariance; contrasts among hybrids; (2011) studied the morpho-agronomic resulting in 12 hybrid populations heritability and genetic variation and molecular divergence of the obtained out of crosses involving seven coefficients, and expected selection germplasm available at UNICENTRO. cultivars (Table 1). gains (%) for the selected hybrids in Eleven cultivars were assessed and relation to the set of hybrids. low similarities were found between Following the crosses, achenes cultivars Dover and Oso Grande (24%), were germinated according to Galvão Selecting promising materials often Dover and Milsei Tudla (24%), Dover et al. (2014) and transferred to in vitro becomes a challenge for the breeder and Sweet Charlie (24%), Dover and cultivation. After 60 days, seedlings in the early stages of the program. Camarosa (29%), and Milsei Tudla were acclimatized and transplanted to Depending on the adopted method, the and Oso Grande (33%), thus revealing the field in augmented block design. number of individuals and characteristics potential for future crosses and for Augmented blocks allow evaluation evaluated is very large, which makes it broadening the genetic base. This without replication. In addition, the impossible to perform comparative genetic information had key importance object of the work is actually the tests among all individuals. As a result, in the planning, execution, and success F1 generation. The controls were three models of selection indexes were of the breeding program, since it cultivars Camarosa and Camino Real, proposed to improve the efficiency allowed defining the best strategies the leading cultivars in Paraná. The of selecting several characteristics to use the germplasm, guided the genetic parameters were estimated simultaneously, thus establishing choice of parents with interesting based on agronomic, post-harvest, and an optimal combination of several characters (Cruz et al., 2014). The rank Table 2. Fragaria x ananassa hybrids selected using the selection indices of Smith (1936) sum index (Mulamba & Mock, 1978) and Hazel (1943); Mulamba & Mock (1978); and Genotype/Ideotype, with economic was used to hierarchize the hybrids for weights established for the selection according to fruit suitability to fresh consumption or each characteristic by assigning higher to processing. Guarapuava, UNICENTRO, 2019. absolute values to those with the best performances. The classic index (Smith, Fresh Market Processing 1936; Hazel, 1943) consists of the linear combination of the phenotypic Ranking Hazel & Mulamba Genotype/ Hazel & Mulamba Genotype/ values of the various economically important characters, with weighting Smith & Mock Ideotype Smith & Mock Ideotype coefficients estimated to maximize the correlation between selection 1 DA04 CS10 CS04 DA04 CS04 CS04 indexes and genotypic aggregate (Cruz et al., 2014). Finally, the genotype- 2 CS10 CS04 CS09 CS10 CS11 CS01 ideotype distance index estimates the distance between evaluated hybrids 3 CS04 CS11 CS07 CS04 CS10 CS07 and an ideotype previously defined by the breeder. These indexes revealed 4 OT22 CS09 CS11 OT22 CS09 TA16 the best hybrids and the selection gains were calculated for them. Barth 5 CA06 FA16 CS10 CA06 TA09 SA15 (2017) applied the selection indexes, distinguishing genotypes intended to 6 CS07 OT21 FA04 CS07 SA15 CS09 fresh consumption of those intended to processing by means of attributing 7 DA11 CS07 CS01 DA11 CA14 SA14 different weights to the characteristics of greater interest to one or another 8 FSC07 CA16 OT21 FSC07 TA16 DA01 purpose. The weights ranged from one (less relevant) to five (more relevant). 9 CA16 TS08 CA06 CA16 CS07 OT22 At first, we used the three selection 10 CS11 CA14 DA01 CS11 CS13 CS06 indexes individually to select the best- ranked hybrids, taking into account 11 OT21 DA01 OT22 FA14 SA12 SA12 their suitability. We selected 2% of the total hybrids produced or 20 hybrids per 12 FA14 TA12 TA12 CS09 CS01 CS13 index, ranked according to the purpose (Table 2). As there was variation 13 SA08 FA04 CA16 OT21 TA07 TA09 among indexes in hybrid ranking, we 14 CS09 CA06 FA16 SA08 TA12 CS11 13 15 FA02 FA14 SA14 CS01 CA06 CS10 16 FA04 TA20 TS08 FA02 TS08 TA12 17 DA01 FA02 FA14 FA04 SA14 CA06 18 TA16 TA09 FSC07 DA01 SA06 SA06 19 CS01 DA04 TA16 TA16 TA05 CA14 20 FA16 SA14 DA11 FA16 DA01 TS08 DA= Dover x Aromas; CS= Camarosa x Sweet Charlie; OT= Oso Grande x Milsei Tudla; CA= Camarosa x Aromas; FS= Festival Flórida x Sweet Charlie; FA= Festival Flórida x Aromas; SA = Sweet Charlie x Aromas; TA= Milsei Tudla x Aromas; TS= Milsei Tudla x Sweet Charlie. Hortic. bras., Brasília, v.37, n.1, January-March 2019

AR Zeist & JTV Resende Table 3. Male and female parents used in the strawberry breeding at UNICENTRO and their Brazilian strawberry cultivars is to join respective number of seedlings. Guarapuava, UNICENTRO, 2018. efforts towards the breeding work. At the same time, the emergence of new Female Parent (♀) Male Parent (♂) Seedlings breeding programs, especially in nascent strawberry producing regions, may Camino Real FVFS07 (Festival x Aromas) 227 contribute to boosting the crop in Brazil. It is vital that the breeding programs Camino Real FS06 (Festival x Aromas) 230 involve professionals from different areas of plant and food science and Camino Real CA 16 (Camarosa x Aromas) 118 technology, to allow for the screening of multiple characteristics. In addition Camino Real DA 11 (Dover x Aromas) 201 to productivity, genotypes should possess resistance to pathogens and Camino Real CS04 (Camarosa x Sweet Charlie) 169 pest-arthropods and tolerance to abiotic factors (such as high temperatures). Camarosa DA 11 (Dover x Aromas) 07 The fruit physicochemical quality is also a challenge, considering that it Camarosa FVFS07 (Festival x Aromas) 25 is necessary to meet consumer’s high expectancies. Camarosa FS06 (Festival x Aromas) 15 Strawberry clones suitable for Albion FVFS07 (Festival x Aromas) 152 the fresh market and/or processing developed in Brazil are likely to be very Albion FS06 (Festival x Aromas) 191 promising in increasing the production of this small fruit in Brazil. These Monterey FVFS07 (Festival x Aromas) 229 genotypes will allow reducing the dependence on imported plant-matrices, Monterey CA 16 (Camarosa x Aromas) 18 a component that has systematically burned production costs for farmers. Total 1582 It is also fair to expect these genotypes will outyield the imported cultivars, as ended up with more than the expected used as controls (Table 3). Agronomic they will have been developed under twenty hybrids that should result from and post-harvest characteristics and tropical and subtropical climate and a 2% selection pressure. In a second response to photoperiod drove the soil, thus presenting better adaptation moment, we took seven hybrids using screening. The second-generation to the Brazilian conditions. The next simultaneously the three indexes for hybrids are expected to be assessed in step is introducing genes from ancient the two purposes, therefore, hybrids trials in several regions of Brazil with Brazilian cultivars such as Campinas, with dual aptitude: CS10, CS04, CS09, the purpose of launching short- and Guarani, Convoy Cascata, Princesa CS11, CS07, CingA06, and DA01. neutral-day productive cultivars, with Isabel, and Vila Nova, to broaden the The hybrid CS04 is the outstanding good post-harvest traits for both fresh germplasm genetic variability and genotype, since it performed better in and industrial purposes in the short- generate more promising segregating all indexes, ranking among the top three term. The best hybrids will be used populations as far as attributes of interest for both aptitudes. Hybrids CS10 and also as parents in the breeding program, are concerned. CA16, for consumption and processing, in intra- and inter-specific crosses, to respectively, also have good chances further increase the expression of the REFERENCES of advancing in the program (Table 2). genetic variability of the species. ANDRIANJAKA-CAMPS, ZN; HERITIER, J; In 2017, we used some hybrids Final considerations and ANÇAY, A; ANDLAUER, W; CARLEN, [CA 16 (Camarosa x Aromas), FS07 perspectives C. 2017. Evolution of the taste-related and (Festival x Aromas), DA 11 (Dover x bioactive compound profiles of the external Aromas), FS06 (Festival x Aromas), The short- and neutral-day and internal tissues of strawberry fruits and CS04 (Sweet Charlie x Camarosa)] strawberry cultivars appropriate for (Fragaria x ananassa) cv. ‘Clery’ during selected in the first generation as male fresh consumption and/or processing ripening. Journal of Berry Research 7: 11-22. parents (pollen donors) in crosses currently available to Brazilian farmers with cultivars with good phenotypic are genotypes developed by foreign ANTUNES, LEC; REISSER JUNIOR, C; adaptability to the local edaphoclimatic breeding programs and do not express SCHWENGBER, JE (org). 2016. conditions: Albion and Monterey the best possible adaptation to the Morangueiro. Brasília: Embrapa, 2016. 589p. (neutral-days) and Camino Real and Brazilian soil and climatic conditions. Camarosa (short-days). The idea here In Brazil, there are very few strawberry BARTH, E. 2017. Aptidão de híbridos is to build segregating populations with breeding initiatives. Therefore, actions to experimentais de morangueiro obtidos a partir characteristics of neutral and short days. support the national breeding programs de cruzamentos intraespecífico. Guarapuava: will greatly contribute to strengthening Crosses were performed and the strawberry chain in the country. seedlings were produced as described earlier. Seedlings were acclimated, Strawberry breeding in Brazil would vernalized in a cold chamber and, in 2018, profit from close cooperation among transplanted to beds in augmented block institutions. The way to overcome design. Cultivars Albion, Monterey, the scarcity of human resources and Camino Real, and Camarosa were increase chances of launching promising 14 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Strawberry breeding in Brazil: current momentum and perspectives Universidade Estadual do Centro-Oeste. 91p. 167-170. Temperate fruit crop breeding. New York: (M.Sc. Thesis) Springer, p.455. FAGHERAZZI, AF; GRIMALDI, F; BRINGHURST, RS. 1990. Cytogenetics and KRETZSCHMAR, AA; MOLINA, AR; HAZEL, LN. 1943. The genetic basis for evolution in American Fragaria. Hortscience GONÇALVES, MA; ANTUNES, LEC; constructing selection indexes. Genetics 28: 25: 879-881. B A R U Z Z I , G ; R U FATO , L . 2 0 1 7 b . 476-490. Strawberry production progress in Brazil. BRINGHURST, RS; VOTH, V. 1984. Breeding Acta Horticulturae 1156: 937-940. HIRAKAWA, H; SHIRASAWA, K; KOSUGI, S; octoploid strawberries. Iowa State Journal of TASHIRO, K; NAKAYAMA, S; YAMADA, Research 58: 371-381. FAN, L; YU, C; FANG, C; ZHANG, M; M ; K O H A R A , M ; WATA N A B E , A ; RANIERI, M; DUBÉ, C; KHANIZADEH, KISHIDA, Y; FUJISHIRO, T; TSURUOKA, BRINGHURST, RS; VOTH, V. 1978. Origin and S. 2011. The effect of three production systems H; MINAMI, C; SASAMOTO, S; KATO, evolutionary potentiality of the day-neutral on the postharvest quality and phytochemical M; NANRI, K; KOMAKI, A; YANAGI, trait in octoploid Fragaria. Genetics 90: 510. composition of Orléans strawberry. Canadian T; GUOXIN, Q; MAEDA, F; ISHIKAWA, Journal of Plant Science 91: 403-409. M; KUHARA, S; SATO, S; TABATA, S; BRUN, H; CHÈVRE, AM; FITT, BD; POWERS, ISOBE, SN. 2014. Dissection of the octoploid S; BESNARD, AL; ERMEL, M; HUTEAU, FOOD AND AGRICULTURAL strawberry genome by deep sequencing of the V; MARQUER, B; EBER, F; RENARD, M; ORGANIZATION. FAOSTAT. 2018. Available genomes of Fragaria species. DNA Research ANDRIVON, D. 2010. Quantitative resistance at <http://www.fao.org/faostat>. Accessed on 21: 169-181. increases the durability of qualitative resistance February 22, 2019. to Leptosphaeria maculans in Brassica napus. HUMMER, K; HANCOCK, J. 2009. Strawberry New Phytologist 185: 285-299. FEDEROVA, NJ. 1946. Crossability and genomics: botanical history, cultivation, phylogenetic relations in the main European traditional breeding, and new technologies. In: CAMARGO, LS; ALVES, S; SCARANARI, H; species of Fragaria. Compte-rendu de I’ FOLTA, KM; GARDINER, SE (eds). Genetics ABRAMIDES, E. 1968. Novos cultivares Academie des Sciences de I’URSS 52: 545- and genomics of Rosaceae, plant genetics and de morangueiro para a região do «Alto 547. genomics: crops and models 6. Springer. New Piracicaba», no Planalto Paulista. Bragantia York. p.413-436. 27: 117-133. GABRIEL, A; RESENDE, JTV; ZEIST, AR; RESENDE, LV; RESENDE, NCV; GALVÃO, KENNEDY, C; HASING, TN; PERES, NA; CASTRO, RL; CASALI, VWD; BARRELLA, AG; ZEIST, RA; LIMA FILHO, RB; WHITAKER, VM. 2013. Evaluation of TP; SANTOS, RHS; CRUZ, CD. 2003. CORRÊA, JVW; CAMARGO, CK. 2018. strawberry species and cultivars for powdery Produtividade de cultivares de morangueiro Phenotypic stability of strawberry cultivars mildew resistance in open-field and high em sistema de cultivo orgânico. Horticultura assessed in three environments. Genetics and tunnel production systems. Hortscience 48: Brasileira 21: 227-230. Molecular Research 17: 01-11. 1125-1129. CHANDLER, CK; FOLTA, K; DALE, A; GALVÃO, AG; RESENDE, LV; GUIMARAES, LUBY, JJ; HANCOCK, JF; DALE, A; SERCE, WHITAKER, VM; HERRINGTON, M. 2012. RM; FERRAZ, AKL; MORALES, RGF; S. 2008. Reconstructing Fragaria x ananassa Strawberry. In: BADENES, ML; BYRNE, MARODIN, JC; CATÃO, HCRN. 2014. utilizing wild F. virginiana and F. chiloensis: DH (ed). Fruitbreeding. New York: Springer. Overcoming strawberry achene dormancy inheritance of winter injury, photoperiod p.305-325. for improved seedling production in breeding sensitivity, fruit size, female fertility and programs. Idesia 32: 57-62. disease resistance in hybrid progenies. COCCO, C; ANDRIOLO, JL; CARDOSO, FL; Euphytica 163: 57-65. ERPEN, L; SCHMITT, OJ. 2011. Crown size GALVÃO, AG; RESENDE, LV; MALUF, and transplant type on the strawberry yield. WR; RESENDE, JTV; FERRAZ, AKL; LUBY, JJ; SHAW, DV. 2009. Plant breeders’ Scientia Agricola 68: 489-493. MARODIN, JC. 2017. Breeding new improved perspectives on improving yield and quality clones for strawberry production in Brazil. traits in horticultural food crops. Hortscience CRONQUIST, A. 1988. The evolution and Acta Scientiarum. Agronomy 39: 149-155. 44: 20-22. classification of flowering plants. Bronx: The New York Botanical Garden. 555p. GIAMPIERI, F; TULIPANI, S; ALVAREZ- MARODIN, JC; RESENDE, JTV; GALVÃO, SUAREZ, JM; QUILES, JL; MEZZETTI, AG; RESENDE, LV; RESENDE, NCV; CRUZ, CD; CARNEIRO, PCS; REGAZZI, B; BATTINO, M. 2012. The strawberry: ZEIST, AR. 2018. Melhoramento genético AJ. 2014. Modelos biométricos aplicados Composition, nutritional quality, and impact do morangueiro. In: RAMPIM, L; SANTOS, ao melhoramento genético. Viçosa: Editora on human health. Nutrition 28: 09-19. LA; GAVA, E; SPLIETHOFF, J (eds). Tópicos UFV. 668p. avançados em produção vegetal. Guarapuava: GIAMPIERI, F; GASPARRINI, M; FORBES- Apprehendere, p.47-72. DARROW, GM. 1936. Interrelation of temperature HERNANDEZ, TY; MAZZONI, L; and photoperiodism in the production of fruit- CAPOCASA, F; SABBADINI, S; ALVAREZ- MEZZETTI, B; BALDUCCI, F; CAPOCASA, buds and runners in the strawberry. Proceeding SUAREZ, JM; AFRIN, S; ROSATI, C; F; ZHONG, CF; CAPPELLETTI, R; DI of the American Society for Horticultural PANDOLFINI, T; MOLESINI, B; SÁNCHEZ- VITTORI, L; MAZZONI, L; GIAMPIERI, Science 34: 360-363. SEVILLA, JF; AMAYA, I; MEZZETTI, B; F; BATTINO, M. 2016. Breeding strawberry BATTINO, M. 2018. Overexpression of the for higher phytochemicals content and claim DARROW, GM. 1966. Holt, Rinehart and anthocyanidin synthase gene in strawberry it: is it possible? International Journal of Fruit Winston: the strawberry history breeding and enhances antioxidant capacity and cytotoxic Science 16: 194-206. physiology. New York: The New England effects on human hepatic cancer cells. Journal Institute for Medical Research. 447p. of Agricultural and Food Chemistry 66: MEZZETTI, B; GIAMPIERI, F; ZHANG, Y; 581-592. ZHONG, C. 2018. Status of strawberry DURNER, EF; POLING, B. 1987. Flower bud breeding programs and cultivation systems in induction, initiation, differentiation and GIL-ARIZA, DJ; AMAYA, I; LÓPEZ-ARANDA, Europe and the rest of the world. Journal of development in the early glow strawberry. JM; SÁNCHEZ-SEVILLA, JF; BOTELLA, Berry Research 8: 205-221. Scientia Horticulturae 31: 61-69. MA; VALPUESTA, V. 2009. Impact of plant breeding on the genetic diversity of MICHALSKA, A; CARLEN, C; HERITIER, J; DUSCHESNE, NA. 1766. Histoire naturelle des cultivated strawberry as revealed by expressed ANDLAUER, W. 2017. Profiles of bioactive fraisiers. sequence tag-derived simple sequence repeat compounds in fruits and leaves of strawberry markers. Journal of the American Society for cultivars. Journal of Berry Research 7: 71-84. FAEDI, W; MOURGUES, F; ROSATI, C. 2002. Horticultural Science 134: 337-347. Strawberry breeding and varieties: situation MORALES, RGF; RESENDE, JTV; FARIA, and perspectives. Acta Horticulturae 567: HANCOCK, JF; DRAKE, CA; CALLOW, PW; MV; SILVA PR.; FIGUEIREDO AST; 51-59. SERÇE, S. 2005. Genetic improvement of CARMINATTI, R. 2011. Divergência genética beach strawberry. Hortscience 40: 1644-1645. em cultivares de morangueiro, baseada em FAGHERAZZI, AF; BORTOLINI, AJ; ZANIN, caracteres morfoagronômicos. Revista Ceres DS; BISOL, L; SANTOS, AM; GRIMALDI, HANCOCK, JF; SJULIN, TM; LOBOS, GA. 58: 323-329. F; KRETZSCHMAR, AA; BARUZZI, G; 2008. Strawberries. In: HANCOCK, JF (ed). FAEDI, W; LUCCHI, P; RUFATO, L. 2017a. New strawberry cultivars and breeding activities in Brazil. Acta Horticulturae1156: Hortic. bras., Brasília, v.37, n.1, January-March 2019 15

AR Zeist & JTV Resende MORALES, RGF; FARIA, MV; RESENDE, JTV; Fragaria L. (strawberry): new insights from plant selection. Annals of Eugenics 7: 240-250. RISSINI, ALL; CARMINATTI, R; FARIA, phylogenetic analyses of low-copy nuclear CMD. 2012. Produtividade do morangueiro em genes. Molecular Phylogenetics and Evolution SONE, K; MOCHIZUKI, T; OKIMURA, função da adubação orgânica complementar 51: 515-530. M; NOGUCHI, Y; KITADANI, E. 2003. em cultivo protegido. Ambiência 8: 23-33. Inheritance of ascorbic acid content in SANTOS, AM. 1999. Melhoramento genético strawberry fruits. Journal of the Japanese MULAMBA, NN; MOCK, JJ. 1978. Improvement do morangueiro. Informe Agropecuário 20: Society for Horticultural Science 72: 141-147. of yield potential of the Eto Blanco maize 24-29. (Zea mays L.) population by breeding for STAUDT, G. 2009. Strawberry biogeography, plant traits. Egyptian Journal of Genetics and SHAW, DV; LARSON, KD. 2008. Performance genetics and systematics. Acta Horticulturae Cytology 7: 40-51. of early-generation and modern strawberry 842: 71-84. cultivars from the University of California NELLIST, CF. 2018. Disease resistance in breeding program in growing systems STEWART P; FOLTA, KMA. 2010. A review of polyploid strawberry. In: HYTÖNEN, T; simulating traditional and modern horticulture. photoperiodic flowering research in strawberry GRAHAM, J; HARRISON, R (eds). The Journal of Horticultural Science & (Fragaria spp.). Critical Reviews in Plant genomes of Rosaceous berries and their wild Biotechnology 83: 648-652. Sciences 29: 01-13. relatives. Springer International Publishing, Cham. p.79-94. DOI: 10.1007/978-3-319- SENANAYAKE, YDA; BRINGHURST, RS. TAZZO, IF; FAGHERAZZI, AF; LERIN, SK; 76020-9_7 1967. Origin of Fragaria polyploids. I., AIKE, A; RUFATO, L. 2015. Exigência cytological analysis. American Journal of térmica de duas seleções e quatro cultivares de OLIVEIRA, ACB; BONOW, S. 2012. Novos Botany 54: 221-223. morangueiro cultivado no planalto catarinense. desafios para o melhoramento genético da Revista Brasileira de Fruticultura 37: 550- cultura do morangueiro no Brasil. Informe SHULAEV, V; SARGENT, DJ; CROWHURST, 558. Agropecuário 33: 21-26. RN; MOCKLER, TC; FOLKERTS, O; DELCHER, AL; JAISWAL, P; MOCKAITIS, TENNESSEN, JÁ; GOVINDARAJULU, OLIVEIRA, ACB; ANTUNES, LEC. 2016. K; LISTON, A; MANE, SP; BURNS, P; R; ASHMAN, TL; LISTON, A. 2014. Melhoramento genético e principais cultivares. DAVIS, TM; SLOVIN, JP; BASSIL, N; Evolutionary origins and dynamics of In: ANTUNES, LEC; REISSER JUNIOR, HELLENS, RP; EVANS, C; HARKINS, T; octoploid strawberry subgenomes revealed by C; SCHWENGBER, JE (eds). Morangueiro. KODIRA, C; DESANY, B; CRASTA, OR; dense targeted capture linkage maps. Genome Brasília: Embrapa. p. 133-147. JENSEN, RV; ALLAN, AC; MICHAEL, Biol Evol 6: 3295-3313 TP; SETUBAL, JC; CELTON, J-M; REES, PINCOT, DDA; POORTEN, TJ; HARDIGAN, DJG; WILLIAMS, KP; HOLT, SH; ROJAS, VIEIRA, SD; SOUZA, DC; MARTINS, IA; MA; HARSHMAN, JM; ACHARYA, CB; JJR; CHATTERJEE, M; LIU, B; SILVA, H; RIBEIRO, GHMR; RESENDE, LV; FERRAZ, COLE, GS; GORDON, TR; STUEVEN, M; MEISEL, L; ADATO, A; FILICHKIN, SA; AKL; GALVÃO, AG; RESENDE, JTV. EDGER, PP; KNAPP, SJ. 2018. Genome- TROGGIO, M; VIOLA, R; ASHMAN, T-L; 2017. Selection of experimental strawberry wide association mapping uncovers Fw1, WANG, H; DHARMAWARDHANA, P; (Fragaria x ananassa) hybrids based on a dominant gene conferring resistance to ELSER, J; RAJA, R; PRIEST, HD; BRYANT, selection indices. Genetics and Molecular Fusarium wilt in strawberry. Genes Genomes DW; FOX, SE; GIVAN, SA; WILHELM, Research 16: 1-11. Genetics 8: 1817-1828. LJ; NAITHANI, S; CHRISTOFFELS, A; SALAMA, DY; CARTER, J; GIRONA, EL; WHITAKER, VM; LEE, S; OSORIO, LF; POLAND, J; RUTKOSKI, J. 2016. Advances and ZDEPSKI, A; WANG, W; KERSTETTER, VERMA, S; ROACH, JA; MANGANDI, challenges in genomic selection for disease R A ; S C H WA B , W; K O R B A N , S S ; J; NOH, YH; GEZAN, S; PERES, N. 2017. resistance. Annual Review of Phytopathology DAVIK, J; MONFORT, A; DENOYES- Advances in strawberry breeding at the 54: 79-98. ROTHAN, B; ARUS, P; MITTLER, R; University of Florida. Acta Horticulturae FLINN, B; AHARONI, A; BENNETZEN, 1156: 1-6. QIN, Y; SILVA, JAT; ZHANG, L; ZHANG, S. JL; SALZBERG, SL; DICKERMAN, 2008. Transgenic strawberry: State of the art AW; VELASCO, R; BORODOVSKY, M; WHITAKER, VM; HASING, T; CHANDLER, for improved traits. Biotechnology Advances VEILLEUX, RE; FOLTA, KM. 2011. The CK; PLOTTO, A; BALDWIN, E. 2011. 26: 219-232. genome of woodland strawberry (Fragaria Historical trends in strawberry fruit quality vesca). Nature Genetics 43: 109-116. revealed by a trial of University of Florida RICHTER, AF; FAGUERAZZI, AF; ZANIN, DS; cultivars and advanced selections. Hortscience SILVA, S; ARRUDA, AL; KRETZSCHMAR, SINGH, A; SINGH, BK; DEKA, BC; SANWAL, 46: 553-557. AA; RUFATO, L. 2018. Produtividade e SK; PATEL, RK; VERMA, MR. 2011. The qualidade de cultivares de morangueiro sob genetic variability, inheritance and inter- WITTER, S; RADIN, B; LISBOA, BB; cultivo de solo e semi-hidropônico. Revista relationships of ascorbic acid, beta-carotene, TEIXEIRA, JSG; BLOCHTEIN, B; Científica Rural 20: 193-203. phenol and anthocyanin content in strawberry IMPERATRIZ‑FONSECA, VL. 2012. (Fragaria x ananassa Duch.). Scientia Desempenho de cultivares de morango ROUSSEAU-GUEUTIN, M; GASTON, Horticulturae 129: 86-90. submetidas a diferentes tipos de polinização A; AINOUCHE, A; AINOUCHE, ML; em cultivo protegido. Pesquisa Agropecuária OLBRICHT, K; STAUDT, G; RICHARD, SMITH, HFA. 1936. Discriminant function for Brasileira 47: 58-65. L; DENOYES-ROTHAN, B. 2009. Tracking the evolutionary history of polyploidy in ZAWADNEAK, MAC; SCHUBER, JM; MÓGOR, ÁF. 2013. Como produzir morangos. Curitiba: UFPR, 280p. 16 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Research CARDOSO, J; TONELLI, L; KUTZ, TS; BRANDELERO, FD; VARGAS, TO; DALLEMOLE-GIARETTA, R. 2019. Reaction of wild Solanaceae rootstocks to the parasitism of Meloidogyne javanica. Horticultura Brasileira 37: 017-021. DOI - http://dx.doi.org/10.1590/S0102-053620190102 Reaction of wild Solanaceae rootstocks to the parasitism of Meloidogyne javanica Jéssica Cardoso 1ID; Luiza Tonelli 1ID; Talita S Kutz 1ID; Fernanda D Brandelero 1ID; Thiago de O Vargas 1  ID; Rosangela Dallemole-Giaretta 1ID 1Universidade Tecnológica Federal do Paraná (UTFPR), Pato Branco-PR, Brazil; [email protected]; luiza_tonelli@hotmail. com; [email protected]; [email protected]; [email protected]; [email protected] ABSTRACT RESUMO Intensive production of vegetables in greenhouses can increase Reação de porta-enxertos de Solanáceas silvestres ao the amount of inoculum of soil-borne pathogens, such as the root- parasitismo de Meloidogyne javanica knot nematode. Thus, in this study we aimed to evaluate the potential of Solanaceae as rootstocks resistant to Meloidogyne javanica A produção intensiva de hortaliças em ambiente protegido pode nematodes as an alternative to tomato grafting. The experiment aumentar a quantidade de inóculo de patógenos habitantes do solo, consisted of seven treatments: wild species joá-vermelho (Solanum a exemplo dos nematoides das galhas. Dessa forma, objetivou-se capsicoides), joá-bagudo (Solanum palinacanthum), joá-bravo avaliar o potencial de solanáceas como porta-enxertos resistentes (Solanum viarum), jurubeba (Solanum spp.) and the commercial ao nematoide Meloidogyne javanica como alternativa à enxertia tomato cultivars Santa Cruz Kada, Batalha and Guardião. The em tomateiro. O experimento foi constituído de sete tratamentos: as analyzed variables were gall index; egg mass index; final nematode espécies silvestres joá-vermelho (Solanum capsicoides), joá-bagudo population; reproduction factor (FR) and reaction: susceptibility, (Solanum palinacanthum), joá-bravo (Solanum viarum), jurubeba resistance and immunity; fresh shoot and root mass and number of (Solanum spp.) e os tomateiros comerciais Santa Cruz Kada, Batalha eggs per gram of roots. The wild species joá-vermelho, joá-bagudo e Guardião. As variáveis analisadas foram índice de galhas; índice de and jurubeba showed resistance, with the lowest indexes of galls, egg massas de ovos; população final de nematoides; fator de reprodução e mass, final population of nematodes and number of eggs per gram reação: de suscetibilidade, resistência e imunidade; matéria da parte of root, not differing from the resistant control treatment (hybrid aérea fresca, matéria de raiz fresca e número de ovos por grama rootstock Guardião), with a reproduction factor less than 1, showing de raiz. As espécies joá-vermelho, joá-bagudo e jurubeba foram potential to be used as a resistant rootstock to M. javanica. Joá-bravo resistentes, apresentando os menores índices de galhas, massa de species showed susceptibility to the root-knot nematode, with a FR>1, ovos, população final de nematoides e número de ovos por grama not differing from the susceptible tomato Santa Cruz Kada. These de raiz, não diferindo do tratamento testemunha resistente (porta- results confirm the resistance of wild species to nematode parasitism, enxerto híbrido Guardião), com um fator de reprodução menor que which can prove the viability of use as possible alternative rootstocks, 1, indicando potencial de utilização como porta-enxerto resistente a and reinforce the idea that more studies should be carried out aiming M. javanica. A espécie joá-bravo mostrou-se suscetível ao nematoide to provide more viable options for farmers and plantlet producers. das galhas, com um fator de reprodução maior que 1, não diferindo do tomateiro suscetível Santa Cruz Kada. Tais resultados confirmam a resistência de espécies silvestres ao parasitismo de nematoides, o que pode comprovar a viabilidade de uso como possíveis porta- enxertos alternativos, reforçando a ideia de que mais estudos devem ser realizados com esse enfoque, visando fornecer opções viáveis para o agricultor, bem como aos produtores de mudas. Keywords: Solanum lycopersicum, root-knot nematode, grafting, Palavras-chave: Solanum lycopersicum, nematoide das galhas, resistance. enxertia, resistência. Received on July 26, 2017; accepted on April 10, 2018 One of the main challenges faced by of Parana showed an increase of 77% of approximately 3 hectares, in about horticulture these days is to meet from 2,000 to 2,016, due to an increase 13% of family properties in the state the growing demand for food due to in crop productivity, as a result of the (EMATER, 2016). global population growth (Rouphael et producer organization and investment al., 2018), as well as to produce fresh, in technology (Salvador, 2017). In order to meet market demand, high-quality and free-chemical-residue According to Instituto Paranaense de farmers use intensive production in food in order to meet the demands of Assistência Técnica e Extensão Rural, protected environment, reducing, consumers (Bisbis et al., 2018). these vegetables are grown essentially partially, the negative effects provided by family farmers, on average areas by harsh climatic conditions (Araújo et Vegetable production in the state al., 2009; King et al., 2010; Bisbis et Hortic. bras., Brasília,v.37, n.1, January-March 2019 17

J Cardoso et al. al., 2018). However, intensive vegetable non-host species and soil fumigation and other important characteristics to be cultivation under greenhouses may are used to control these pathogens, considered in order to improve crops, increase inoculums of soil pathogen, resistance is still the most employed being possible alternative rootstocks due to the fact that, when the producer and sustainable strategy (Louws et al., for tomato crop (Keatinge et al., 2014; specializes in growing one vegetable 2010). Migicovsky & Myles, 2017). species, performs successive cultivation in this environment, limiting crop The chemical nematicides generally Some studies on wild Solanum rotation (King et al., 2010; Rosa et al., used to control these pathogens are of species as rootstocks, to control 2013; Pinheiro et al., 2014). high costs and present potential risks for Fusarium oxysporum f. sp., Lycopersici, beneficial soil microorganisms (Huang Verticillium dahliae, Ralstonia Among the species, grown in et al., 2014), environment and human solanacearum, and root-knot nematode, protected environment, the tomato crop health (Fournet et al., 2012; Jones have been carried out at Embrapa stands out due to its high sensitivity et al., 2013; Becker, 2014; Onkendi Hortaliças. These studies showed to inclement weather (Gusmão et al., et al., 2014; Kyriacou et al., 2017). promising results (Pinheiro et al., 2009, 2006; Bergougnoux et al., 2014; Çelik Moreover, the increasing market for 2011, 2014; Pereira et al., 2014; Lopes et al., 2017) and susceptibility to several organic tomatoes does not allow the use & Mendonça, 2016). In nematodes, pests and diseases, which makes this of agrochemicals (López-Pérez et al., the potential of wild Solanum species cultivation difficult, with economic and 2006; Lee et al., 2010). had been already proved in relation to environmental risk factors, caused by parasitism of M. incognita (González excessive use of chemical products (Luz Giving up growing tomato in areas et al., 2010; Dhivya et al., 2014), M. et al., 2007; Loos et al., 2008). infested with root-knot nematode is arenaria (González et al., 2010) and M. not a viable option for the farmer, javanica (Boiteux & Charchar, 1996). Considering soil pathogens, the especially when this area is the only root-knot nematode belonging to the option for cultivation. Thus, more In this context, the aim of this study genus Meloidogyne is of great economic sustainable strategies are necessary to was to evaluate the reaction of rootstocks importance for tomato crop (Carvalho make production in areas infested with of wild species joá-vermelho (Solanum et al., 1999; Podestá et al., 2016). these pathogens viable (Huang et al., capsicoides), joá-bagudo (Solanum Its popular name derives from the 2016). palinacanthum), joá-bravo (Solanum main symptom presented by plants viarum) and jurubeba (Solanum spp.) when affected by these pathogens, Grafting can be a technique used to parasitism of Meloidogyne javanica. which consists of nourishing cells (gall in an integrated management system nematodes), which act as a permanent aiming to minimize damage caused MATERIAL AND METHODS feeding place, providing nutrients by root-knot nematode (Peil, 2003; for the nematode development and Krumbein & Schwarz, 2013; Verdejo- The experiment was carried interfering negatively in nutritional and Lucas et al., 2013). This practice out in a greenhouse at Centro de water absorption by plants (Jones et al., improves the crop quality, with more Biotecnologia Agropecuária of Paraná 2013; Karssen et al., 2013; Kepenekci efficient water and nutritional use, State (26°11’43”S, 52°41’12”W). In this et al., 2018). increase in plant vigor and harvest time, study, the authors tested the wild species making the tomato plant more tolerant to joá-vermelho (S. capsicoides), joá- The reaction of plants to the root- pathogen attack, such as phytonematods bagudo (S. palinacanthum), joá-bravo knot nematode can vary according to (Rizzo, et al., 2004; Lee et al., 2010; (S. viarum), jurubeba (Solanum spp.) species and cultivar, being that the crop Kyriacou et al., 2017). and tomato Santa Cruz Kada (root-knot- rotation, duration of the development susceptible variety), Batalha (susceptible cycle, planting season, population Although the genetic basis of hybrid) and Guardião (resistant-hybrid density and kind of soil also interfere rootstocks for tomato crop seems to tomato rootstock) commercial tomatoes. in damage severity (Jones et al., 2013). be wide, considering the great quantity Each experimental unit consisted of Generally, these observed symptoms of species related to the crop which a pot with one plant, in completely include reduced fruit yield and quality, could be used, the current genetic basis randomized experimental design, with slow growth, yellowish leaves, wilting is limited (King et al., 2010). Most 10 replications per treatment. in the hottest hours of the day, and commercially available rootstocks decreased resistance to other biotic are high-cost hybrids, produced by The inoculum of root knot nematode and abiotic factors (Jones et al., 2013; specialized companies (King et al., M. javanica used in the experiment was Podestá et al., 2016; Kepenekci et al., 2010; Lopes et al., 2015). obtained from a pure population kept in 2018). tomato plants, grown in a greenhouse. These rootstocks make the The nematode eggs were obtained The root-knot nematodes are production more expensive for farmers according to the methodology described mandatory endoparasites, which may and that is why identifying alternative by Hussey & Barker (1973), modified by be native or inserted into new production rootstocks, resistant or tolerant, as an Bonetti & Ferraz (1981). The seedlings regions, through contaminated soils, root alternative to commercial hybrids, is of all wild and commercial species were remnants or infected plants (Louws et essential. Wild Solanum species are al., 2010). Although crop rotation with sources of resistance characteristics to various soil pathogens, fruit quality 18 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Reaction of wild Solanaceae rootstocks to the parasitism of Meloidogyne javanica produced in a greenhouse, in polystyrene were compared to controls (commercial compared to the other wild Solanaceae trays with 128 cells. Plantlets were cultivars) by Dunnett test (p<0.05). species, did not differ statistically from transplanted 30 days after emergence, Analyses were performed using Assistat joá-vermelho. in 1-kg-capacity plastic containers, software (Silva & Azevedo, 2002). with substrate, soil and sand in the ratio The lowest development of shoot 2:1 (v:v), autoclaved in advance for 1 RESULTS AND DISCUSSION area of the plants is related to the h at 120˚C, 1 atm, (Ito et al., 2014). highest number of galls which cause One week after seedling transplant, the The wild species joá-bagudo and interferences on plant roots, which nematode was inoculated using 2 mL jurubeba showed the lowest gall index interfere on efficient absorption of of suspension containing 5,000 eggs of values (IG). For egg mass (IMO), nutrients and consequently on plant M. javanica through 4 equidistant holes jurubeba showed the lowest value, development (Jones et al., 2013; Karssen open in soil, close to the plant stem. followed by joá-bagudo and joá- et al., 2013; Kepenekci et al., 2018). vermelho. On the other hand, joá-bravo Therefore, plants showing lower MPAF Sixty days after nematode showed the highest indexes for both generally show higher susceptibility to inoculation, gall index (IG), egg mass variables (Table 1). M. javanica. index (IMO), final nematode population (Pf); reproduction factor (FR) and Final nematode population (Pf) In relation to MRF, the species reaction of: susceptibility (S), resistance and number of eggs per gram of root joá-bravo showed the lowest value (in (R) and immunity (I); fresh shoot (NOGR) of joá-vermelho, joá-bagudo relation to the other wild Solanaceae mass (MPAF); fresh root mass (MRF); and jurubeba showed lower values species) and did not differ statistically number of eggs per gram of root (Table 1), in comparison to the other from jurubeba. These results were (NOGR) were evaluated. species, proving the lowest root-knot obtained due to the slow initial growth nematode multiplication rate. However, of jurubeba, which results in a lower In order to determine gall index (IG), the species joá-bravo showed the development, considering that this the scale proposed by Charchar et al. highest value for both variables, due species showed reduced number of galls. (2003) was used: after being washed, to high ratio of Pf/MRF, proving the the roots were graded from 1 to 5 (1= high susceptibility of this species to The species joá-bagudo, jurubeba without galls; 2= up to 10 small galls; nematode M. javanica. Silva et al. and joá-vermelho showed to be resistant 3= up to 50 small galls; 4= more than (2013) found similar values for Pf in to M. javanica, when compared to 50 small galls and up to 10 big galls; 5= another species of the wild Solanaceae, the susceptible commercial controls roots with more than 50 small galls and Maria-pretinha (Solanum americanum), (Batalha and Santa Cruz Kada) and more than 10 big galls). which showed to be susceptible with a similar to resistant-hybrid rootstock final population of 34,720 eggs. Guardião (Table 2), showing FR<1 The egg mass index (IMO) was according to Oostenbrink (1966). calculated following the scale proposed Variable MPAF showed lower value However, the species joá-bravo showed by Huang et al. (1986), considering a for wild Solanaceae joá-bravo, for its high susceptibility showing FR>1, not grading scale from 1 to 5 (1= without high susceptibility to nematode M. differing from susceptible tomato Santa egg masses; 2= 1 to 5 egg masses; 3= javanica, followed by jurubeba. On the Cruz Kada, which proved viability of 6 to 15 egg masses; 4= 16 to 30 egg other hand, although the species joa- the inoculum used in the present study, masses; 5= more than 30 egg masses). bagudo presented a higher value when showing FR>1. Coloration methodology was performed according to Rocha et al. (2005). The results found in this study corroborate the ones found by Pinheiro et Final nematode population per root (Pf) was obtained according to the Table 1. Average values of gall index (IG), egg mass index (IMO), final nematode population methodology described by Hussey & (Pf), fresh shoot mass (MPAF), fresh root mass (MRF) and number of eggs per gram of Barker (1973), modified by Bonetti & roots (NOGR) of Meloidogyne javanica on alternative and commercial rootstocks. Pato Ferraz (1981). Branco, UTFPR, 2015. Reproduction factor (FR) was Treatment IG IMO Pf MPAF (g) MRF (g) NOGR calculated using the ratio between final nematode population (Pf) and initial Batalha 4.8 a 4.5 a 66,029.0 a 12.9 b 7.0 a 9,344.0 b population (Pi), and classified according to Oostenbrink (1966), expressed Santa Cruz Kada 4.9 a 5.0 a 32,555.0 b 6.1 c 4.2 b 7,865.5 b as follows: FR= 0: immune; FR<1: resistant; FR≥ 1: susceptible. joá-bravo 4.9 a 4.3 a 32,081.0 b 1.7 e 2.5 b 13,450.1 a Variable data were submitted to joá-vermelho 3.4 b 2.4 b 258.0 c 6.3 c 7.9 a 33.2 c analysis of variance using F test, comparing the treatment averages joá-bagudo 1.5 c 1.7 c 889.3 c 7.8 c 8.0 a 126.2 c by Scott-Knott test (p<0.05). For reproduction factor (FR), the averages jurubeba 1.5 c 1.0 d 691.9 c 4.5 d 4.2 b 295.3 c of treatments using wild Solanaceae Guardião 1.0 c 1.0 d 133.7 c 15.7 a 7.9 a 16.9 c CV (%) 15.4 26.9 25.5 30.4 87.9 79.2 Averages followed by same lowercase letter in the column do not differ statistically by Scott-Knott test (p<0.05). Hortic. bras., Brasília, v.37, n.1, January-March 2019 19

J Cardoso et al. Table 2. Average values of reproduction factor (FR) and rootstock reaction of wild Solanaceae BONETTI, JIS; FERRAZ, S. 1981. Modificações species submitted to Meloidogyne javanica parasitism and comparison with susceptible and do método de Hussey & Barker para extração resistant controls. Pato Branco, UTFPR, 2015. de ovos de Meloidogyne exígua em raízes de cafeeiro. Fitopatologia Brasileira 6: 553. Treatments Reproduction factor Reaction CARVALHO, JWA; MALUF, WR; FIGUEIRA, Batalha 13.2 S AR; GOMES, LAA. 1999. Obtenção de linhagens de tomateiro de crescimento Santa Cruz Kada 6.5 S determinado com resistência múltipla a nematóides de galhas e a tospovírus. Ciência Guardião 0.0 R e Agrotecnologia 23: 593-607. joá-bravo 6.4(1.3) S ÇELIK, Ö; AYAN, A; ATAK, Ç. 2017. Enzymatic and non-enzymatic comparison of two different joá-vermelho 0.1(1.2) R industrial tomato (Solanum lycopersicum) varieties against drought stress. Botanical joá-bagudo 0.2(1.2) R Studies 58: 1-13. jurubeba 0.1(1.2) R CHARCHAR, JM; GONZAGA, V; GIORDANO, LB; BOITEUX, LS; REIS, NVB; ARAGÃO, CV(%) 79.2 - FAS. 2003. Reações de cultivares de tomate à infecção por população mista de Meloidogyne Averages followed by 1, 2 or 3 differ from the controls: Batalha, Santa Cruz Kada and incognita raça 1 e M. javanica em estufa Guardião respectively, by Dunnett test (p<0.05). S= susceptible; R= resistant. plástica e campo. Nematologia Brasileira 27: 49-54. al. (2009), who observed that the species (2013) obtained S. gilo, S. lycocarpum S. asperolanatum, S. stramonifolium and and S. stramonifolium as alternative DHIVYA, R; SADASAKTHI, A; SIVAKUMAR, Solanum spp., showed to be resistant to rootstocks compatible with tomato M. 2014. Response of wild solanum rootstocks Meloidogyne incognita race 1, whereas and suitable for conditions in Brazilian to root-knot nematode (Meloidogyne incognita S. straminifolium, S. paniculatum, and S. Amazon Region. This fact demonstrates Kofoid and White). International Journal of subinerme were resistant to Meloidogyne feasibility of grafting and the importance Plant Sciences 9: 117-122. enterolobii, Sin.: M. mayaguensis. Some of further studies aiming to show the studies evaluating different accessions efficiency of these species as alternative EMATER. 2016. A agricultura familiar e a of Solanum stramonifolium in relation to rootstocks for tomato crop. olericultura no Paraná. Disponível em http:// parasitism of nematode M. enterolobii, www.emater.pr.gov.br/modules/noticias/ Pinheiro et al. (2014) found 6 accessions ACKNOWLEDGEMENTS article.php?storyid=4624. Accessed on June, of Solanaceae resistant to 17 studied 2018. species, being suitable rootstocks To Conselho Nacional de for Solanaceae in areas infested with Desenvolvimento Científico e FARIAS, EAP; FERREIRA, RLF; ARAÚJO this pathogen. Besides, Dhivya et al. Tecnológico (CNPq) for scholarship NETO, SE; COSTA, FC; NASCIMENTO, (2014), evaluating rootstocks of wild granted to the first author. DS. 2013. Organic production of tomatoes in Solanaceae resistant to M. incognita, the amazon region by plants grafted on wild obtained similar values for joá-bravo REFERENCES Solanum rootstocks. Ciência e Agrotecnologia with FR>1, showing to be susceptible, 37: 323-329. however five from the other evaluated ARAÚJO, JS; ANDRADE, AP; RAMALHO, Solanaceae showed to be resistant or CL; AZEVEDO, CAV. 2009. Cultivo do FOURNET, S; KERLAN, MC; RENAULT, L; moderately resistant to the pathogen. pimentão em condições protegidas sob DANTEC, JP; ROUAUX, C; MONTARRY, diferentes doses de nitrogênio via fertirrigação. J. 2012. Selection of nematodes by resistant These results confirm the resistance Revista Brasileira de Engenharia Agrícola e plants has implications for local adaptation and of wild species (belonging to this Ambiental 13: 559-565. cross‐virulence. Plant Pathology 62: 184-193. family) to nematode parasitism, which can prove the viability of using them BECKER, JO. 2014. Plant health management: GONZÁLEZ, FM; GÓMEZ, L; RODRÍGUEZ, as alternative rootstocks, and reinforce crop protection with nematicides. In: NEAL, MG; PIÑÓN, M; CASANOVA, A; GÓMEZ, the idea that further studies on grafting KA. Encyclopedia of Agriculture and Food O; RODRÍGUEZ, Y. 2010. Respuesta de should be carried out, aiming to provide Systems. Oxford: Academic Press, p.400-407. genotipos de solanáceas frente a Meloidogyne more viable options for farmers. incognita (Kofoid y White) Chitwood raza 2 BERGOUGNOUX, V. 2014. The history of y M. arenaria (Neal) Chitwood. Revista de Although the wild Solanaceae tomato: From domestication to biopharming. Protección Vegetal 25: 51-57. species (joá-bagudo, joá-vermelho and Biotechnology Advances 32: 170-189. jurubeba), evaluated in the present study, GUSMÃO, MTA; GUSMÃO, SAL; ARAÚJO, showed resistance to the nematode M. BISBIS, MB; GRUDA, N; BLANKE, M. 2018. JAC. 2006. Produtividade de tomate tipo javanica, the compatibility of these Potential impacts of climate change on cereja cultivado em ambiente protegido e em species is another important factor to vegetable production and product quality - A diferentes substratos. Horticultura Brasileira be taken into account. In this context, review. Journal of Cleaner Production 170: 24: 431-436. Simões (2014) obtained compatibility of 1602-1620. jiló and jurubeba species as rootstocks HUANG, SP; MIRANDA, JEC; MALUF, WR. for tomato cultivar IPA-6. Farias et al. BOITEUX, LS; CHARCHAR, JM. 1996. 1986. Resistance to root-knot nematodes Genetic resistance to root-knot nematode in a Brazilian sweet potato collection. (Meloidogyne javanica) in eggplant (Solanum Fitopatologia Brasileira 11: 761-767. melongena). Plant Breeding 115: 198-200. HUANG, W; CUI, J; LIU, S; KONG, L; WU, Q; PENG, H; HE, W; SUN, J; PENG, D. 2016. Testing various biocontrol agents against the root-knot nematode (Meloidogyne incognita) in cucumber plants identifies a combination of Syncephalastrum racemosum and Paecilomyces lilacinus as being most effective. Biological Control 92: 31-37. ITO, LA; GAION, LA; GALATTI, FS; BRAZ, LT; SANTOS, JM. 2014. Resistência de porta-enxertos de cucurbitáceas a nematóides 20 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Reaction of wild Solanaceae rootstocks to the parasitism of Meloidogyne javanica e compatibilidade da enxertia em melão. para uso como porta-enxerto em tomateiro. January, 2017. Horticultura Brasileira 32: 297-302. Horticultura Brasileira 34: 356-360. PINHEIRO, JB; MENDONÇA, JL; SANTANA, JONES, JT; HAEGEMAN, A; DANCHIN, EGJ; LÓPEZ-PÉREZ, JALE; STRANGE, M; JP. 2011. Wild Solanaceae: potential for the use GAUR, HS; HELDER, J; MGH; KIKUCHI, T; KALOSHIAN, I; PLOEG, AT. 2006. as rootstocks resistant to root-knot nematode MANZANILLA-LÓPEZ, R; PALOMARES- Differential response of Mi gene-resistant (Meloidogyne spp.). Acta Horticulturae 917: RIUS, JE; WESEMAEL, WML; PERRY, RN. tomato rootstocks to root-knot nematodes 243-247. 2013. Top 10 plant-parasitic nematodes in (Meloidogyne incognita). Crop Protection molecular plant pathology. Molecular Plant 25: 382-388. PODESTÁ, GS; AMORA, DX; MAFFIA, LA; Pathology 14: 946-961. NASU, ÉGC; FERRAZ, S; FREITAS, LG. LOUWS, FJ; RIVARD, CL; KUBOTA, C. 2016. Effect of time between soil infestation KARSSEN, G; WESEMAEL, W; MOENS, M. 2010. Grafting fruiting vegetables to manage with Pochonia chlamidosporia and planting 2013. Root-knot nematodes. In: PERRY, soilborne pathogens, foliar pathogens, on the efficacy of the fungus in managing RN; MOENS, M (eds). Plant Nematology. arthropods and weeds. Scientia Horticulturae Meloidogyne javanica. Crop Protection 2nd edition, CAB International, Wallingford, 127: 127-146. 90:77-83. UK, 73-108 LUZ, JMQ; SHINZATO, AV; SILVA, MAD. RIZZO, AAN; CHAVES, FCM; LAURA, VA; KEATINGE, JDH; LIN, LJ; EBERT, AW; CHEN, 2007. Comparação dos sistemas de produção GOTO, R. 2004. Avaliação de métodos WY; HUGHES, JA; LUTHER, GC; WANG, de tomate convencional e orgânico em cultivo de enxertia e porta-enxertos para melão JF; RAVISHANKAR, M. 2014. Overcoming protegido. Bioscience Journal 23: 7-15. rendilhado. Horticultura Brasileira 22: biotic and abiotic stresses in the Solanaceae 808-810. through grafting: current status and future MIGICOVSKY, Z; MYLES, S. 2017. Exploiting perspectives. Biological Agriculture & wild relatives for genomics-assisted breeding ROCHA, FS; MUNIZ, MFS; CAMPOS, VP. 2005. Horticulture 30: 272-287. of perennial crops. Frontiers in Plant Science Coloração de fitonematoides com corantes 8: 460. usados na indústria alimentícia brasileira. KEPENEKCI, I; HAZIR, S; OKSAL, E; Nematologia Brasileira 29: 293-297. LEWIS, EE. 2018. Application methods of ONKENDI, EM; KARIUKI, G; MARAIS, M; Steinernema feltiae, Xenorhabdus bovienii and MOLELEKI, LN. 2014. The threat of root‐ ROSA, JMO; WESTERICH, JN; WILCKEN, Purpureocillium lilacinum to control root-knot knot nematodes (Meloidogyne spp.) in Africa: SRS. 2013. Reprodução de Meloidogyne nematodes in greenhouse tomato systems. a review. Plant Pathology 63: 727-737. javanica em olerícolas e em plantas utilizadas Crop Protection 108: 31-38. na adubação verde. Tropical Plant Pathology OOSTENBRINK, M. 1966. Major characteristics 38: 133-141. KING, SR; DAVIS, AR; ZHANG, X; CROSBY, of the relation between nematodes and plants. K. 2010. Genetics, breeding and selection of Medelingen Van De Landbouwhogeschool ROUPHAEL, Y; KYRIACOU, MC; rootstocks for Solanaceae and Cucurbitaceae. 66: 1-46. PETROPOULOS, SA; PASCALE, S; Scientia Horticulturae 127: 106-111. COLLA, G. 2018. Improving vegetable PEIL, RM. 2003. A enxertia na produção de mudas quality in controlled environments. Scientia KRUMBEIN, A; SCHWARZ, D. 2013. Grafting: de hortaliças. Ciência Rural 33: 1169-1177. Horticulturae 234: 275-289. a possibility to enhance health-promoting and flavor compounds in tomato fruits of shaded PEREIRA, RB; MENDONÇA, JL; AGUIAR, SALVADOR, CA. 2017. Olericultura - análise da plants? Scientia Horticulturae 149: 97-107. FM; RIBEIRO, MCV; PINHEIRO, JB. conjuntura agropecuária - novembro de 2017. 2014. Reação de acessos de jurubeba Juna Secretaria da agricultura e do abastecimento KYRIACOU, MC; ROUPHAEL, Y; COLLA, (Solanum stramonifolium) a Fusarium (SEAB). Available at http://www.agricultura. G; ZRENNER, R; SCHWARZ, D. 2017. oxysporum f. sp. lycopersici raça 3. Brasília: pr.gov.br. Accessed June, 2018. Vegetable grafting: the implications of a Embrapa Hortaliças (Boletim de Pesquisa e growing agronomic imperative for vegetable Desenvolvimento 113). Available at https:// SILVA, FAS; AZEVEDO, CAV. 2002. Versão fruit quality and nutritive value. Frontiers in ainfo.cnptia.embrapa.br/digital/ bitstream/ do programa computacional Assistat para Plant Science 8: 1-23. item/118235/1/BPD-113.pdf. Accessed June, o sistema operacional Windows. Revista 2018. Brasileira de Produtos Agroindustriais 4: LEE, JM; KUBOTA, C; TSAO, SJ; BIE, Z; 71-78. ECHEVARRIA, PH; MORRA, L; ODA, M. PINHEIRO, JB; MENDONÇA, JL; RODRIGUES, 2010. Current status of vegetable grafting: CS; PEREIRA, RB; SUINAGA, FA. 2014. SILVA, SLS; SANTOS, TFS; RIBEIRO, NR; diffusion, grafting techniques. Scientia Avaliação de Solanum stramonifolium para SILVÉRIO, AT; MORAIS, TS. 2013. Reação Horticulturae 127: 93-105. reação a Meloidogyne enterolobii. Brasília: de plantas daninhas a Meloidogyne incognita Embrapa Hortaliças (Boletim de Pesquisa e e M. javanica, Nematologia Brasileira 37: LOOS, RA; SILVA, DJH; FONTES, PCR; Desenvolvimento, 124). Available at https:// 57-60. PICANÇO, MC. 2008. Identificação e ainfo.cnptia.embrapa.br/digital/bitstream/ quantificação dos componentes de perdas de item/117999/1/BPD-124.pdf. Accessed SIMÕES,AC. 2014. Compatibilidade de tomateiro produção do tomateiro em ambiente protegido. January, 2017. sob diferentes portaenxertos e métodos de Horticultura Brasileira 26: 281-286. enxertia em sistema orgânico. Enciclopédia PINHEIRO, JB; MENDONÇA, JL; SANTANA, Biosfera 10: 961-972. LOPES, CA; BOITEUX, LS; ESCHEMBACK, JP. 2009. Solanáceas silvestres: potencial V. 2015. Eficácia relativa de porta-enxertos de uso como porta-enxertos resistentes ao VERDEJO-LUCAS, S; BLANCO, M; CORTADA, comerciais de tomateiro no controle da nematóide-das-galhas (Meloidogyne spp.). L; SORRIBAS, FJ. 2013. Resistance of tomato murcha-bacteriana. Horticultura Brasileira Brasília: Embrapa Hortaliças (Boletim de rootstocks to Meloidogyne arenaria and 33: 125-130. Pesquisa e Desenvolvimento, 57). Available Meloidogyne javanica under intermittent at https://www.infoteca.cnptia.embrapa.br / elevated soil temperatures above 28 C. Crop LOPES, CA; MENDONÇA, JL. 2012. Reação bitstream/doc/783050/1/bpd57.pdf. Accessed Protection 46: 57-62. de acessos de jurubeba à murcha bacteriana Hortic. bras., Brasília, v.37, n.1, January-March 2019 21

Research ZAMORA, VRO; SILVA, MM; SILVA, GF; SANTOS JÚNIOR, JA; MENEZES, D; MENEZES, SM. 2019. Pulse drip irrigation and fertigation water depths in the water relations of coriander. Horticultura Brasileira 37: 022-028. DOI - http://dx.doi.org/10.1590/S0102-053620190103 Pulse drip irrigation and fertigation water depths in the water relations of coriander Valentin Ruben O Zamora 1ID; Manasses M da Silva 1 ID; Geronimo F da Silva 1 ID; José Amilton Santos Júnior 1 ID; Dimas Menezes 1ID; Sirleide Maria de Menezes 1 ID 1Universidade Federal Rural de Pernambuco (UFRPE), Recife-PE, Brazil; [email protected]; [email protected]; geronimo. [email protected]; [email protected]; [email protected]; [email protected] ABSTRACT RESUMO This study was installed to evaluate the effect of pulse drip Gotejamento por pulsos e lâminas de fertirrigação nas irrigation under different water depth levels (fertigation) in the relações hídricas do coentro main water relations of coriander crop (Coriandrum sativum). The experiment was installed under protected environment conditions, O presente trabalho foi desenvolvido com o objetivo de avaliar o at UFRPE, Recife, Brazil. The experimental design was randomized efeito do gotejamento por pulsos, sob diferentes níveis da lâmina de blocks in a 2x5 factorial scheme, with three replications. Treatments fertirrigação, nas principais relações hídricas da cultura do coentro consisted of two application types (continuous and pulsed irrigation), (Coriandrum sativum). O experimento foi realizado em condições and five water depths with replacement of 40, 60, 80, 100 and 120% de ambiente protegido, nas dependências da UFRPE, campus Dois of crop evapotranspiration (ETc). Water demand was estimated Irmãos, Recife-PE. O delineamento experimental foi de blocos through water balance using a drainage lysimetry. Six irrigation casualizados em esquema fatorial 2x5, com três repetições. Os pulses were defined with a 60-minute-rest interval between two tratamentos consistiram de dois tipos de aplicação (irrigação contínua successive applications. Plants irrigated by pulses showed higher e por pulsos) e cinco lâminas de reposição da fertirrigação de 40, 60, water productivity values (fresh and dry mass), higher water content 80, 100 e 120% da evapotranspiração de cultivo (ETc). A demanda (shoot and root), higher shoot mass production index and lower de água foi estimada por balanço hídrico via lisimetria de drenagem. root mass production index and root-shoot ratio. The reduction of Foram definidos seis pulsos de irrigação com intervalo de 60 minutos applied fertigation water depths increased plant water stress index. de repouso entre duas aplicações sucessivas. As plantas irrigadas The irrigation pulses used ensured water content able to maintain por pulsos apresentaram maior produtividade de água (massa seca the crop’s marketable quality. Pulse application in irrigation system e fresca), maior teor de água (parte aérea e raíz), maior índice de increased shoot mass production index and reduced root mass produção de massa na parte aérea e menor índice de produção de production index. massa na raiz e razão raiz parte aérea. A redução das lâminas de fertirrigação aplicadas aumentou o índice de estresse hídrico das plantas. Os pulsos de irrigação utilizados garantiram um teor de água na planta capaz de manter a qualidade comerciável da cultura. A aplicação dos pulsos na irrigação aumentou o índice de produção de massa da parte aérea e reduziu o índice de produção de massa da raiz. Keywords: Coriandrum sativum, intermittent irrigation, water Palavras-chave: Coriandrum sativum, irrigação intermitente, déficit deficit, dripping irrigation system. hídrico, irrigação localizada. Received on April 9, 2018; accepted on November 20, 2018 In Brazil, rainfall scarcity and essential for the sector sustainability outdoor markets and supermarkets and irregularity are among the main (Lima et al., 2011). the fruits are used for industries (Maciel limiting factors for agricultural et al., 2012). production. In the Northeastern part Among important crops, in the of the country, even under unfavorable Northern and Northeastern regions of Due to weather conditions of water availability conditions, agriculture the country, the coriander stands out. the region, coriander is grown using has prominent role in the regional Coriander is an annual herbaceous irrigation. Generally, it is exploited economy. In Sertão Region prevails vegetable that, due to its versality, in small areas with water from small subsistence farming and this agriculture is of considerable value and great sources such as ponds, Amazon wells, practice is sometimes hampered by socioeconomic importance. The crop is natural wells in riverbeds, tubular wells, droughts (Castro, 2013). Thus, using cultivated mostly by small and medium- among others (Medeiros et al., 1998). more efficient irrigation systems is sized farmers, in order to be used as During its cultivation, irrigation systems spice. This herb is commercialized in and high frequency fertigation can be 22 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Pulse drip irrigation and fertigation water depths in the water relations of coriander adopted in order to save water, control Agronomy Department of Universidade observations. external solute movement and improve Federal Rural de Pernambuco, Campus product quality. Dois Irmãos, Recife PE, Brazil (8°1’7” Plots were irrigate using a drip tape S; 34°56’46”W; 6,5 m altitude). (DN 16 mm); spacing among drippers On the other hand, the authors was 0.30 m, nominal flow was 0.60 L h-1 highlight that the used water has to be According to Köppen’s classification, and operating pressure of 10 mca. For totally available for the crop, through an the local climate is classified As’, hot an appropriate operation, drain valves, efficient application and soil storage. A and humid tropical, rainfall during solenoid valves, pressure regulator, technique to maximize the use of water autumn and winter, presenting a dry filter, microcontroller and a pumping is pulse irrigation, which consists of a season, which extends from September system with installed capacity of 0.5 more frequent, split water application. to February, and a rainy season from CV were used. Thus, using this technique, it is expected March to August (Jales et al., 2012). to save water, which would be eventually Temperature and relative humidity were Irrigation time was determined wasted in a continuous irrigation, due to monitored via ARDUINO; average considering the irrigation water depth to evaporation or deep percolation losses maximum temperature of 34.35ºC be applied in each treatment. Irrigation (Nascimento et al., 2013). and average minimum temperature of water depth was obtained using simple 25.66ºC; the average maximum relative relationship between ETc and average Moreover, water splitting allows to humidity observed was 92.22% and efficiency of the irrigation system keep water and soluble nutrients near the average minimum relative humidity (90%). active root zone of the crop, resulting in was 55.90%. a reduced risk of water and nutrients to Differences between treatments move under the root zone. Experimental units were installed in were observed from 10th day after a protected environment measuring 162 sowing. Until this day, all plots were To ensure good productivity, m2, greenhouse, chapel type, consisting irrigated daily, applying 100% of ETc irrigation can be associated with of 30 masonry seedbeds, 1.0 m2 (5.0x0.2 continuously, totalizing 19.2 mm. nutrients, essential to the crop, using m) and 0.2 m deep. Each seedbed was fertigation. In order to make this practice waterproofed with plastic polyethylene Water depth split application and efficient, a balance between quantity of film and equipped with a drainage calculus of application times were nutrients and applied water is necessary, system. done automatically, according to each to maintain appropriate concentration treatment, through an electronic control of fertilizers in the irrigation water, The soil used in this study presented circuit ARDUINO. Daily irrigations for an appropriate crop development, sandy texture, 904 g kg-1 of sand, 32 g were done always at 9 a.m. providing nutrient absorption in required kg-1 of silt and 64 g kg-1 of clay. Soil quantities. densities and particles were 1.5 and 2.5 Description and conduction of kg dm-3, respectively. Water contents the crop Water and nutrient use is related to equivalent to the field capacity were 0.10 water use efficiency, which is expected m3 m-3 and permanent wilting point was Coriander cultivar Verdão was to be increased under fractional 0.09 m3 m-3. Chemical soil properties, sown directly in the experimental management, as evidenced by Almeida before the experiment installment were: units, placing 20 seeds per pit, spacing et al. (2015), for replacement of 75% pH (water 1:2.5)= 5.1; Ca2+= 2.0 cmolc 10x15 cm. Plants were thinned ten days ETc. Warner et al. (2009), evaluating dm-3; Mg= 1.5 cmolc dm-3; Al= 0.2 cmolc after sowing, leaving six plants per pit. tomato crop, verified water savings of dm-3; Na= 0.01 cmolc dm-3; K= 0.01 Sampling useful area at harvest was 1.0 40%, keeping productivity and quality cmolc dm-3; P= 2.0 mg dm-3; M.O.= 9.69 m2 per plot. of crop. Abdelraouf et al. (2012), g kg-1; H+Al= 4.68 cmolc dm-3. studying potato, noticed an increase of Agricultural limestone (calcitic) was 63.90% in water productivity, applying Randomized block design, in applied (484 kg ha-1) in order to correct pulse treatments, highlighting water a factorial scheme 2x5, was used. soil acidity and neutralize exchangeable savings of up to 25% per crop cycle. Treatments consisted of two water Al. Liming and phosphate fertilization application types (pulse and continuous (127 kg ha-1 simple superphosphate) Given the above, considering irrigation) and five fertigation water was performed conventionally, done scarcity of information, this study depths with replacement of 40, 60, 80, according to the methodological aimed to evaluate the effect of pulse 100 and 120% crop evapotranspiration procedures recommended by drip irrigation under different levels (ETc), with three replications, totalizing Cavalcanti et al. (2008). The macro of fertigation, considering main water ten treatments, making 30 experimental and micronutrients, essential to the variables and water use efficiency by plots. Six irrigation pulses with a crop, were applied daily via fertigation, the coriander crop. 60-minute break between two successive according to Furlani (1998). irrigations were defined. ETc was MATERIAL AND METHODS determined by water balance using a Water consumption drainage lysimetry installed in 5.0-liter The experiment was carried out pots inside the greenhouse. ETc was During the experiment, 34 daily between August and September, 2017, in calculated using the average of four irrigations were applied. Irrigation water depth was established considering a Hortic. bras., Brasília, v.37, n.1, January-March 2019 range of 20%, from the lowest water depth 40%, up to 120% replacement ETc, totalizing 54.4 mm and 124.8 mm, 23

VRO Zamora et al. respectively. Differentiated water depths Root and shoot water content was computer statistical software SISVAR for each treatment are shown in Table 1. calculated using the ratio between (Ferreira, 2011). fresh and dry mass of shoot and root, Two evaluations were performed according to the methodology proposed RESULTS AND DISCUSSION in order to verify water distribution by Benincasa (1988), following the uniformity in the irrigation system, equations 4 and 5. Va r i a n c e a n a l y s i s s h o w e d a one at the beginning and another at the significant effect (p<0.01) concerning end of the experiment, according to the (4) the type of application and fertigation methodology described by Merriam & water depth in relation to root water Keller (1978). For an average operating (5) content (RWC), shoot and root mass pressure of 10.0 mca the average production index (SMPI, RMPI) and flow of the drippers was 0.55 L h-1. In which SWC= shoot water content root-shoot ratio (RSr). The authors The coefficient of water distribution (%); SFM= shoot fresh mass (g); SDM= noticed significant effect (p<0.01) uniformity for the beginning and the shoot dry mass (g); RWC= root water only for fertigation water depth in end of the experiment was 98.20 and content (%); RFM= root fresh mass (g); relation to water stress index (WSI) 97.09%, respectively. RDM= root dry mass (g). and shoot water content (SWC). For water productivity of fresh and dry Evaluated variables Shoot and root mass production mass production (WPFM, WPDM), an index interaction between the two factors was Water stress index noticed (p<0.01). Shoot and root mass production Crop water stress index was index was calculated using the ratio Water stress index (WSI) of calculated using the difference of the between shoot and root dry mass and coriander linearly decreased in the leaf temperature and the temperature total dry mass, according to Benincasa ratio 0.058ºC for each 1% increase in inside the greenhouse, following the (1988), using equations 6 and 7. replacement water depth independently methodology of Idso et al. (1977), of the type of application (Figure 1A). according to equation 1. (6) The fact that WSI increases in relation to the reduction of water depth, makes (1) (7) it clear that plants submitted to water deficit transpired less due to the stomatal In which WSI= water stress index In which SMPI= shoot mass closing in the leaves, resulting directly (ºC); TL= leaf temperature (ºC); TA= air production index; RMPI= root mass in higher values of leaf temperature. temperature (ºC). production index; SDM= shoot dry mass (g); RDM= root dry mass (g); TDM= For all treatments, negative values of Leaf temperature was registered total dry mass (g). WSI were observed, showing that plants daily using a portable digital which did not suffer from water stress, infrared thermometer, at the time of Root-shoot ratio maintained leaf surface temperature maximum solar radiation of the day. below air temperature. This fact was Air temperature was measured using The root-shoot ratio is the index probably because of the greenhouse a calibrated electronic temperature which allows to evaluate the effect of cover, which decreased the effect of the and humidity sensor, installed in the water stress and salinity conditions in sun’s rays, besides the adaptation of the experimental area. soil, through evaluating the highest genotype used to the climatic conditions and the lowest development of roots of the northeast region. Water productivity in relation to shoot part of the plant, in order to improve water absorption Shoot water content (SWC) of Water productivity was determined process and soil nutrients. the coriander adjusted to a quadratic as an indicator of the efficiency of model (Figure 1B). SWC decreased in agricultural water use to increase the The root-shoot ratio (RSr) was relation to the reduction of water depth crop yield. Water productivity was calculated relating the root dry mass and because of a negative effect of the plant obtained through the ratio of total crop shoot dry mass, according to Magalhães biological processes, resulting in a production (fresh and dry) and volume (1979), using equation 8. decrease of fresh mass accumulation. of applied water, according to equations According to Eid et al. (2013), this 2 and 3. (8) fact is explained due to an increase of soil surface evaporation rate caused (2) In which RSr= root-shoot ratio by intervals between pulses. These (dimensionless); RDM= root dry mass intervals provide an increase in salt (3) (g); DM= shoot dry mass (g). concentration near plant root area. Thus, because of an increase in osmotic In which WPFM= water productivity Statistical analysis potential and, therefore. probability in fresh mass production (g L-1); WPDM= water productivity in dry Obtained results were submitted to mass production (g L-1); TFM= total the variance analysis using F test. When fresh mass (g); TDM= total dry mass some significant effect was verified, (g); TWC= total water consumption (L the authors performed the regression plant-1). analysis for the quantitative factor and agglomerative Scott Knott test at 5% Root and shoot water content significance for qualitative factor, using 24 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Pulse drip irrigation and fertigation water depths in the water relations of coriander of plasmolysis (loss of water through a possibility of reaching maximum (Figure 2B), the authors verified that osmosis), a decrease in fresh matter is WPFM of 20.40 g L-1 for a water productivity of pulse-irrigated plants noticed. depth of 71.60% ETc. Plants irrigated was superior (p>0.01) in relation to continuously reached a WPFM of 12.97 productivity of continuously-irrigated For fresh mass water productivity, g L-1, replacing 100% of ETc (Figure 2). plants. The average increase observed the authors observed adjustment to This fact highlights the superiority of was 41.12%. Under pulse irrigation, quadratic model to the averages of productivity of water on fresh matter a maximum WPDM of 2.21 g L-1 for obtained data, WPFM of pulse-irrigated of coriander when pulse irrigation a water depth of 68.88% ETc can plants was higher (p>0.01) an average of technique is used. be reached, being this productivity 43.04% in comparison to continuously- superior than the one obtained by irrigated plants (Figure 2A), with For water productivity on dry mass continuous irrigation replacing 100% ETc. As verified for fresh mass water Table 1. Fertigation water depths applied in each treatment. Recife, UFRPE, 2017. productivity, pulse irrigation provided higher water productivity (p>0.01) in Fertigation water Type of application Water depth Total water dry matter (WPDM) of the coriander, depths (%ETc) (mm) depth (mm) except for water depths of 120 and 100% 120 Pulses or continuous 105.6 ETc. This finding demonstrates the 100 Pulses or continuous 88.0 124.8 benefit of pulse irrigation use in WPDM 80 Pulses or continuous 70.4 107.2 of coriander. One plausible explanation 60 Pulses or continuous 52.8 89.6 for the benefit of this technique on 40 Pulses or continuous 35.2 72.0 water productivity in fresh and dry 54.4 matter is that the water application Figure 1. Effect of fertigation water depths on water stress index (WSI) and shoot water content (SWC) on coriander cv. Verdão cultivated under protected environment conditions. Bars represent standard error of averages. Recife, UFRPE, 2017. Figure 2. Analysis of interaction between type of application and fertigation water depths for water productivity in fresh and dry mass production (WPFM, WPDM) of cv. Verdão cultivated under protected environment conditions. Bars represent the standard error of averages; different letters indicate significant differences between treatments by Scott Knott test, P<0.05. Recife, UFRPE, 2017. Hortic. bras., Brasília, v.37, n.1, January-March 2019 25

VRO Zamora et al. Figure 3. Analysis of type of application effect and fertigation water depths in root water content (RWC) (A and B), shoot mass production index (SMPI) (C and D), on root mass production index (RMPI) (E and F) and root-shoot ratio (RSr) (G and H), on coriander cv. Verdão cultivated under protected environment conditions. Bars represent standard error of averages. Different letters indicate significant differences between treatments by Scott Knott test, P<0.05. Recife, UFRPE, 2017. 26 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Pulse drip irrigation and fertigation water depths in the water relations of coriander occurs at practically the same rate as the is directly related to plant water content; area. This root surface increase is evapotranspiration of the crop occurs if water content decreases, a higher caused by a greater need of water and during the day (Abdelraouf et al., 2012). concentration of dry matter in the root nutrient absorption in soil, resulting in occur, to the detriment of the shoot area a decrease of shoot mass, due to greater Root water content (RWC) increased which is the commercial part of the crop. nutrient translocation to form new root linearly in relation to applied water tissue. The opposite was noticed in depths, considering an increase of When plants were pulse irrigated, pulse irrigation: lower RSr indicates a 0.033% for each 1% increase of applied RMPI observed was 20% lower than better condition in relation to water and water depth, independently of the type RMPI of plants continuously irrigated nutrient absorption by the root. of application (Figure 3A). This increase (Figure 3F). The highest RMPI in the is due to the fact that treatments with treatments with continuous irrigation Values of WPFM, WPDM, SWC, higher water depths concentrate higher is directly realted to the fact that water RWC and SMPI were superior for pulse- water content and, therefore, higher deficit stimulates a higher development irrigated plants, whereas RMPI and RSr fresh matter than the treatments in which and root system expansion for deeper and were superior in continuous irrigation. less water is provided. According to wetter soil layers, causing displacement This makes it clear that water deficit was Figure 3B, the authors observed that of a large part of the photoassimilates maintained in this type of application. obtained RWC of the coriander with produced for the greater formation of The reduction of the applied irrigation pulse irrigation was 90.40%, whereas this organ, to the detriment of other water depths increased plant water for continuously-irrigated plants this vegetative and reproductive parts of stress index. Splitting irrigation used in content was 89.41%, which represents the plant (Santos & Carlesso, 1998; this experiment ensured enough water an increase of 1.10%. This increase is Albuquerque, 2015). The opposite content to keep crop quality, besides because the plant was turgid, since less happens in pulse irrigation, where a mitigating the negative effects of water evaporation of soil water was observed, constant wet bulb in the root zone is stress conditions, meaning higher SMPI ensuring the normal maintenance of guaranteed by better water availability and lower RMPI. physiological processes, such as water conditions and lower evaporation and absorption at the cellular level by the deep percolation losses. ACKNOWLEDGEMENTS vacuoles, allowing normal plant growth (UPV, 2017). Evaluating effect of drip pulses and The authors thank CAPES soil cover in formation of wet bulb and (Coordenação de Aperfeiçoamento de Evaluating Figure 3C, it is possible lettuce productivity, Almeida (2012) Pessoal de Nível Superior) and CNPq to verify that an increase of water depth observed a greater superficial root (Conselho Nacional de Desenvolvimento provided an increase of 0.0004% in shoot proliferation in the first centimeters of Científico e Tecnológico) for financial mass production index (SMPI) for each the soil; this fact was attributed to the support for the project. 1% increase in replacement water depth effect of pulse irrigation, considering that independently of the type of application. as water supply occurs more frequently, REFERENCES The authors highlight the importance to it probably favors productivity. observe that as SMPI increases, RMPI ABDELRAOUF, RE; ABOU-HUSSEIN, SD; decreases proportionally, due to higher The improvement generated by the REFAIE, KM; EL-METWALLY, IM. 2012. nutrient and water accumulation in shoot pulses on the bulb wetted in root was Effect of pulse irrigation on clogging emitters, area when comparing to root (Figures also verified by Bakeer et al. (2009), application efficiency and water productivity 3C, 3E). studying the effect of pulse irrigation of potato crop under organic agriculture on potato crop, concluded that replacing conditions. Australian Journal of Basic and Pulse-irrigated plants showed higher 100% of the required humidity, the Applied Sciences 6: 807-816. values for SMPI (p>0.01) in comparison volume of wet soil is greater in pulse to continuously-irrigated plants. The irrigation in 48% than in the continuous ALBUQUERQUE, AHP. 2015. Distribuição da authors concluded that plants under application. umidade do solo no cultivo da goiabeira sob pulse irrigation produced 2.27% more altas frequências de irrigação e diferentes shoot mass than plants under continuous In relation to root-shoot ratio (RSr) coberturas mortas. Ceará: UFC. 87p (Ph.D. irrigation. Adopting pulse irrigation is a linear reduction of 0.0005 per unit thesis). notoriously advantageous since it favors increase of replacement water depth of higher development to shoot part of ETc (Figure 3G) was observed. This ALMEIDA, WF. 2012. Gotejamento por pulsos plant, considering that this is essential decreasing highlights that under water e cobertura do solo na formação do bulbo as this is the commercial part of the crop stress, root growth stimulus and shoot molhado e produtividade da alface americana. (Figure 3D). growth reduction was observed. Minas Gerais: UFLA. 80p (Ph.D. thesis). For root mass production index According to Figure 3H, the authors ALMEIDA, WF; LIMA, LA; PEREIRA, GM. (RMPI), the authors observed as the verified that continuously-irrigated 2015. Drip pulses and soil mulching effect on value of replacement water depth of ETc plants showed RSr 18.18% higher than American crisphead lettuce yield. Engenharia increased in one unit, RMPI decreased plants submitted to pulse irrigation. This Agrícola 35: 1009-1018. in 0.0004%, independently of the type high value of RSr observed in continuous of application (Figure 3E). This decrease application is due to a relative increase BAKEER, GAA; EL-EBABI, FG; EL-SAIDI, of root surface in comparison to shoot MT; ABDELGHANY, ARE. 2009. Effect of pulse drip irrigation on yield and water Hortic. bras., Brasília, v.37, n.1, January-March 2019 use efficiency of potato crop under organic agriculture in sandy soils. Journal of 27

VRO Zamora et al. Agricultural Engineering 26: 736-765. hortaliças de folhas pela técnica de Hidroponia da qualidade e quantidade da água de irrigação NFT. Campinas: Instituto Agronômico. 30p. sobre o coentro cultivado em substrato BENINCASA, MMP. 1988. Análise de inicialmente salino. Revista Brasileira de crescimento de plantas. Noções Básicas. IDSO, SB; JACKSON, RD; REGINATO, RJ. Engenharia Agrícola e Ambiental 2: 22-26. Jaboticabal: FUNEP/FCAV-UNESP. 42p. 1977. Remote-sensing of crop yields. Science 196: 19-25. MERRIAM, JL; KELLER, J. 1978. Farm CASTRO, CN. 2013. A agricultura no nordeste irrigation system evaluation: a guide for brasileiro: Oportunidades e limitações ao JALES, MC; FEITOSA, FAN; KOENING, ML; management. Logan: Utah State University. desenvolvimento. Boletim regional, urbano e BASTOS, RB; MACHADO, RCA. 2012. O 271p. ambiental, Instituto de Pesquisa Econômica ecossistema recifal de Serrambi (nordeste do Aplicada 8: 77-89. Brasil): biomassa fitoplanctônica e parâmetros NASCIMENTO, T; AZEVEDO, CAV; NETO, hidrológicos. Atlântica 34: 87-102. JD; LIMA, VLA; WANDERLEY, JAC. 2013. CAVALCANTI, FLA; SANTOS, JCP; PEREIRA, Velocidade da frente de umidade em neossolo JR.; LEITE, JP; SILVA, MCL; FREIRE, LIMA, AD; NOBRE, JGA; VIANA, TVA; quartzarênico sob irrigação intermitente por FJ; SILVA, DJ; SOUSA, AR; MESSIAS, MOREIRA, LG; AZEVEDO, BMA; gotejamento. Revista Verde de Agroecologia e AS; FARIA, CMB; BURGOS, N; LIMA ALBUQUERQUE, AHP. 2011. Influência Desenvolvimento Sustentável 8: 41-48. JÚNIOR, MA; GOMES, RV; CAVALCANTI, de níveis de irrigação, estimados a partir AC; LIMA, JFVF. 2008. Recomendações de da evaporação medida no evaporímetro de SANTOS, RF; CARLESSO, R. 1998. Déficit adubação para o estado de Pernambuco (2ª Piche, na cultura da mamoneira. Agropecuária hídrico e os processos morfológico e fisiológico aproximação). Recife: IPA. 212p. Técnica 32: 42-48. das plantas. Revista Brasileira de Engenharia Agrícola e Ambiental 2: 287-294. EID, AR; BAKRY, BA; TAHA, MH. 2013. Effect MACIEL, GM; COSTA, CP; SALA, FC. 2012. of pulse drip irrigation and mulching systems Linhagens de coentro com pendoamento tardio UPV Univerdidad Politecnica de Valencia. on yield, quality traits and irrigation water sob dois sistemas de plantio. Horticultura 2017. February 15. La vacuola vegetal y las use efficiency of soybean under sandy soil Brasileira 30: 607-612. sustancias ergasticas. Available http://www. conditions. Agricultural Sciences 4: 249-261. euita.upv.es/varios/biologia/temas/La%20 MAGALHÃES, ACN. 1979. Análise quantitativa Vacuola.htm. FERREIRA, DF. 2011. Sisvar: a computer do crescimento. In: FERRI, MG (ed). statistical analysis system. Ciência e Fisiologia vegetal. São Paulo: USP. p.331-350. WARNER, R; HOFFMAN, O; WILHOIT, J. Agrotecnologia 35: 1039-1042. 2009. The effects of pulsing drip irrigation on MEDEIROS, JF; MEDEIROS, DS; PORTO tomato yield and quality in Kentucky. Fruit FURLANI, PR. 1998. Instruções para o cultivo de FILHO, FQ; NOGUEIRA, ICC. 1998. Efeitos and Vegetable Crop Research Report 1: 39-40. 28 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Research ZEIST, AR; RESENDE, JTV; LIMA FILHO, RB; GABRIEL, A; HENSCHEL, JM; SILVA, IFL. 2019. Phenology and agronomic components of first and second-cycle strawberry. Horticultura Brasileira 37:029-034 DOI - http://dx.doi.org/10.1590/S0102-053620190104 Phenology and agronomic components of first and second-cycle strawberry André R Zeist 1ID; Juliano TV de Resende 2ID; Renato B Lima Filho 3ID; André Gabriel 3ID; Juliane M Henschel 4ID; Israel FL da Silva 3ID 1Universidade do Oeste Paulista (UNOESTE), Presidente Prudente-SP, Brazil; [email protected]; [email protected]; 2Universidade Estadual de Londrina, Londrina-PR, Brazil; [email protected]; 3Universidade Estadual do Centro-Oeste (UNICENTRO), Guarapuava-PR, Brazil; [email protected]; [email protected]; 4Universidade Federal de Viçosa (UFV), Viçosa-MG, Brazil; [email protected] ABSTRACT RESUMO Several strawberry growers have cultivated the same plants Fenologia e componentes agronômicos de morangueiros de for two consecutive cycles aiming a greater economic return after primeiro e segundo ciclo seedling transplant. However, the phenological development and the agronomic potential of second-cycle strawberry have to be estimated. Em busca de maior retorno econômico após o transplantio This research was installed to estimate the thermal need, leaf das mudas, muitos produtores de morango têm feito o cultivo por appearance rate, phyllochron and yield of strawberry cultivars in two dois ciclos consecutivos. No entanto, há necessidade de estimar o consecutive crop cycles in the region of the Third Planalto Paranaense. desenvolvimento fenológico e avaliar o potencial agronômico do Cultivars Camarosa, Camino Real, Albion, Aromas, Monterrey morangueiro nesse sistema. O objetivo deste trabalho foi comparar and San Andreas were evaluated in the first and second growing a necessidade térmica, a taxa de aparecimento foliar, o filocrono e cycles using completely randomized blocks and four replications. a produtividade de cultivares de morangueiro no segundo ciclo de Leaf appearance rate was estimated by linear regression coefficient cultivo, em comparação ao primeiro, na região do Terceiro Planalto between the number of leaves and the accumulated thermal sum. Paranaense. Avaliaram-se as cultivares Camarosa, Camino Real, Phyllochron was estimated by the inverse of regression coefficient. Albion, Aromas, Monterrey e San Andreas, utilizando o delineamento Aromas was the only cultivar with an increased fruit production experimental de blocos ao acaso e com quatro repetições. A taxa de in the second cycle. On the contrary, there was a considerable aparecimento foliar foi estimada a partir do coeficiente angular da reduction of production for ‘Camino Real’, ‘Albion’, ‘Monterrey’ regressão linear entre o número de folhas e a soma térmica acumulada, and ‘San Andreas’ in that same cycle. The highest number and mass enquanto o filocrono foi estimado pelo inverso do coeficiente angular of marketable fruits of the second and first cycles were observed for da regressão. Observou-se que Aromas foi a única cultivar que ‘Camarosa’and ‘Camino Real’, respectively. In the second crop cycle, aumentou a produção de frutos no segundo ciclo. Ao contrário, nesse strawberry cultivars required a lower thermal sum to begin flowering mesmo ciclo houve considerável redução da produção para ‘Camino and fruit harvest. The plants presented a higher leaf appearance rate Real’, ‘Albion’, ‘Monterrey’ e ‘San Andreas’. Destacaram-se com and low phyllochron values. maior número e massa de frutos comerciais do segundo e primeiro ciclo, ‘Camarosa’ e ‘Camino Real’, respectivamente. No segundo ciclo de cultivo, as cultivares de morangueiro necessitaram menor soma térmica acumulada para iniciar o florescimento e colheita dos frutos e, apresentaram maior taxa de aparecimento foliar e menores valores de filocrono. Keywords: Fragaria x ananassa, leaves emission, phyllochron, fruit Palavras-chave: Fragaria x ananassa, emissão de folhas, filocrono, production, thermal sum. produção, soma térmica. Received on November 15, 2017; accepted on September 14, 2018 Strawberry (Fragaria x ananassa) The main strawberry cultivars in should be evaluated on productivity, is cultivated in a wide geographic Brazil derive from genetic improvement quality, growth and vegetative distribution due to its ability to adapt programs conducted in the United development (Tazzo et al., 2015). to different soil and climatic conditions States, with emphasis on ‘Oso Grande’, (Morales et al., 2012). This small ‘Camarosa’, ‘Aromas’, ‘Diamante’, Aiming greater economic returns fruit is the most widely cultivated and ‘Camino Real’, ‘Albion’, Monterey’, after seedling transplanting, many consumed fruit in the world (Tazzo et al., ‘San Andreas’, ‘Palomar’ and ‘Portola’, strawberry producers have cultivated 2015). In Brazil, it is mainly produced in developed at the University of the same plants for two or more small rural properties. In recent years, California; ‘Dover’, ‘Sweet Charlie’and consecutive cycles. Family farmers there has been a considerable increase ‘Florida Festival’, were developed at the in the municipality of Guarapuava- in its production (Witter et al., 2012). University of Florida. These materials PR, located in the region of the Third Planalto Paranaense, have reported Hortic. bras., Brasília,v.37, n.1, January-March 2019 29

AR Zeist et al. that production is lower in the second verified that there was variability among Chile in 2013, certified and diseases production cycle than in the first one. them, with a lower phyllochron value for free, cultivated during the 2013-2014 However, fruits are produced earlier, selection 1 (69.96º day leaf-1) and a higher harvest. Seedlings were kept in the thus guaranteeing a high market value. value for the Albion cultivar (135.61º same place of cultivation of the previous In that municipality, approximately day leaf-1). Mendonça et al. (2012a) cycle in 2014, in a low tunnel. They 60 tons of strawberry were harvested verified a variation in phyllochron were managed according to climatic in 2017, amounting approximately values among strawberry cultivars in elements, subjected to removal of all R$ 900,000. However, there is yet no strawberry intercropped with fig trees leaves (toilet) on June 20, 2014, and then scientific information on the productive and in single crop. used to conduct one of the experiments. potential of strawberry in the second The first-cycle plants were commercial cycle compared to the first one. Although there is information on seedlings imported from Chile in 2014, phyllochron for strawberry cultivars, it is and transplanted to the field at the The knowledge on the phenological necessary to identify their phenological beginning of July in order to conduct behavior of a particular plant species performance at the site of cultivation the other experiment. or cultivar is of extreme importance (Tazzo et al., 2015). In addition, there since it is a tool for forecasting events is a need to determine the growth, The cultivars of both cycles were and making decisions regarding crop development and agronomic potential planted in a 0.8 m-high tunnel system, management (Pereira et al., 2010; of second-cycle strawberry. Considering covered with a transparent 75-micra Tomazetti et al., 2015). Among the the aforementioned information, the low-density polyethylene film (LDPE), factors closely related to changes in objective of this study is to estimate on beds 1.0 m wide and 0.25 m phenological stages, temperature is the thermal needs, leaf emission rate, high, covered with a 50-micra black most relevant. It results in thermal energy phyllochron and yield of strawberry polyethylene film. Plants were arranged and drives vegetative development and cultivars in second crop cycle in in a quincunx, on 30x30 cm spacing. growth (Liu & Heins, 2002). In first- comparison to the first cycle in the cycle strawberry plants, there is a close Terceiro Planalto region of Paraná. Based on chemical analysis, the relationship between temperature and soil was corrected three months before vegetative canopy formation (Mendonça MATERIAL AND METHODS transplanting by applying 50.0 g per m2 et al., 2012a,b,c; Tazzo et al., 2015). of dolomitic limestone (75% PRNT), However, similar to the productive The experiments were conducted at in order to reach 80% base saturation. potential, second-cycle plants may the Center for Research on Vegetables At the moment of transplanting the present a different developmental of the Department of Agronomy of first-cycle and pruning second-cycle response to air temperature. the State University of the Center- leaves, 200 g single superphosphate, West (UNICENTRO) located in the 25 g potassium chloride, 25 g urea and A biologically realistic measurement municipality of Guarapuava, Paraná 2.5 kg cattle manure were applied on the for estimating growth and development (25°38’S, 51°48’W, 1,100 meters surface of each plot and incorporated regarding air temperature is the thermal altitude). This region belongs to the into the soil, as recommended by sum (°C days) (Streck et al., 2008; Third Planalto Paranaense. The climate, Henschel et al. (2017). Heldwein et al., 2010; Lucas et al., according to Köppen’s classification, is 2012). It has a greater meaning regarding Cfb (humid mesothermic subtropical), Phytosanitary control was plants than calendar days. Based on the temperate, with no defined dry season, performed using preventive sprays thermal sum, it is possible to estimate hot summers and moderate winters of commercial products containing the number of leaves in strawberry by (Wrege et al., 2011). The soil is classified thiamethoxam (Actara) and azoxystrobin means of phyllochron (°C day leaf-1), as typical dystroferric Bruno Latosol + diphenoconazole (Amistar Top) which is the time interval between the (Embrapa, 2013). according to technical manufacturer appearance of two successive leaves recommendations. Irrigation was in the main canopy (Xue et al., 2004; The strawberry cultivars Camarosa, performed by micro-drips according to Streck et al., 2005). Camino Real (short-day cultivars), practical observations of crop’s water Albion, Aromas, Monterrey and San requirement. Studies using the phyllochron Andreas (neutral day cultivars) were concept have been carried out on several evaluated in the second and first cycles During the experimental periods, agricultural species, such as barley and in 2014. The experimental design daily data of minimum (Tn) and wheat (Xue et al., 2004), safflower was randomized blocks with four maximum (Tx) air temperatures (Streck et al., 2005), lettuce (Hermes replications, with each plot consisting were collected at the automatic et al., 2001), eucalyptus (Martins et of twelve useful plants. The two crop meteorological station of the Center- al., 2007) and tomato (Pivetta et al., cycles were studied in individualized West State University, located 120 m 2007). Regarding strawberry, Tazzo et experiments. from the experiment. In second-cycle al. (2015) evaluated the phyllochron in plants, the number of leaves (NL) of two selections (‘SEL1’ and ‘SEL2’) and Second-cycle plants were each plant was counted after thinning. in the cultivars Camino Real, Camarosa, commercial seedlings imported from For the first cycle, NL count was San Andreas and Albion. The authors performed after leaf emission. A leaf is new when it is at least 1 cm long. The 30 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Phenology and agronomic components of first and second-cycle strawberry NL count was performed every five the ASSISTAT software, version 7.7 (October 15th), Tx ranged from 11.0ºC days until the beginning of fruit harvest. (Silva & Azevedo, 2016). (July 25th) to 33.6°C (October 17th), and During the cycle, the time when plants Tn values ranged from 8.0°C (July 1st) started flowering was also recorded. It RESULTS AND DISCUSSION to 25.0°C (October 10th). During the was defined when 50% of the plants had observations, there was an incidence at least one inflorescence per plant. The Due to the significant interaction of minimum temperatures below the beginning of the harvest was defined between cycles and genotypes, results base temperature (7.0ºC) at 14 and 12 when at least 50% of plants had at least will be presented separately. days for second and first-cycle plants, one fruit at harvest stage. respectively (Figure 1). During the observation periods The fruits were harvested at a (June to October 2014) for second-cycle The values of daily thermal sum maturation stage with 2/3 red staining. strawberry cultivars, the minimum (TSd) for cultivars in the second cycle They were evaluated in their production temperature values (Tn) ranged from ranged from 1 to 13ºC day. In the first components: number of marketable -2.0ºC (July 1st) to 15.6ºC (September cycle, values ranged from 1 to 18ºC fruits (NCF, plant fruit-1), total number 2nd) and the maximum temperatures day. The beginning of flowering of all of fruits (TNF, plant fruits-1), mass (Tx) ranged from 11.0ºC (July 25th) cultivars in the second cycle occurred of marketable fruits (MCF, g plant-1) to 27.2ºC (August 24th). For average with an accumulated thermal sum and total fruit mass per plant (TFM, air temperatures (Tm), the range was (TSa) of 188.8ºC day, lower than the g plant-1). Fruits were considered from 8.0ºC (July 1st) to 20.0°C (August first cycle, which was 381.9ºC day for marketable with a mass greater than 10 24th). For first-cycle plants, Tn values short-day cultivars and 316.4ºC for g without defects (wilted, deteriorated, ranged from -2.0ºC (July 1st) to 19.2ºC neutral-day cultivars (Table 1). malformed, mechanically damaged or attacked by diseases or pests). Figure 1. Minimum (Tn, °C), maximum (Tx, °C) and average air temperatures (Tm, ºC) and daily thermal sum (TSd, ºC day) during the periods considered to estimate phyllochron The daily thermal sum (TSd, °C in strawberry cultivars of second (A) and first (B) cycles in the Third Planalto Paranaense day) was calculated as proposed by region. Guarapuava, UNICENTRO, 2014. Arnold (1960): TSd = (Tm - Tb) * 1 day (1). The mean air temperature (Tm) was determined by the arithmetic average between Tn and Tx of the air. Tb is the base temperature for strawberry leaf emission, below which there is no emission of new leaf structures. The adopted Tb was 7.0°C (Mendonça et al., 2012a; Tazzo et al., 2015). The accumulated thermal sum (TSa, °C day) was defined by summing the daily values (TSa = ΣTSd). The leaf appearance rate (LAR, leaf °C day-1) was estimated using linear regression coefficient between the NL and the accumulated thermal sum (TSa, °C day). The phyllochron (ºC day leaf-1) of each plant was estimated by the inverse of the linear regression coefficient between NL and TSa (Streck et al., 2005; Martins et al., 2007; Pivetta et al., 2007). The data of the evaluated characteristics were tested for normality and homogeneity of residual variances by Lilliefors & Bartlett tests, respectively, and later submitted to analysis of variance, individually and combining both experiments. When the F test was significant, means were submitted to comparison by Tukey test at 5% probability and analyzed using Hortic. bras., Brasília, v.37, n.1, January-March 2019 31

AR Zeist et al. Table 1. Phenological cycle of defoliation/transplanting at the beginning of flowering (D/T - Fl) and defoliation/transplanting at the beginning of fruit harvest (D/T - BFH) of strawberry cultivars of second and first cycles in the Third Planalto Paranaense region. Guarapuava, UNICENTRO, 2014. Genotype Defoliation Second cycle D - BFH (TSd) D - Fl (TSd) Camarosa 06/20/2014 07/13/2014 (188.8ºC day) 09/02/2014 (598.5ºC day) Camino Real 06/20/2014 07/13/2014 (188.8ºC day) 09/02/2014 (598.5ºC day) Albion 06/20/2014 07/13/2014 (188.8ºC day) 09/02/2014 (598.5ºC day) Aromas 06/20/2014 07/13/2014 (188.8ºC day) 09/02/2014 (598.5ºC day) Monterrey 06/20/2014 07/13/2014 (188.8ºC day) 09/02/2014 (598.5ºC day) San Andreas 06/20/2014 07/13/2014 (188.8ºC day) 09/02/2014 (598.5ºC day) First cycle Transplanting T - Fl (TSd) T - BFH (TSd) Camarosa 07/01/2014 08/19/2014 (381.9ºC day) 10/19/2014 (1,076.5ºC day) Camino Real 07/01/2014 08/19/2014 (381.9ºC day) 10/17/2014 (1,045.3ºC day) Albion 07/01/2014 08/10/2014 (316.4ºC day) 10/12/2014 (961.9ºC day) Aromas 07/01/2014 08/10/2014 (316.4ºC day) 10/12/2014 (961.9ºC day) Monterrey 07/01/2014 08/10/2014 (316.4ºC day) 10/12/2014 (961.9ºC day) San Andreas 07/01/2014 08/10/2014 (316.4ºC day) 10/06/2014 (873.0ºC day) Table 2. Leaf appearance rate (LAR), phyllochron and coefficient of determination (R2) of linear regressions between the number of leaves and the accumulated thermal sum of strawberry cultivars of second and first cycles in the Third Planalto Paranaense region. Guarapuava, UNICENTRO, 2014. Genotype LAR (leafºC day-1) Phyllochron (ºC day leaf-1) R2 Second First Second First Second First Camarosa 0.0244 Ab* 0.0085 Babc 41.0 Bb* 117.9 Ac 0.95 0.96 Camino Real 0.0171 Ac 0.0084 Babc 58.6 Ba 120.0 Ac 0.95 0.96 Albion 0.0163 Ac 0.0070 Bbc 61.3 Ba 142.4 Ab 0.95 0.97 Aromas 0.0241 Ab 0.0109 Ba 41.8 Bb 91.8 Ae 0.95 0.96 Monterrey 0.0326 Aa 0.0062 Bc 31.0 Bc 160.8 Aa 0.93 0.94 San Andreas 0.0155 Ac 0.0097 Ba 66.8 Ba 103.5 Ad 0.96 0.97 CV (%) 8.7 5.1 - *Means followed by different uppercase letters on lines and different lowercase letters in columns differ by Tukey test,<5% probability. Due to the early flowering of second- cultivars Camino Real, Camarosa, San prediction of management activities and cycle cultivars, the beginning of fruit Andreas and Albion. This demonstrates the scheduling of the harvest period of harvest was also anticipated, beginning that the thermal sum is a realistic strawberry fruits (Tazzo et al., 2015). when TSa reached 598.5ºC day. In the measurement to estimate the growth first cycle, a higher TSa was required to and development of strawberry from a The regressions between the number reach the fruit harvest point. The thermal biological point of view. of leaves (NL) and TSa carried out to accumulation for the cultivar San obtain leaf appearance rate (LAR) and Andreas was 873.0ºC day, for Albion, Among the cultivars in the first phyllochron estimates showed a close Aromas and Monterrey was 961.9ºC cycle, there was variation of TSa needs relation (R2≥0.93) for combinations day, for Camino Real was 1,045.3ºC to start the flowering and maturation (cultivars x cycles) (Table 2). R2≥0.93 day, and for Camarosa was 1,076.5ºC of fruits (Table 1).This indicates that values indicate the existence of linearity day (Table 1). the phenological behavior based on between NL and TSa. The values also thermal energy should also be taken indicated that air temperature is an The TSa values of this work for the into account in the choice of cultivars abiotic element highly related to the beginning of flowering and harvesting to be planted in a given geographic appearance of leaves in strawberry of first-cycle fruits are close to those region. The knowledge on the response cultivars. This corroborates with the observed by Tazzo et al. (2015) for the of phenological stages enables the studies by Mendonça et al. (2012a) and 32 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Phenology and agronomic components of first and second-cycle strawberry Tazzo et al.(2015). fact that plants presented a developed second-cycle Camarosa showed the root system and were acclimatized highest TNF (82.6 fruits) (without By comparing second-cycle to the environmental conditions after differing from Aromas), the highest cultivars, Monterrey presented the transplanting. On the other hand, first- TFM (719.2 g) and NCF (35.3 fruits) highest LAR (0.0326 leaf ºC day-1) and cycle cultivars underwent stresses due (without differing from Aromas), and the lowest phyllochron (31.0ºC day leaf-1). to the transplant process and used the the highest MCF (410.7 g). In general, For the same cycle, cultivars Camino first assimilates for the growth and although Camarosa did not stand out Real, Albion and San Andreas presented development of the root system. In for production components related to the lowest values of LAR and the highest addition, there were several lateral marketable fruits in the first cycle, it values of phyllochron. In the first cycle, “canopies” in the second-cycle plants. presented the highest potential to be Monterrey had the lowest LAR (0.0062 Each canopy emitted several leaves. On cultivated for two consecutive cycles leaf ºC day-1), without differing from the contrary, seedlings initially present a (Table 3). Camarosa, Camino Real and Albion. single canopy in first-cycle plants, which It also had the highest phyllochron represents a low number of leaves, low In relation to the first cycle after (160.8ºC day leaf-1). Cultivars Aromas LAR and a greater phyllochron. transplanting, Camino Real obtained and San Andreas had the highest LAR, the highest TNF (112.3 fruits) (without without differing from Camarosa and Only cultivar Aromas showed a differing from Camarosa, Monterrey Camino Real. Aromas obtained the gain in production components in the and San Andreas), the highest TFM lowest phyllochron (Table 2). second cycle compared to the first (1,012.7 g), the highest NCF (66.7 fruits) cycle. Camino Real, Albion, Monterrey (without differing from Albion) and the There was a higher LAR and a lower and San Andreas presented higher total highest MCF (907.0 g). However, when phyllochron for all cultivars in the number of fruits (TNF), total fruit mass Camino Real was cultivated for the second cycle (Table 2). If LAR is high (TFM), number of marketable fruits second consecutive cycle, it presented a and phyllochron is low, plants should (NCF) and mass of marketable fruits decrease in TNF, TFM, NCF and MCF have a greater efficiency for emission (MCF) in the first crop cycle (Table 3). (Table 3): 43.9, 40.9, 30.6 and 24.0%, of leaves in function of air temperature. respectively. Higher LAR, lower phyllochron and For Camarosa, there was no anticipation of flowering start and difference in production components Although the cultivars Camino Real, harvest of fruits, of plants managed in between both crop cycles. When Albion, Monterrey and San Andreas the second cycle, possibly are due to the compared to the other cultivars, the showed lower yields in the second cycle, compared to the first cycle, the Table 3. Total number of fruits (TNF), total fruit mass (TFM), number of marketable fruits use of second-cycle strawberry plants (NCF) and mass of marketable fruits (MCF) of strawberry cultivars of second and first cycles is an interesting alternative because it in the Third Planalto Paranaense region. Guarapuava, UNICENTRO, 2014. allows costs reduction in importation of seedlings, anticipation of fruit harvest Genotype TNF (plant fruits-1) TFM (g plant-1) and a greater market value. However, strawberry plants cultivated in second Second First Second First cycle present higher risk of pests and diseases incidence. The pruning of Camarosa 82.6 Aa 99.32Aab 719.2 Aa 773.3 Ac leaves in late fall is required, associated with preventive phytosanitary crop Camino Real 49.3 Bbc 112.3 Aa 414.1 Bc 1012.7 Aa management. Albion 19.5 Bc 83.3 Ab 166.3 Bd 882.7 Ab Phenological components, in function of thermal sum calculated by Aromas 74.3 Aa 49.7 Bc 621.6 Ab 354.0 Bd the representation of biological time, are a widely used method. This method Monterrey 59.1 Bb 95.0 Aab 571.4 Bbc 777.6 Ac allows improving the prediction of dates of vegetative development stages San Andreas 57.3 Bb 101.0 Aab 444.2 Bc 768.1 Ac (Zeist et al., 2017). Based on these components, the strawberry cultivars CV (%) 17.3 19.7 analyzed in this work, cultivated on the second consecutive cycle, require NCF (plant fruits-1) MCF (g plant-1) less thermal energy for emission of leaves, for flowering and for harvest. Second First Second First Such thermal values make it possible to stipulate the duration of development Camarosa 35.3Aa* 37.0 Ac 410.7 Aa 482.0Ad stages according to thermal conditions. It allows a better decision-making Camino Real 20.4 Bb 66.7 Aa 218.3 Bc 907.0 Aa regarding the most appropriate Albion 9.0 Bc 67.0 Aa 105.0 Bd 784.3 Ab Aromas 30.9 Aa 13.7 Bd 343.7 Ab 160.0 Be Monterrey 25.1 Bb 59.7 Ab 321.8 Bb 643.0 Ac San Andreas 21.5 Bb 57.3 Ab 226.6 Bc 622.8 Ac CV (%) 16.2 18.5 *Means followed by different uppercase letters on lines and different lowercase letters in columns differ by Tukey test,<5% probability. Hortic. bras., Brasília, v.37, n.1, January-March 2019 33

AR Zeist et al. management in two consecutive cycles plastocrono de plantas de melancia. Revista SCHUH, M. 2005. Estimating leaf appearance of cultivation. However, depending Ciência Agronômica 43: 288-292. and phyllochron in safflower (Carthamus on the strawberry cultivar, there is a tinctorius L.). Ciência Rural 35:1448-1450. considerable decrease in fruit production MARTINS, FB; SILVA, JC; STRECK, NA. 2007. in the second crop cycle. Estimativa da temperatura-base para emissão STRECK, NA; PAULA, GM; CAMERA, C; de folhas e do filocrono em duas espécies de MENEZES, NL; LAGO, I. 2008. Estimativa REFERENCES eucalipto na fase de muda. Revista Árvore do plastocrono em cultivares de soja. Bragantia 31: 373-381. 67: 67-73. ARNOLD, CY. 1960. Maximum-minimum temperature as a basis for computing heat MENDONÇA, HFC; CALVETE, EO; NIENOW, TAZZO, IF; FAGHERAZZI, AF; LERIN, SK; units. Proceedings of the American Society for AA; COSTA, RC; ZERBIELLI, L; BONAFÉ, AIKE, A; RUFATO, L. 2015. Exigência Horticultural Science 76: 682-692. M. 2012a. Estimativa do filocrono de térmica de duas seleções e quatro cultivares de morangueiro em sistemas consorciado e morangueiro cultivado no planalto catarinense. EMBRAPA - Empresa Brasileira de Pesquisa solteiro em ambientes protegidos. Revista Revista Brasileira de Fruticultura 37: 550- Agropecuária. 2013. Sistema brasileiro de Brasileira de Fruticultura 34: 15-23. 558. classificação de solos. 3.ed. Rio de Janeiro: Embrapa Solos. 353p. MENDONÇA, HFC; MÜLLER, AL; BOENO, TOMAZETTI, TC; ROSSAROLLA, MD; MC; ZERBIELLI, L; BONAFÉ, M; TAZZO, ZEIST, AR; GIACOBBO, CL; WELTER, HELDWEIN, AB; STRECK, NA; STURZA, IF; CALVETE, EO; NIENOW,AA. 2012b. The LJ; ALBERTO, CM. 2015. Fenologia e VS; LOOSE, LH; ZANON, AJ; TOEBE, M; phyllochron of strawberry intercropped with acúmulo térmico em videiras viníferas na SOUZA, AT; PETERS, MB; KARLEC, F. fig trees in a greenhouse. Acta Horticulturae região da Fronteira Oeste do Rio Grande do 2010. Plastocrono e rendimento de feijão-de- 926: 547-550. Sul. Pesquisa Agropecuária Brasileira 50: vagem cultivado sob ambiente protegido e 1033-1041. no ambiente externo em semeadura tardia no MENDONÇA, HFC; MÜLLER, AL; TAZZO, outono. Ciência Rural 40: 768-773. IF; CALVETE, EO. 2012c. Accumulated leaf WITTER, S; RADIN, B; LISBOA, BB; number in strawberry cultivars grown in a TEIXEIRA, JSG; BLOCHTEIN, B; HENSCHEL, JM; RESENDE, JTV; GILONI- greenhouse. Acta Horticulturae 926: 295-300. IMPERATRIZ-FONSECA, VL. 2012. LIMA, PC; ZEIST, AR; LIMA FILHO, RB; Desempenho de cultivares de morango SANTOS, MH. 2017. Production and quality MORALES, RGF; FARIA, MV; RESENDE, JTV; submetidas a diferentes tipos de polinização of strawberry cultivated under different colors RISSINI, ALL; CARMINATTI, R; FARIA, em cultivo protegido. Pesquisa Agropecuária of low tunnel cover. Horticultura Brasileira CMD. 2012. Produtividade do morangueiro em Brasileira 47: 58-65. 35: 364-370. função da adubação orgânica complementar em cultivo protegido. Ambiência 8: 23-33. WREGE, MS; STEINMETZ, S; REISSER HERMES, CC; MEDEIROS, SLP; MANFRON, JUNIOR, C; ALMEIDA, IR. 2011. Atlas PA; CARON, B; POMMER, SF; BIANCHI, PEREIRA, LC; CAMPELO JÚNIOR, JH; climático da Região Sul do Brasil: Estados CAM. 2001. Emissão de folhas de alface em FERRONATO, A. 2010. Comparação de do Paraná, Santa Catarina e Rio Grande do função da soma térmica. Revista Brasileira de métodos para estimativa do plastocrono em Sul. 1. Pelotas: Embrapa Clima Temperado; Agrometeorologia 9: 269-275. algodoeiro em condições tropicais. Pesquisa Colombo: Embrapa Florestas, 336p. Agropecuária Tropical 40: 213-220. LIU, B; HEINS, D. 2002. Photothermal ratio XUE, Q; WEISS, A; BAENZIGER, PS. 2004. affects plant quality in ‘Freedom’ Poinsettia. PIVETTA, CR; TAZZO, IF; MAASS, GF; Predicting leaf appearance in field-grown Journal of the American Society for STRECK, NA; HELDWEIN, AB. 2007. winter wheat: evaluating linear and non-linear Horticultural Science 127: 20-26. Emissão e expansão foliar em três genótipos models. Ecological Modelling 175: 261-270. de tomateiro (Lycopersicon esculentum Mill.). LUCAS, DDP; STRECK, NA; BORTOLUZZI, Ciência Rural 37: 1274-1280. ZEIST, AR; TOMAZETTI, TC; ROSSAROLLA, MP; TRENTIN, R; MALDANER, IC. 2012. MD; ALBERTO, CM; GIACOBBO, CL; Temperatura base para emissão de nós e SILVA, FAS; AZEVEDO, CAV. 2016.The Assistat WELTER, LJ. 2017. Plastochron index of Software Version 7.7 and its use in the analysis ‘Cabernet Sauvignon’ and ‘Chardonnay’ of experimental data. African Journal of grapevines in Fronteira Oeste, in the state Agricultural Research 11: 3733-3740. of Rio Grande do Sul, Brazil. Pesquisa Agropecuária Brasileira 52: 244-251. STRECK, NA; BELLÉ, RA; ROCHA, EK; 34 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Research FERREIRA, MG; ALMEIDA, GQ; PESSOA, HP; DARIVA, FD; DIAS, FO; NICK, C. 2019. Selection of squash “Menina Brasileira” carrying the allele “Bush” with high yield potential. Horticultura Brasileira 37: 035-039 DOI - http://dx.doi.org/10.1590/S0102-053620190105 Selection of squash “Menina Brasileira” carrying the allele “Bush” with high yield potential Mariane G Ferreira ¹ID; Gabriella Q de Almeida ¹ID; Herika P Pessoa ¹ID; Françoise D Dariva ¹ID; Felipe de O Dias ¹ID; Carlos Nick¹ID ¹Universidade Federal de Viçosa (UFV), Viçosa-MG, Brazil; [email protected]; [email protected]; [email protected]; [email protected]; [email protected]; [email protected] ABSTRACT RESUMO This study was performed to introduce the allele Bush of Seleção de populações de abóbora menina brasileira commercial cultivars with a bush growth habit into Cucurbita portadoras do alelo “Bush” com alto potencial produtivo moschata accessions and select the best crossings for production potential and standard fruit shape “Menina Brasileira” through Objetivou-se introduzir o alelo Bush, de cultivares com hábito general combining ability (GCA) and specific combining ability de crescimento tipo “moita”, em acessos de Cucurbita moschata e (SCA). To determine GCA and SCA, a partial diallel analysis was selecionar os melhores cruzamentos quanto ao potencial produtivo performed. The parental group (group I) consisted of two cultivars e ao formato de fruto padrão “menina brasileira” por meio da containing the dwarfism bush gene, and the second group (Group II), capacidade geral (CGC) e da capacidade específica (CEC) de formed by five accessions of UFV Vegetable Germplasm Bank, with combinação. Para determinar a CGC e a CEC foi realizada análise high production potential and fruit shape “Menina Brasileira”. We dialélica parcial. O grupo parental (grupo I) foi formado por duas evaluated: productivity (PROD), fruit shape (FORM), growth rate cultivares tipo “moita”, enquanto o segundo grupo (grupo II) por until the 50th day after transplanting (CRESC), and length of the main cinco acessos do Banco de Germoplasma de Hortaliças da UFV, com stem on the 50th day (COMP). Significant differences were noticed alto potencial produtivo e formato de fruto “menina brasileira”. Foram for CRESC and COMP only between GCA of parents belonging to avaliadas a produtividade (PROD), o formato de fruto (FORM), a group I, in which Zapallo stood out. For PROD and FORM, diallel taxa de crescimento até os 50 dias (CRESC) e o comprimento da analysis proved to be efficient in studying GCA effects. Cultivar rama principal aos 50 dias (COMP). Para CRESC e COMP, houve Piramoita (group I) and accessions BGH-4360 and BGH-5253 diferenças significativas apenas entre a CGC dos genitores do grupo (group II) showed positive values for GCA, suggesting that these I, onde destacou-se a cultivar Zapallo. Para as características PROD parents possess a higher frequency of favorable alleles for these two e FORM a análise dialélica mostrou-se eficiente no estudo dos traits. Significance in SCA effects was also verified, highlighting efeitos de CGC. A cultivar Piramoita (grupo I) e os acessos BGH- the crossing Piramoita x BGH-4360, for PROD, indicating that this 4360 e BGH-5253 (grupo II) apresentaram valores positivos para combination is the most promising for breeding purposes. CGC, o que indica que esses genitores possuem maior frequência de alelos favoráveis para essas duas características. Também houve significância nos efeitos da CEC, com destaque para o cruzamento Piramoita x BGH-4360, para a característica PROD, sendo essa, a combinação mais promissora e mais indicada para seguir no programa de melhoramento de abóboras. Keywords: Cucurbita moschata, plant architecture, “bush type”, Palavras-chave: Cucurbita moschata, arquitetura de planta, tipo genetic resources, vegetable breeding. “moita”, recursos genéticos, melhoramento de hortaliças. Received on November 27, 2017; accepted on July 16, 2018 Cucurbits play an important role & Silva, 2005; Resende et al., 2013). in cell size in this region, which is a in human nutrition mainly in Corroborating this statement, Wu et result from drastic reduction of the tropical and subtropical regions (Glala al. (2007) highlight that the species C. content of gibberellins associated with et al., 2011). In Brazil, this plant is moschata sends branches which spread the presence of the bush gene (Lopez- grown mainly in the Northeast region and can reach 15 meters long. Juez et al., 1995), which culminates in where it is used for human and animal plant size reduction (Wu et al., 2007). nutrition (Aruah et al., 2012). Among Few studies on genetic control of The dominant homozygous bush gene cucurbits, squash is considered a very growth habit can be found in literature promotes the compact growth of plants expansive crop due to its indeterminate (Vallejo & Mosquera, 1998), however it of the genus Cucurbita, reducing the growth habit and long internodes. One is known that gene “Bush” is responsible internode length from 15 cm to 2 cm, single plant is able to cover an useful for compact growth habit in this genus in average (Zhang et al., 2012). area ranging from 12 to 25 m2 (Puiatti (Robinson et al., 1976). The reduction of internode results from a decrease Squash plants with reduced growth Hortic. bras., Brasília,v.37, n.1, January-March 2019 35

MG Ferreira et al. habit show advantages, and, among cultivars Piramoita and Zapallo de days after transplanting (cm day-1), them, the possibility of planting a larger Tronco, cultivars belonging to the weekly calculated until 50 days after population by area, greater earliness species C. moschata and C. maxima, transplanting, and main stem growth, 50 of plants (Maynard et al., 2002) and respectively; the second group was days after transplanting (cm). easier conducting of cultural practices formed by accessions of C. moschata: and harvest. Moreover, an increase in BGH-1956, BGH-4360, BGH- In order to evaluate hybrid productivity can be obtained, since 5253, BGH-5621 and BGH-7663. combination performance, the authors in spite of the fact that the fruits are The accessions of BGH-UFV were compared these hybrid combinations smaller, the quantity is greater (Wu et previously identified as plant genetic with cultivars Sandy and Daiane, both al., 2007). resources of high productive potential showing the same fruit shape “menina and standard fruit shape “menina brasileira” (Sakata Sudamerica). The Studies on heterotic and brasileira”. The cultivars carry the gene comparison was done using analysis combinatorial effects, which involve “Bush” in dominant homozygosity of variance and mean grouping test of accessions of germplasm banks, have which gives them the bush growth Scott-Knott. been carried out in relation to species habit. The ten hybrids F1 were obtained breeding. This indicates accessions through manual crossings for the Then, the authors calculated average which can be integrated into improved introgression of the “Bush” gene. The squares and estimates of general populations and expand their genetic commercial cultivars were used as combining ability (GCA) and specific base (Machado & Miranda, 2003). pollen donors, whereas the accessions combining ability (SCA) in diallel Besides that, this information may allow were used as receptors, being the ovary analysis. The diallel analysis was to choose the best strategies in breeding shape that determines fruit type. performed using Method IV adapted program conduction (Azevedo et al., for partial diallels, defined by Griffing 2012; Ferreira et al., 2016). The experiment was carried out (1956). So, observations were described during 2014/2015 spring/summer through the statistical model: In this context, an alternative to harvest in Viçosa, Minas Gerais, genetic improvement is the use of (20°45’14’’S; 42°52’53’’W; 649 m Yij = µ + gi + gj + sij + εij a hybridization program, in order altitude). According to Köppen’s to produce new cultivars adapted classification, the local climate is in which Yij= mean value of hybrid to different purposes, such as small “Cwa”, total average rainfall 1221.4 combination between ith parent of group plants. In order to have a successful mm, with rainfall concentration in 1 and jth parent of group 2; μ= overall breeding program, knowing previously Summer. mean; gi= effect of general combining the behavior of population available in ability of ith parent of group 1; gj= hybrid combinations is important. Thus, Seeds from ten combinations effect of general combining ability of jth an analysis of the combining ability of obtained through the crossings were parent of group 2; si= effect of specific the potential parents allows to identify sown in expanded polystyrene, 72-cell combining ability between parents i those most apt to convey the desirable trays, containing commercial substrate and j, belonging to groups I and II, characteristics to the offspring (Souza for vegetable seedling production. respectively; and εij= mean experimental et al., 2013). Diallel crossing systems Seedlings were transplanted to field with error. are quite efficient to evaluate cultivars, two definitive leaves, approximately 20 since they can indicate the best hybrids, days after sowing, in spacing 3.0x3.0 To obtain contribution of additive and also help choose the most promising m. Hybrids and controls were placed in (GCA) and dominance (SCA) effects parents to be used in hybridization a randomized block design, with three GCA the authors calculated coefficients program (Cruz et al., 2014). replications and five plants per plot, of determination (R²) of each trait, considering useful the three central through ratio between the sum of Thus, the aim of this study was plants. Fertilization was performed squares of GCA and SCA and the sum to introduce the allele “Bush”, of according to recommendations of the of squares of treatments, according to commercial cultivars with bush growth 5th Approach (Ribeiro et al., 1999) for the methodology proposed by Ramalho habit, in accessions of C. moschata squash crop. et al. (2012). The genetic analyses were and select crossings in relation to its carried out using statistical software productive potential and standard fruit The authors analyzed the Genes, v 3.1 (Cruz, 2013). shape “menina brasileira” through characteristics of productivity (kg ha-1); general combining ability (GCA) and fruit shape [using the grading scale: 1= RESULTS AND DISCUSSION specific combining ability (SCA). globular, 2= flattened, 3= disk-shaped, 4= oblong, 5= elliptical, 6= cordiform, Significant effect between cultivars, MATERIAL AND METHODS 7= pyriform, 8= belted, 9= elongated, for all traits, was noticed; this fact 10= upper turbined, 11= crowned, shows genetic variation between the Accessions and commercial cultivars 12= bottom turbined, 13= curved and, cultivars for these traits. Significant were crossed in partial diallel scheme. 14= crooked neck, obtained using a differences for GCA were observed Group I consisted of commercial descriptor table for squash (MAPA, only between cultivars Piramoita and 2004)]; main stem-growth rate, 50 Zapallo Tronco in relation to growth 36 rate up to 50 days and main stem size at Hortic. bras., Brasília, v.37, n.1, January-March 2019

Selection of squash “Menina Brasileira” carrying the allele “Bush” with high yield potential 50 days, and no difference was noticed degrees of complementation among fruit shape. The authors highlight that among accessions. Pandey et al. (2010) individuals belonging to two groups, the accession BGH-5621 of group II reported that information related to GCA where specific hybrid combinations showed positive estimate for fruit shape, effects of parents is essential, since show a difference in the expected despite presenting a negative estimate they successfully help predict genetic phenotypic performance based only for productivity. potential of crossings. on GCA effects. The authors verified, through determination coefficient, a Values relatively high for gi Evaluating plant growth habit in predominance of additive gene effects, showed that the accessions and cultivar all field crossings, the authors noticed since R² values for GCA are always Piramoita showed high frequency of that the plants grew in an indeterminate higher than R² values for SCA, with R² favorable alleles for the evaluated traits form, sending stems throughout their values for GCA of 89.2; 92.8; 72.4; 68.7 (Vencovsky & Barriga, 1992). Thus, growth period, mainly after flowering. and SCA of 10.8; 7.2; 27.6 and 31.3 for these accessions and this cultivar can This phenomenon occurred due to the fruit shape, productivity, growth rate be used in intercrosses with individuals presence of bush gene in heterozygosity up to 50 days and main stem size at 50 belonging to different heterotic groups, (Bubu) in F1 generation, promoting a days, respectively. aiming to form new populations with reversal of dominance and therefore the higher concentration of favorable plants send stems in an indeterminate As a matter of fact, if we take alleles, allowing to provide new superior form, as related by several authors ‘productivity’ as an example, whereas individuals when compared to the who worked with species of the genus GCA values (Table 1) in group II current ones (Cruz et al., 2014). Curcubita (Robinson et al., 1976). ranged from –2531.26 to +8835.77, that means, an amplitude of 11367.03, Hybrid combinations associated The authors verified significant SCA values (Table 2) ranged from with higher estimates of Sij (Table 2) effects for GCA and SCA (p<0.01 and -2505.75 to +2505.75, an amplitude of in relation to productivity were those p<0.05 respectively) for productivity, only 5011.35. The same happens to fruit resulting from the crossings between showing that besides additive, the shape, showing GCA of amplitude 2.0 BGH-4360 x Piramoita (Sij= 2505.75) presence of non additive gene action whereas SCA of only 1.9. Significance and BGH-5253 x Zapallo Tronco was significant among loci related to of GCA shows that additive gene effects (Sij= 2465.11). The two parents of this trait, since SCA does not show are involved in genetic control of the combination BGH-4360 x Piramoita significance in absence of dominance trait. So, the existence of additive gene showed positive estimates of GCA, (Vencovsky & Barriga, 1992). effects for evaluated traits allows us to thus, the authors believe that this assume the possibility of obtaining new combination has a high degree of allelic For fruit shape, GCA for groups cultivars from segregating populations complementation. Hybrid combinations I and II were significant. SCA can be through crossings with tested parents BGH-7663 x Zapallo Tronco (Sij= used to show the best crossings through as suggested by Carvalho et al. (1999). 1482.15), BGH-5621 x Piramoita (Sij= genetic complementarity among the 700.69) and BGH-1956 x Piramoita evaluated parents, since it depends on Cultivar Piramoita belonging to (Sij= 740.81) involved parents with loci with dominance and/or epistasis group I and the accessions BGH-4360 negative estimates of GCA and, effects (Lalla et al., 2010). However, in and BGH-5253 of group II stood out for considering the combinations mentioned the absence of significance for SCA, a productivity and fruit shape, since they above, also showed positive estimates promising combination observing only showed positive estimates of gi (Table of Sij for productivity. However, the the estimates of GCA may be suggested 1). Accession BGH-4360 showed the magnitude of SCA was relatively lower (Ramalho et al., 2012). highest estimate for productivity and for the combinations mentioned above, BGH-5253 the highest estimate for suggesting the occurrence of an average Significant effect of SCA for degree of complementation between productivity also highlights different the mentioned accesses and cultivars (Table 2). Table 1. Estimates of general combining ability for fruit shape, productivity, growth rate of the main stem until the 50th day after transplanting and length of the main stem at the end of For fruit shape, the most favorable the 50th day. Viçosa, UFV, 2015. hybrid combination was BGH-1956 x Piramoita (Sij= 0.97), which showed Parent Fruit shape Productivity Growth rate Stem length the highest positive estimate of Sij, Zapallo Tronco -1.58 -2956.4 -0.63 -43.92 even having a parent belonging to Piramoita 1.58 2956.4 0.63 43.92 group II with negative estimate of DP (gi) 0.19 545.49 0.16 11.82 GCA for this trait. This fact suggests BGH-7663 -0.30 -2531.26 0.08 -2.62 that this crossing shows high degree BGH-5621 0.20 -8017.18 -0.51 -48.55 of allelic complementation between BGH-1956 -0.97 -1027.92 0.09 5.80 parents. Similar result was observed BGH-5253 1.03 2740.59 0.66 51.60 for combination BGH-5253 x Zapallo BGH-4360 0.32 8835.77 -0.32 -6.23 Tronco (Sij= 0.81), in which parent of DP (gj) 0.38 790.99 0.32 23.64 group I also presented negative estimate Hortic. bras., Brasília, v.37, n.1, January-March 2019 37

MG Ferreira et al. Table 2. Estimates of specific combining ability for fruit shape, productivity, growth rate resources for this project development. of the main stem until the 50th day after transplanting and length of the main stem at the end of the 50th day. Viçosa, UFV, 2015. REFERENCES Treatments Fruit Productivity Growth Stem ARUAH, BC; UGURU, MI; OYIGA, BC. 2012. shape rate length Genetic variability and inter-relatioship among some Nigerian pumpkin accessions (Cucurbita BGH-7663 X Zapallo Tronco -0.30 1482.15 -0.24 -19.36 spp.). International Journal of Plant Breeding BGH-7663 X Piramoita 0.30 -1482.15 0.24 19.36 6: 34-41. BGH-5621 X Zapallo Tronco 0.20 0.20 BGH-5621 X Piramoita -0.20 -700.69 -0.20 4.58 AZEVEDO, AM; ANDRADE JÚNIOR, VC; BGH-1956 X Zapallo Tronco -0.97 700.69 -0.29 -4.58 PEDROSA, CE; FERNANDES, JSC; BGH-1956 X Piramoita 0.97 -740.81 0.29 -26.28 VALADARES, NR; FERREIRA, MRA; BGH-5253 X Zapallo Tronco 0.81 740.81 -0.46 26.28 MARTINS, RAV. 2012. Desempenho BGH-5253 X Piramoita -0.81 2465.11 0.46 -31.53 agronômico e variabilidade genética em BGH-4360 X Zapallo Tronco -0.26 -2485.11 0.79 31.53 genótipos de couve. Pesquisa Agropecuária BGH-4360 X Piramoita 0.26 -2505.75 -0.79 72.58 Brasileira 47: 1751-1758. DP(Sij) 0.38 2505.75 0.32 -72.58 790.99 23.65 CARVALHO, ACPP; LEAL, NR; RODRIGUES, R; COSTA, FA. 1999. Capacidade de of GCA for fruit shape (Tables 1 and 2). accessions, confirming the presence combinação para oito caracteres agronômicos of favorable alleles related to positive em cultivares de feijão de vagem de The authors used the average test value of general combining ability. crescimento determinado. Horticultura for evaluated traits in order to compare Brasileira 17: 102-105. the agronomic performance of hybrid For main stem size at 50 days, the combinations with the performance authors noticed emission of stems after CRUZ, CD. 2013. Genes: a software package of commercial cultivars. This test is flowering in all hybrid combinations. for analysis in experimental statistics and necessary due to the fact that when Although significant differences quantitative genetics. Acta Scientiarum diallel crossings are performed, positive between treatments were verified, the Agronomy 35: 271-276. values of GCA and SCA can only show results for growth rate of the main stem that the parent or crossing is superior are not conclusive in this study. More CRUZ, CD; REGAZZI, AJ; CARNEIRO, PCS. to the average of other tested parents combinations for generation F2, for a 2014. Modelos Biométricos Aplicados ao or crossings in that experiment. These possible dominant homozygous bush Melhoramento Genético. Viçosa: UFV. 514p. values do not show if a parent or hybrid gene, are necessary. combination has superior or similar FERREIRA, MG; SALVADOR, FV; LIMA, MNR; agronomic performance when compared The authors concluded that dominant AZEVEDO, AM; NETO, IDSL; SOBREIRA, to commercial cultivars, though. bush allele was introduced into plants of FM; SILVA, DJH. 2016. Parâmetros genéticos, generation F1. Partial diallel analysis dissimilaridade e desempenho per se em Hybrid combinations and showed to be efficient in the study on acessos de abóbora. Horticultura Brasileira two commercial cultivars showed effects both for parents GCA and SCA of 34: 537-546. significant differences among each hybrid combinations. The combination other for productivity and main stem BGH-4360 x Piramoita was promising GLALA,AA;ABD-ALLA,AM; EL-DESSOUKY, size at 50 days. The authors verified among the evaluated combinations, AM; OBIADALLA-ALI, HA. 2011. Heterosis that the crossings with accession BGH- presenting positive estimates of SCA for and combining ability for earliness, yield, 4360 showed higher productivities, productivity, as well as averages higher and fruit quality of some Egyptian melon overcoming the productivity of than the ones of the two controls. Thus, inbred lines via line × tester analysis. Acta commercial cultivars Sandy and Dayane. this combination is the most indicated Horticulturae 918: 491-500. This indicates a great productive to form a basic population for squash potential of this accession, confirmed breeding program. The accessions GRIFFING, B. 1956. Concept of general and by the positive values of GCA. BGH-4360 and BGH-5253 showed specific combining ability in relation to positive values of GCA for fruit shape diallell crossing systems. Australian Journal Hybrids from crossings BGH-5253 and productivity being recommended of Biology Sciences 9: 463-493. x Piramoita, BGH-7663 x Piramoita, to continue being parents in a breeding BGH-1956 x Piramoita and BGH- program. LALLA, JG; LAURA, VA; SEABRA JÚNIOR, 5253 x Zapallo Tronco also showed S; CARDOSO, AII. 2010. Capacidade significant values for productivity, ACKNOWLEDGEMENTS combinatória e heterose de linhagens de pepino overcoming two controls. In general, do grupo japonês para caracteres de produção. the crossings with cultivar Piramoita To CNPq, FAPEMIG and CAPES Horticultura Brasileira 28: 337-343. showed higher productivity average for scholarship granted and financial in relation to crossings with Zapallo LOPEZ-JUEZ, E; KOBAYASHI, M; SAKURAI, Tronco, when compared with the same A; KAMIYA, Y; KENDRICK, RE. 1995. Phytochrome, gibberellins, and hypocotyl growth: A study using the cucumber (Cucumis sativus 1) long hypocotyl mutant. Plant Physiology 107: 131-140. MACHADO, R; MIRANDA, JB. 2003. Heterosis expression in crosses between maize populations. year yield. Scientia Agricola 60: 519-524. MAPA. 2004. Instrução para execução dos ensaios de distinguibilidade, homogeneidade e estabilidade de cultivares de abóbora (Cucurbita spp.). Available at www. agricultura.gov.br/...cultivar/.../ab-d3bora- formul-c1rio-28abr2004-49282.doc. Accessed 10/03/2016. MAYNARD, DN; ELMSTROM, GW; 38 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Selection of squash “Menina Brasileira” carrying the allele “Bush” with high yield potential CARLE, RB. 2002. ‘EI Dorado’ and ‘La RESENDE, GM; BORGES, RME; GONÇALVES, Horticultura Brasileira. 31: 595-601. Estrella’:compact plant tropical pumpkin NPS. 2013. Produtividade da cultura da VALLEJO, FA; MOSQUERA, SE. 1998. hybrids. HortScience 37: 831-833. abóbora em diferentes densidades de plantio no Vale do São Francisco. Horticultura Brasileira Transferencia del gen bu a poblaciones PANDEY, S; JHAA; KUMAR, S; RAI, M. 2010. 31: 504-508. de zapallo, Cucurbita sp. con crecimiento Genetics and heterosis of quality and yield postrado. Acta Agronómica 48: 3-4. of pumpkin. Indian Journal of Horticulture RIBEIRO, AC, GUIMARÃES, PTG; ALVAREZ, 67: 333-338. VH. 1999. Recomendações para o uso de VENCOVSKY, R; BARRIGA, P. 1992. Genética corretivos e fertilizantes em Minas Gerais, 5th biométrica no fitomelhoramento. Ribeirão PUIATTI, M; SILVA, DJH. 2005. Abóboras ed. Viçosa: Sociedade Brasileira de Ciência do Preto: Sociedade Brasileira de Genética. 496p. e morangas. In: FONTES, PCR (eds). Solo (SBCS). 322p. Olericultura: teoria e prática. Viçosa: UFV. WU, T; ZHOU, J; ZHANG, Y; CAO, J. 2007. p.279-297. ROBINSON, RW; MUNGER, HM; WHITAKER, Characterization and inheritance of a bush- TW; BOHN, GW. 1976. Genes of the type in tropical pumpkin (Cucurbita moschata RAMALHO, MAP; ABREU, AFB; SANTOS, JB; Cucurbitaceae. HortScience 11: 554-568. Duchesne). Scientia Horticulturae 114: 1-4. NUNES, JAR. 2012. Aplicações da genética quantitativa no melhoramento de plantas SOUZA, FF; DIAS, RCS; QUEIRÓZ, MA. 2013. ZHANG, QI; YU, E; MEDINA, A. 2012. autógamas. Lavras: UFLA. 522p. Capacidade de combinação de linhagens Development of advanced interspecific-bridge avançadas e cultivares comerciais de melancia. lines among Cucurbita pepo, C. maxima, and C. moschata. Hortscience 47: 452-458. Hortic. bras., Brasília, v.37, n.1, January-March 2019 39

Research DIAS, DM; RESENDE, JTV; ZEIST, AR; GABRIEL, A; SANTOS, MH; VILELA, NC. 2019. Resistance of processing tomato genotypes to leafminer (Tuta absoluta). Horticultura Brasileira 37: 040-046. DOI - http://dx.doi.org/10.1590/S0102-053620190106 Resistance of processing tomato genotypes to leafminer (Tuta absoluta) Diego M Dias 1ID; Juliano TV de Resende ;1,4ID André R Zeist 2ID; André Gabriel 1ID; Matheus H Santos 1ID; Nathalia C Vilela 3ID 1Universidade Estadual do Centro-Oeste (UNICENTRO), Guapuava-PR, Brazil; [email protected]; [email protected]; [email protected]; [email protected]; 2Universidade do Oeste Paulista (UNOESTE), Presidente Prudente-SP, Brazil; [email protected]; 3Universidade Federal de Lavras (UFLA), Lavras-MG, Brazil; [email protected]; 4Universidade Estadual de Londrina (UEL), Londrina-PR, Brazil; [email protected] ABSTRACT RESUMO Tomato crop presents several obstacles that hinder its cultivation, Resistência de genótipos de tomateiro para processamento à especially the tomato leafminer Tuta absoluta (Lepidoptera: traça (Tuta absoluta) Gelechiidae). To reduce damages caused by this pest, the development of resistant cultivars is one of the main alternatives. In this study we A cultura do tomateiro apresenta vários entraves que dificultam aimed to select tomato genotypes with high acylsugar contents and o seu cultivo, com destaque para a traça-do-tomateiro, Tuta absoluta resistant to tomato leafminer. For this, contrasting F2RC1 genotypes (Lep.: Gelechiidae). Para reduzir os danos causados por essa praga, for allelochemical contents, resulting from the interspecific cross o desenvolvimento de cultivares resistentes é uma das principais between cultivar Redenção with processing characteristics, and alternativas. Objetivou-se com este trabalho selecionar genótipos de the wild species Solanum pennellii accession ‘LA-716’, with high tomateiro com elevados teores de acil-açúcar e resistentes à traça- acylsugar contents, were submitted to a test of resistance to tomato do-tomateiro. Para isso, genótipos F2RC1, contrastantes para teores leafminer with 14 treatments, being eight genotypes with high de aleloquímicos, resultantes do cruzamento interespecífico entre acylsugar content and four with low acylsugar content, in addition a cultivar Redenção, com características para processamento, e a to the parental. Significant correlations and contrasts were observed espécie silvestre Solanum pennellii, acesso ‘LA-716’ de altos teores between acylsugar contents and traits related to the resistance to de acil-açúcares, foram submetidos a um ensaio de resistência à traça- tomato leafminer. The genotype RVTA-2010-31-pl#177 presented do-tomateiro, contendo 14 tratamentos, sendo oito genótipos com alto similar behavior to the wild parental, demonstrating potential to teor de acil-açúcar, quatro com baixo teor, além dos parentais. Houve advance in the tomato breeding program for industrial processing correlações e contrastes significativos entre os teores de acil-açúcar with resistance to tomato leafminer. e características relacionadas à resistência à traça-do-tomateiro. O genótipo RVTA-2010-31-pl#177 comportou-se de maneira semelhante ao parental silvestre, demonstrando potencial para avançar no programa de melhoramento do tomateiro para processamento industrial com resistência à traça-do-tomateiro. Keywords: Solanum lycopersicum, Solanum pennellii, allelochemical, Palavras-chave: Solanum lycopersicum, Solanum pennellii, resistance to insects, acylsugars. aleloquímico, resistência a insetos, acil-açúcares. Received on November 6, 2017; accepted on August 16, 2018 Tomato (Solanum lycopersicum) is control increases production costs due Wild species of tomato are frequently the most important fruit vegetable to the great use of pesticides, causing adopted as a source of resistance to pests in world agriculture (El Balla et al., ecological imbalance and adverse effects and diseases in the improvement of 2013). In Brazil, tomato cultivation for on the health of the rural worker and commercial cultivars of tomato (Lima in natura consumption is carried out consumer (Silva et al., 2009; Mamta et et al., 2016; Lucini et al., 2015; Dias et especially in small and medium-sized al., 2016). al., 2016), such as the species Solanum properties, while processing tomato is pennellii, accession ‘LA-716’, which cultivated in large areas (Gameiro et One of the most relevant pests shows resistance to pests (Moreira al., 2007) with business characteristics, of tomato cultivated in Brazil is the et al., 2013; Dias et al., 2016). The occupying, in the world, the position of leafminer Tuta absoluta (Lepidoptera: resistance obtained from this accession main industrialized vegetable. Gelechiidae). In order to reduce the has been associated with the presence of use of pesticides for its management, allelochemicals, acting on mechanisms of Processing tomato presents obstacles farmers should use alternative methods, antibiosis and antixenosis (Maluf et al., that hinder its cultivation, especially the such as planting pest-resistant genotypes 2010; Tian et al., 2012; Dias et al., 2016). susceptibility to different pests. Pest (Silva et al., 2013). 40 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Resistance of processing tomato genotypes to leafminer (Tuta absoluta) The most characteristic and laboratory analyses RVTA-2010-31-pl#310, RVTA-2010- allelochemical in the accession ‘LA- 31-pl#319, RVTA-2010-83-pl#346, 716’ is the acylsugar (AS), which is To obtain F1BC1 plants, the RVTA-2010-31-pl#347, RVTA-2010- exuded by type IV glandular trichomes backcrossing of F2 genotypes developed 94-pl#378, and RVTA-2010-94-pl#381 (Andrade et al., 2017), which has a and selected by Dias et al. (2013) for a were selected for high AS content, while deleterious effect on the development of high AS content was carried out with the genotypes RVTA-2010-94-pl#50, certain phases of insects or even prevent the commercial cultivar Redenção [S. RVTA-2010-94-pl#95, RVTA-2010- their oviposition and feeding (Moreira et lycopersicum line developed by Ferraz 94-pl#258, and RVTA-2010-94-pl#272 al., 2013; Lucini et al., 2015). Resende et al. (2003) of determined growth were selected for low AS content. et al. (2002) and Gonçalves et al. habit and characteristics for industrial (2006) revealed that high AS contents processing, resistant to geminivirus Thereafter, these F2BC1 genotypes are due to the action of a larger gene, and tospovirus, and low AS contents]. were cloned using axillary sprouts in associated with others of smaller effect In turn, the F2 genotypes developed by order to increase the number of plants. with additive action. Due to the type of Dias et al. (2013) were obtained from On the same date, seeds from the parents inheritance involved, obtaining resistant interspecific cross-breeding of the ‘Redenção’ and ‘LA-716’ were sown or partially resistant hybrids will be cultivar Redenção with the wild species in 128-cell polystyrene trays. When possible by crossing and selecting lines S. pennellii accession ‘LA-716’ (pollen the clones from the F2BC1 genotypes with high contents of leaf AS. donor parent with high AS contents and for high and low AS contents had the resistant to tomato leafminer). From root system formed and the parents According to Resende et al. (2009), the self-fertilization of F1BC1 plants, had between three and five true leaves, genotypes selected for high AS contents a segregating population F2BC1 was seedlings were transplanted to pots with are promising in breeding programs obtained. a capacity of 8 dm3, containing sieved aimed at pest resistance. According to soil and fertilizer as recommended for these authors, by means of backcrossing, For quantifying AS content and the crop. resistant lines with favorable commercial selecting F2BC1 tomato genotypes, characteristics can be obtained and used 40 plants of ‘Redenção’, 40 plants of Bioassay with tomato leafminer for the development of tomato hybrids. ‘LA-716’, and 420 plants of F2BC1 generation genotypes were cultivated The experimental design was a Several studies have been in a greenhouse, being randomly randomized block design with four carried out aiming at obtaining lines distributed and duly identified. The replications. Treatments consisted of the with characteristics for in natura parents ‘Redenção’ and ‘LA-716’ were selected genotypes for the contrasting consumption, with high allelochemical used as a standard for quantifying AS AS contents, eight with high contents contents in the leaflets and resistant to contents, such as low and high AS and four with low contents, as previously pests (Silva et al., 2009; Gonçalves contents, respectively. described. Cultivar Redenção and ‘LA- Neto et al., 2010; Maluf et al., 2010). 716’, parents of first generation of Studies on pest resistance in tomatoes At 35 days after transplanting, crossings, were also used as standard. for industrial processing are practically samples of young and expanded leaflets Each sample unit corresponded to nonexistent. Thus, there is a need to from the upper third of plants were one pot containing one plant of each explore the interspecific variability collected to determine AS content genotype. to obtain genotypes with an aptitude following the methodology proposed for industry and high AS contents. In by Resende et al. (2002). For this At 45 days after transplanting, this sense, the aim of this study is to purpose, six leaf discs were collected plants that were in early flowering select second-generation genotypes of in triplicate from each sample and were infested with two-day old adults first backcrossing (F2BC1) with high conditioned in test tubes, totaling 6 of tomato leafminer. Three females AS contents and resistant to tomato cm2 of leaf area. Subsequently, AS was were released for each male per plant leafminer. extracted by adding dichloromethane in the greenhouse. The insects came and a colorimetric reaction by the from Laboratory of Entomology of the MATERIAL AND METHODS Sommogy-Nelson test. Then, samples Department of Agronomy of Unicentro, were submitted to absorbance reading from a programmed rearing, i.e. with The experiments were conducted in at a wavelength of 540 nm in a Cary 60 individuals of the same age. a greenhouse of the Center for Research spectrophotometer (Nelson, 1944). AS in Vegetables of the Department of concentrations in leaflets are directly Severity of damages caused by the Agronomy of the Midwestern proportional to absorbance values, i.e. tomato leafminer was assessed by means State University, Cedeteg campus, higher absorbance values lead to higher of a grading scale (Labory et al., 1999), Guarapuava-PR, Brazil (25°23′00″S, allelochemical contents. as follows: a) Plant damage intensity 51°29′38.50″W, altitude 1100 m). (PDI) [0= no damage; 1= small lesions Through the average absorbance (0.1 to 5% damage); 2= small and non- Obtaining segregating generations values, contrasting plants from F2BC1 coalescing lesions (5.1 to 20% damage); population were selected for AS 3= medium to large lesions (20.1 to contents. The genotypes RVTA-2010- 50% damage); 4= large and coalescing 31-pl#177, RVTA-2010-83-pl#357, lesions (50.1 to 80% damage); and 5= Hortic. bras., Brasília, v.37, n.1, January-March 2019 41

DM Dias et al. completely destroyed plants (above 80% RESULTS AND DISCUSSION acylsugar contents and ‘LA 716’showed damage)]. b) Types of leaflet lesions a lower number of caterpillars in the (TLL) (0= without lesions; 1= few and For the results related to the severity leaflets at 7 DAI, not differing from small lesions; 2= small and medium of damages caused by the tomato each other. However, the low-content lesions; 3= medium-sized lesions, leafminer (Table 1), the genotype genotypes and cultivar Redenção without coalescence; 4= large and RVTA-2010-31-pl#177 (high AS presented the highest number of coalescing lesions, deformed leaflets; content) stood out with the lowest caterpillars attacking leaflets, thus and 5= completely destroyed leaflet). c) plant damage intensity (PDI) at 14 evidencing the pest preference for these Attacked leaflets (%) (PAL) (0= without DAI, type of leaflet lesions (TLL) at 21 genotypes. attacked leaflets; 1= 0.1 to 5% attacked DAI, and percentage of attacked leaflets leaflets; 2= 5.1 to 20% attacked leaflets; (PAL) at 14 and 21 DAI. Only the wild At 14 DAI, the lowest number 3= 20.1 to 50% attacked leaflets; 4= 50.1 parent ‘LA-716’ presented inferior of caterpillars was observed in the to 80% attacked leaflets; and 5= more results. This evidences the potential of genotypes S. pennellii ‘LA-716’, RVTA- than 80% attacked leaflets). this genotype for the improvement of 2010-31-pl#177 (high), RVTA-2010- tomato with characteristics for industrial 83-pl#357 (high), RVTA-2010-31- Assessments were carried out by five processing aiming at obtaining plants pl#310 (high), and RVTA-2010-31- previously trained evaluators, 14 and 21 with resistance to tomato leafminer. pl#347 (high). However, the genotypes days after infestation. Population growth Another F2BC1 genotype that presented RVTA-2010-31-pl#319 (high), RVTA- of tomato leafminer was assessed 7, a low damage severity was RVTA-2010- 2010-83-pl#346 (high), RVTA-2010- 14, and 21 days after infestation by 94-pl#381, with values of PDI and TLL 94-pl#378 (high), and RVTA-2010- counting the number of eggs on the not differing from RVTA-2010-31- 94-pl#381 (high), although selected adaxial and abaxial surface and number pl#177 at 14 DAI (Table 1). for high contents of allelochemicals, of caterpillars in the leaflets. For this, showed a higher number of caterpillars three expanded leaflets were collected Regarding the oviposition of tomato in the leaflets when compared to the from the upper, middle, and lower thirds leafminer on the adaxial surface of genotypes mentioned above. However, of each plant and the number of eggs leaflets (Table 2), the assessments at 7 these genotypes were superior to and caterpillars was counted in an area and 14 DAI showed that the genotypes those selected for low contents of of 4 cm2 of each leaflet, excluding the RVTA-2010-31-pl#177, RVTA-2010- allelochemical, which had a high midrib. 83-pl#357, RVTA-2010-31-pl#310, infestation by caterpillars. RVTA-2010-31-pl#347, and RVTA- Statistical analyses 2010-94-pl#378, selected for high AS At 21 DAI, the genotypes RVTA- contents, had a low number of eggs in 2010-31-pl#177 (high), RVTA-2010- The values of grades applied to the the leaflets, not differing from the parent 83-pl#357 (high), RVTA-2010-31- damage of plants, the percentage of ‘LA-716’. pl#310 (high), RVTA-2010-31-pl#319 attacked leaflets, number of attacked (high), RVTA-2010-83-pl#346 (high), leaflets, number of eggs, and number of Generally, a lower number of and RVTA-2010-31-pl#347 (high), larvae were analyzed for the normality eggs was observed at 21 DAI for all together with ‘LA716,’ presented the of residual variances by the Shapiro- genotypes of a low AS content and lowest number of caterpillars in the Wilk test. Subsequently, an analysis of ‘Redenção’. This occurred due to the leaflets, showing a satisfactory level variance was carried out, followed by a severe damage caused by caterpillars, of resistance to this pest. The low- grouping of means by the Scott-Knott which reduced the attractiveness of acylsugar genotypes and the cultivar test at 5% probability level using the plants and the possibility of oviposition Redenção, together with the high- statistical program SISVAR (Ferreira, by tomato leafminer. content genotypes RVTA-2010-94- 2008). pl#378 and RVTA-2010-94-pl#381, Regarding the assessment of the were the most infested by caterpillars. The association of AS contents abaxial surface, the genotypes RVTA- This result is due to the high pest and genotype resistance, mediated by 2010-31-pl#177, RVTA-2010-83- suppression in the greenhouse, which damages in plants and number of eggs pl#357, RVTA-2010-31-pl#310, and migrated to the other plants after and larvae, were estimated using the RVTA-2010-31-pl#319, along with destroying those susceptible. Pearson correlation and the significance ‘LA-716’, presented lower number of of correlations by means of the t-test eggs deposited on leaflets at 7 and 14 In general, for the number of using the program Assistat 7.7 Beta DAI. The genotype RVTA-2010-31- caterpillars (NC) and eggs of the adaxial (Silva & Azevedo, 2016). Orthogonal pl#347 differed only at 14 DAI for the and abaxial surfaces, the genotypes contrasts between parents (‘Redenção’ characteristic under analysis. However, selected for high AS contents presented and ‘LA-716’) and genotype groups no difference was observed between the the lowest incidence of caterpillars with contrasting AS contents were assessed genotypes for the number of (Table 2). estimated in the bioassay using the eggs of the abaxial surface at 21 DAI statistical program SISVAR (Ferreira, due to the destruction of low-content As observed for the number of eggs, 2008). genotypes by caterpillars. the genotype RVTA-2010-94-pl#272 (low AS content) was completely 42 The genotypes selected for high damaged by the attack of tomato Hortic. bras., Brasília, v.37, n.1, January-March 2019

Resistance of processing tomato genotypes to leafminer (Tuta absoluta) Table 1. Plant damage intensity (PDI), type of leaflet lesions (TLL), and percentage of leafminer at 21 DAI, which resulted in a attacked leaflets (PAL) assessed at 14 and 21 days after infestation (DAI) with tomato low number of caterpillars in the leaflets. llyecaofmpeinrseirc(uTmutcaualbtisvoalruRtae)diennFç2ãBoCa1ngdenSootlyapneusmwpitehncnoenlltiriaascticnegssaicoynls‘uLgAar-7c1o6n’t.enGtus,aSraoplaunauvma, UNICENTRO, 2015/2016. Oviposition and number of caterpillars in the leaflets were lower Genotype  Acylsugar1 14 DAI PDI in several F2BC1 genotypes selected 21 DAI for high AS contents. However, some high-content genotypes did not differ S. pennellii ‘LA-716’ 0.620 1.30 a 1.40 a from those selected for low contents, presenting a higher number of eggs RVTA-2010-31-pl#177 (high) 0.434 2.25 b 3.25 b and caterpillars. Dias et al. (2013) obtained similar results, in which some RVTA-2010-83-pl#357 (high) 0.482 3.75 c 4.80 c genotypes with high AS content showed oviposition and number of caterpillars RVTA-2010-31-pl#310 (high) 0.416 3.40 c 4.80 c without differing from the genotypes selected for low allelochemical content. RVTA-2010-31-pl#319 (high) 0.654 3.65 c 4.80 c In addition, Gonçalves Neto et al. (2010) verified high oviposition by tomato RVTA-2010-83-pl#346 (high) 0.484 4.00 d 4.80 c leafminer in clones with high contents of this allelochemical, with no difference RVTA-2010-31-pl#347 (high) 0.463 4.10 d 4.80 c for low-content controls. These results may be due to the presence of other RVTA-2010-94-pl#378 (high) 0.444 4.14 d 4.75 c allelochemicals with an antagonistic effect to resistance coming from RVTA-2010-94-pl#381 (high) 0.489 3.15 b 4.75 c high acylsugar contents. Maluf et al. (2010) reported that the divergence RVTA-2010-94-pl#50 (low) 0.120 4.02 d 4.90 c of results is commonly observed in breeding programs aiming at pest RVTA-2010-83-pl#95 (low) 0.145 4.00 d 4.55 c resistance in genotypes obtained from interspecific crossings between a line RVTA-2010-94-pl#258 (low) 0.160 4.10 d 4.75 c of S. lycopersicum and a wild parent with subsequent backcrossing with S. RVTA-2010-94-pl#272 (low) 0.155 4.80 d 4.80 c lycopersicum. ‘Redenção’ 0.143 4.75 d 5.00 c The linear correlations were negative and significant at 7 and 14 DAI between CV (%) 12.06 4.88 AS contents of the assessed genotypes and values for the number of eggs Correlation -0.61** 0.40 of the adaxial and abaxial surfaces and NC, with values of −0.56 and Acylsugar1 14 DAI TLL −0.76, −0.74 and −0.81, and −0.86 21 DAI and −0.83, respectively (Table 2). These correlations indicate a direct S. pennellii ‘LA-716’ 0.620 1.25 a 1.20 a association between the non-preference for oviposition of tomato leafminer and RVTA-2010-31-pl#177 (high) 0.434 2.00 a 3.30 b high AS contents in the leaflets of the genotypes, thus demonstrating the action RVTA-2010-83-pl#357 (high) 0.482 3.80 b 4.80 c of this allelochemical on resistance mechanisms known as antixenosis. RVTA-2010-31-pl#310 (high) 0.416 3.35 b 4.90 c Lucini et al. (2015) studied the RVTA-2010-31-pl#319 (high) 0.654 3.60 b 4.80 c resistance mechanisms presented by F2 genotypes with contrasting AS contents RVTA-2010-83-pl#346 (high) 0.484 4.05 c 4.85 c from a crossing between S. lycopersicum and S. pennellii accession ‘LA-716’. By RVTA-2010-31-pl#347 (high) 0.463 4.02 c 4.90 c means of choice and no-choice tests, the presence of resistance mechanisms RVTA-2010-94-pl#378 (high) 0.444 4.05 c 4.80 c by antixenosis and antibiosis in F2 genotypes selected for high AS contents RVTA-2010-94-pl#381 (high) 0.489 3.10 b 4.90 c was identified when submitted to the RVTA-2010-94-pl#50 (low) 0.120 4.18 c 4.90 c 43 RVTA-2010-83-pl#95 (low) 0.145 4.15 c 4.90 c RVTA-2010-94-pl#258 (low) 0.160 4.10 c 4.95 c RVTA-2010-94-pl#272 (low) 0.155 4.80 c 5.00 c ‘Redenção’ 0.143 4.7 c 5.00 c CV (%) 14.36 4.08 Correlation -0.63** -0.44 Acylsugar1 14 DAI PAL 21 DAI S. pennellii ‘LA-716’ 0.620 1.00 a 1.05 a RVTA-2010-31-pl#177 (high) 0.434 3.20 b 3.35 b RVTA-2010-83-pl#357 (high) 0.482 4.50 c 5.00 c RVTA-2010-31-pl#310 (high) 0.416 4.30 c 5.00 c RVTA-2010-31-pl#319 (high) 0.654 4.40 c 5.00 c RVTA-2010-83-pl#346 (high) 0.484 4.35 c 5.00 c RVTA-2010-31-pl#347 (high) 0.463 4.35 c 5.00 c RVTA-2010-94-pl#378 (high) 0.444 4.50 c 5.00 c RVTA-2010-94-pl#381 (high) 0.489 4.00 c 5.00 c RVTA-2010-94-pl#50 (low) 0.120 4.60 c 5.00 c RVTA-2010-83-pl#95 (low) 0.145 4.55 c 5.00 c RVTA-2010-94-pl#258 (low) 0.160 4.73 c 5.00 c RVTA-2010-94-pl#272 (low) 0.155 4.90 c 5.00 c ‘Redenção’ 0.143 4.75 c 5.00 c CV (%) 8.68 4.88 Correlation -0.54** -0.40 *Means followed by same letters in the column belong to the same group by the Scott-Knott test, 5% probability; **Significant by Student test, 5% probability; 1Acylsugar contents at 540 nm. PDI= notes from 0 (no damage) to 5 (completely destroyed plants). TLL= notes from 0 (without lesions) to 5 (completely destroyed leaflet). PAL= notes from 0 (without attacked leaflets, 0%) to 5 (more than 80% attacked leaflets). Hortic. bras., Brasília, v.37, n.1, January-March 2019

DM Dias et al. Table 2. Number of eggs and caterpillars of tomato leafminer (Tuta absoluta) in leaflets presence of the tomato leafminer. of F2BC1 genotypes with contrasting acylsugar contents, Solanum lycopersicum cultivar Redenção and Solanum pennellii accession ‘LA-716’ at 7, 14, and 21 days after infestation At 21 DAI, no significant correlations (DAI). Guarapuava, UNICENTRO, 2015/2016. were observed between AS contents in the genotypes and the assessed Genotype Acylsugar1 Number of eggs of the adaxial surface  variables, given the destruction of low- content plants (Tables 1 and 2). S. pennellii ‘LA-716’ 0.620 7 DAI 14 DAI 21 DAI RVTA-2010-31-pl#177 (high) 0.434 At 21 DAI, the difference of RVTA-2010-83-pl#357 (high) 0.482 0.16 a 0.50 a 0.33 a resistance of F2BC1 genotypes selected RVTA-2010-31-pl#310 (high) 0.416 for high AS contents was not more RVTA-2010-31-pl#319 (high) 0.654 3.75 a 2.16 a 1.25 b evident due to the joint action of RVTA-2010-83-pl#346 (high) 0.484 two ecological conditions imposed RVTA-2010-31-pl#347 (high) 0.463 1.83 a 1.00 a 0.08 a by the restricted environment of the RVTA-2010-94-pl#378 (high) 0.444 greenhouse: population and hosts. Thus, RVTA-2010-94-pl#381 (high) 0.489 2.33 a 1.50 a 0.33 a the most susceptible genotypes (low AS RVTA-2010-94-pl#50 (low) 0.120 content) allowed the population growth RVTA-2010-83-pl#95 (low) 0.145 6.58 b 3.09 a 0.92 b of tomato leafminer in a number higher RVTA-2010-94-pl#258 (low) 0.160 than that the environment supported, RVTA-2010-94-pl#272 (low) 0.155 6.00 b 5.08 b 1.42 b which led to the destruction of these ‘Redenção’ 0.143 hosts and migration of the pest to CV (%) 3.58 a 2.17 a 0.58 a lower susceptible genotypes (high AS Correlation   content). However, the tendency is that   3.99 a 3.08 a 0.25 a plants selected for high AS content and S. pennellii ‘LA-716’ exposed to natural infestation conditions RVTA-2010-31-pl#177 (high) Acylsugar1 5.33 b 3.25 a 0.58 a have superior resistance to leafminer RVTA-2010-83-pl#357 (high) over the tomato growing cycle. A RVTA-2010-31-pl#310 (high) 0.620 5.67 b 6.25 b 1.25 b complementary study conducted with RVTA-2010-31-pl#319 (high) 0.434 no chance to choosing by the host could RVTA-2010-83-pl#346 (high) 0.482 5.80 b 5.50 b 1.25 b better evidence this issue. RVTA-2010-31-pl#347 (high) 0.416 RVTA-2010-94-pl#378 (high) 0.654 5.50 b 4.42 b 1.33 b By means of the estimate of contrasts RVTA-2010-94-pl#381 (high) 0.484 of interest for the characteristics RVTA-2010-94-pl#50 (low) 0.463 9.42 b 4.58 b 0.00 a related to population growth of tomato RVTA-2010-83-pl#95 (low) 0.444 leafminer, a difference was observed RVTA-2010-94-pl#258 (low) 0.489 6.92 b 6.42 b 0.83 b between both groups of F2BC1 genotypes RVTA-2010-94-pl#272 (low) 0.120 with contrasting AS contents at 14 DAI ‘Redenção’ 0.145 52.13  43.61  103.61 (−2.52, −4.44, and −13.05 for the CV (%) 0.160 number of eggs of adaxial and abaxial Correlation 0.155 -0.56**  -0.76**  -0.27 surface and NC, respectively) (Table 0.143 3). In addition, no difference was S. pennellii ‘LA-716’ Number of eggs of the abaxial surface  observed between the parent ‘LA-716’ RVTA-2010-31-pl#177 (high)   vs. F2BC1 genotypes with high AS RVTA-2010-83-pl#357 (high)   7 DAI 14 DAI 21 DAI contents, F2BC1 genotypes with low RVTA-2010-31-pl#310 (high) AS contents differed from ‘LA-716’ RVTA-2010-31-pl#319 (high) Acylsugar1 1.08 a 0.75 a 0.17 a for these same characteristics, those of RVTA-2010-83-pl#346 (high) high content differed from ‘Redenção’ RVTA-2010-31-pl#347 (high) 0.620 3.50 a 2.08 a 0.92 a for NC, and no difference was observed RVTA-2010-94-pl#378 (high) 0.434 for genotypes with a low AS content RVTA-2010-94-pl#381 (high) 0.482 3.99 a 3.33 a 0.42 a with ‘Redenção’. Thus, the promotion RVTA-2010-94-pl#50 (low) 0.416 of resistance to tomato leafminer attack RVTA-2010-83-pl#95 (low) 0.654 3.42 a 3.17 a 0.42 a was related to the presence of the AS RVTA-2010-94-pl#258 (low) 0.484 allelochemical at high concentrations RVTA-2010-94-pl#272 (low) 0.463 5.42 a 4.58 a 0.67 a in the leaf epidermis. ‘Redenção’ 0.444 CV (%) 0.489 5.25 a 6.84 b 0.83 a Maluf et al. (2010), Maciel et al. Correlation 0.120 (2011), Dias et al. (2013), and Baier et 0.145 4.67 a 3.08 a 0.50 a al. (2005) reported that high AS contents 0.160 in leaflets of genotypes obtained 0.155 7.09 b 4.33 a 1.42 a from the interspecific crossing of S. 0.143 6.42 b 4.58 a 0.75 a 7.92 b 10.83 b 1.83 a 6.75 b 7.92 b 1.08 a 6.75 b 8.67 b 1.83 a 10.50 b 6.33 b 0.00 a 9.89 b 8.5 b 1.08 a 55.08 48.11 103.43 -0.74** -0.81** -0.48 Number of caterpillars 7 DAI 14 DAI 21 DAI 0.00 a 0.00 a 0.08 a 0.92 a 4.58 a 10.67 a 1.25 a 5.50 a 5.83 a 0.58 a 1.58 a 4.33 a 0.83 a 9.33 b 7.58 a 1.08 a 8.84 b 9.42 a 1.50 a 4.59 a 8.08 a 0.83 a 8.08 b 12.92 b 1.17 a 7.92 b 17.33 b 2.83 b 23.42 c 16.92 b 3.34 b 17.80 c 15.67 b 2.33 b 12.34 b 21.25 b 3.83 b 24.58 c 0.33 a 5.25 b 21.14 c 18.33 b 93.22 36.79 89.44 -0.86** -0.83** -0.50 *Means followed by same letters in the column belong to the same group by Scott-Knott test, 5% probability; **Significant by Student test, 5% probability; 1Acylsugar contents at 540 nm. 44 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Resistance of processing tomato genotypes to leafminer (Tuta absoluta) Table 3. Estimates of the means of contrasts of interest used for comparisons of resistance SILVA, MCL; FRANÇA, JGE; SILVA, DJ. to tomato leafminer (Tuta absoluta) in plants of F2BC1 genotypes with contrasting acylsugar 2003. Redenção: nova cultivar de tomate para a contents, Solanum lycopersicum cultivar Redenção and Solanum pennellii accession ‘LA- indústria resistente a geminivírus e tospovírus. 716’ at 7, 14, and 21 days after infestation (DAI). Guarapuava, UNICENTRO, 2015/2016. Horticultura Brasileira 21: 578-580. Contrasts of interest Number of eggs of the adaxial surface  FERREIRA, D. 2008. SISVAR: um programa para análises e ensino de estatística. Revista Genotypes (high) vs. Genotypes (low) 7 DAI   14 DAI   21 DAI Symposium 6: 36-41. ‘LA-716’ vs. Genotypes (high) ‘LA-716’ vs. Genotypes (low) -2.42   -2.52*   -0.28 GAMEIRO, AH; CAIXETAFILHO, JV; ROCCO, ‘Redenção’ vs. Genotypes (high) CD; RANGEL, R. 2007. Estimativas de perdas ‘Redenção’ vs. Genotypes (low) -4.01   -2.17   -0.34 no suprimento de tomates para processamento industrial no estado de Goiás. Informações Genotypes (high) vs. Genotypes (low) -6.43   -4.69*   -0.62 Econômicas 37: 7-16. ‘LA-716’ vs. Genotypes (high) ‘LA-716’ vs. Genotypes (low) 2.74   3.75   0.16 GONÇALVES, LD; MALUF, WR; CARDOSO, ‘Redenção’ vs. Genotypes (high) MG; RESENDE, JTV; CASTRO, EM; ‘Redenção’ vs. Genotypes (low) 0.32   1.23   -0.12 SANTOS, NM; NASCIMENTO, IR; FARIA, MV. 2006. Relação entre zingibereno, Genotypes (high) vs. Genotypes (low) Number of eggs of the abaxial surface  tricomas foliares e repelência de tomateiros ‘LA-716’ vs. Genotypes (high) a Tetranychus evansi. Pesquisa Agropecuária ‘LA-716’ vs. Genotypes (low) 7 DAI   14 DAI   21 DAI Brasileira 41: 267-273. ‘Redenção’ vs. Genotypes (high) ‘Redenção’ vs. Genotypes (low) -3.01   -4.44*   -0.45 GONÇALVES NETO, AC; SILVA, VF; MALUF, WR; MACIEL, GM; NÍZIO, DAC; GOMES, -3.88   -3.25   -0.57 LAA; AZEVEDO SM de. 2010. Resistência à traça-do-tomateiro em plantas com altos -6.89   -7.69*   -1.02 teores de acil-açúcares nas folhas. Horticultura Brasileira 28: 203-208. 4.29   4.50   0.34 LABORY, CRG; SANTA-CECÍLIA LVC; 1.91   0.06   -0.10 MALUF, WR; CARDOSO, CG; BEARZOTTI, E; SOUZA, JC. 1999. Seleção indireta Number of caterpillars para teor de 2-tridecanona em tomateiros segregantes e sua relação com a resistência 7 DAI   14 DAI   21 DAI à traça-do-tomateiro. Pesquisa Agropecuária Brasileira 34: 733-740. -2.06   -13.05*   -4.02 LIMA, IP; RESENDE, JTV; OLIVEIRA, JRF; -1.02   -6.30   -9.44 FARIA, MV; DIAS, DM; RESENDE, NCV. 2016. Selection of tomato genotypes for -3.08   -19.35*   -13.46 processing with high zingiberene content, resistant to pests. Horticultura Brasileira 34: 4.22   14.84*   8.81 387-391. 2.17   1.78   4.79 LUCINI, T; FARIA, MV; ROHDE, C; RESENDE, JTV; OLIVEIRA, JRF. 2015. Acylsugar and *Significant by Student test at 5% probability. the role of tricomes in tomato genotypes resistence to Tetranychus urticae. Arthropod- lycopersicum with the wild accession DM; MALUF, WR. 2017. Inheritance of Plant Interactions 9: 45-53. ‘LA-716’ and subsequent backcrossing type IV glandular trichome density and its with S. lycopersicum act as an important association with whitefly resistance from MACIEL, GM; MALUF, WR; SILVA, VF; provider of pest resistance. Among the Solanum galapagense accession LA140. GONÇALVES NETO, AC; GOMES, LAA. tested segregating F2BC1 genotypes, Euphytica 213: 52- 64. 2011. Híbridos pré-comerciais resistentes RVTA-2010-31-pl#177 stood out a Tuta absoluta obtidos de linhagem de with high AS contents, proving to be BAIER, JE; RESENDE, JTV; FARIA, MV; tomateiro rica em acil-açúcares. Horticultura resistant to tomato leafminer since the SCHWARZ, K.; MEERT, L. 2015. Indirect Brasileira 29: 151-156. oviposition, the number of caterpillars, selection of industrial tomato genotypes and the severity of damage to plants resistant to spider mite Tetranychus urticae. MALUF, WR; MACIEL, GM; GOMES, LAA; decreased. Genetics and Molecular Research 14: 244- CARDOSO, MG; GONÇALVES, LD; SILVA, 252. EC; KNAPP, M. 2010. Broad-spectrum Selection of genotypes with high arthropod resistance in hybrids between high- acylsugar contents, resistant to tomato DIAS, DM; RESENDE, JTV; FARIA, MV; and low-acylsugar tomato lines. Crop Science leafminer, is of great relevance in CAMARGO, LKP; LIMA, IP. 2013. Selection 50: 439-450. a genetic breeding program since it of processing tomato genotypes with high acyl allows prospecting generations to sugar content that are resistant to the tomato MAMTA, K; REDDY, RK; RAJAM, MV. 2016. obtain isogenic lines with backgrounds pinworm. Genetics and Molecular Research Targeting chitinase gene of Helicoverpa more compatible with established 12: 381-389. armigera by host-induced RNA interference requirements within the productive confers insect resistance in tobacco and chain of processing tomato. DIAS, DM; RESENDE, JTV; MARODIN, JC; tomato. Plant Molecular Biology 90: 281-292. MATOS, R; LUSTOSA, IF; RESENDE, REFERENCES NCV. 2016. Acyl sugars and whitefly (Bemisia MOREIRA, GR; SILVA, DJH; CARNEIRO, tabaci) resistance in segregating populations PCS; PICANÇO, MC; VASCONCELOS, AA; ANDRADE, MC; SILVA, AA; NEIVA, IP; of tomato genotypes. Genetics and Molecular PINTO, CMF. 2013. Herança de caracteres OLIVEIRA, IR; CASTRO, EM; FRANCIS, Research 15: 1-11. de resistência por antixenose de Solanum pennellii à traça-do-tomateiro em cruzamento EL BALLA, MMA; HAMID, AA; com ‘Santa Clara’. Horticultura Brasileira ABDELMAGEED, AHA. 2013. Effects of 31: 574-581. time of water stress on flowering, seed yield and seed quality of common onion (Allium NELSON, N. A photometric adaptation of the cepa L.) under the arid tropical conditions Sommogy method for the determination of Sudan. Agricultural Water Management of glucose. 1944. Journal of Biological 121: 49-157. 45 FERRAZ, E; RESENDE, LV; LIMA, GSA; Hortic. bras., Brasília, v.37, n.1, January-March 2019

DM Dias et al. Chemistry 153: 375-380. 27: 345-348. SILVA, AA; ANDRADE, MC; CARVALHO, RC; RESENDE, JTV; MALUF, WR; CARDOSO, MG; SILVA, VF; MALUF, WR; CARDOSO, MG; NEIVA, IP; SANTOS, DC; MALUF, WR. 2016. Resistência à Helicoverpa armigera NELSON, DL; FARIA, MV. 2002. Inheritance GONÇALVES NETO, AC; MACIEL, GM; em genótipos de tomateiro obtidos do of acylsugar contents in tomatoes derived from NÍZIO, DAC; SILVA, VA. 2009. Resistência cruzamento de Solanum lycopersicum com an interspecific cross with the wild tomato mediada por aleloquímicos de genótipos de Solanum galapagense. Pesquisa Agropecuária Lycopersicon pennellii and their effect on tomateiro à mosca‑branca e ao ácaro‑rajado. Brasileira 51: 801-808. spider mite repellence. Genetics and Molecular Pesquisa Agropecuária Brasileira 44: 1262- Research 1: 106-116. 1269. TIAN, D; TOOKER, J; PEIFFER, M; CHUNG, RESENDE, JTV; MALUF, WR; CARDOSO, SILVA, FAZ; AZEVEDO, CAV. 2016. The SH; FELTON, GW. 2012. Role of trichomes MG; GONÇALVES, LD; FARIA, MV; Assistat Software Version 7.7 and its use in in defense against herbivores: comparison NASCIMENTO, IR. 2009. Resistance of the analysis of experimental data. African of herbivore response to woolly and hairless tomato genotypes to the silverleaf whitefly Journal of Agricultural Research 11: 3733- trichome mutants in tomato (Solanum mediated by acylsugars. Horticultura Brasileira 3740. lycopersicum). Planta 236: 1053-1066. 46 Hortic. bras., Brasília, v.37, n.1, January-March 2019

Research ALVAREZ, JM; PASIAN, C; LAL, R; LÓPEZ, R; FERNÁNDEZ, M. 2019. Vermicompost and biochar substrates can reduce nutrients leachates on containerized ornamental plant production. Horticultura Brasileira 37: 047-053. DOI - http://dx.doi.org/10.1590/S0102-053620190107 Vermicompost and biochar substrates can reduce nutrients leachates on containerized ornamental plant production José M Alvarez 1,2ID; Claudio Pasian 2ID; Rattan Lal 2ID; Rafael López 3ID; Manuel Fernández 1ID 1Escuela Técnica Superior de Ingeniería, Universidad de Huelva, Huelva, Spain; [email protected] (corresponding author); [email protected]; 2Ohio State University, Columbus OH, USA; [email protected]; [email protected]; 3Instituto de Recursos Naturales y Agrobiología de Sevilla, Consejo Superior de Investigaciones Científicas, Sevilla, Spain; [email protected] ABSTRACT RESUMO Containerized ornamental plant production is facing several Substratos de vermicomposto e biochar podem reduzir os environmental challenges. One of them is to replace the widely lixiviados de nutrientes na produção de plantas ornamentais used, but with questionable sustainability, peat based substrates em contêineres and another is to avoid water contamination by chemicals leaching from the nursery. Therefore, as have been verified that petunia and A produção de plantas ornamentais em contêineres está pelargonium plants can be produced in peat-based growing media enfrentando vários desafios ambientais. Um deles é substituir partially replaced by vermicompost (V) and biochar (B) without os substratos amplamente utilizados, mas com sustentabilidade decreasing commercial quality, this study has focused on analyzing questionável, baseados em turfa, e outro é evitar a contaminação the leachate from a standard peat-based substrate as a control, used da água por produtos químicos lixiviados do viveiro. Verificou-se for producing these two ornamental species, and those from the same que as plantas de petúnia e gerânio podem ser produzidas em meios substrate to which different proportions in volume of V (10% and de crescimento baseados em turfa parcialmente substituídos por 20%) and B (4% and 12%) have been added. The amount of nitrogen vermicomposto (V) e biochar (B) sem diminuir a sua qualidade leached from the mixed substrates was reduced compared to the comercial. Este estudo concentrou-se na análise do lixiviado de uma control one in both species (on average 37%). Nitrogen was leached turfa padrão como controle, utilizado para a produção destas duas mainly as nitrate-nitrogen (89% in Petunia and 97% in Pelargonium). espécies ornamentais, e o mesmo substrato ao qual foram adicionados In Petunia phosphorous leaching was also decreased (30%) for the diferentes proporções em volume de V (10% e 20%) e B (4% e treatment with 10% V and 4% B, while potassium leaching in substrate 12%). Verificou-se que a quantidade de nitrogenio lixiviado dos containing 20% V and 12% B increased by 100%. Our results show substratos misturados foi reduzida em comparação com a testemunha that these two organic materials tested (V and B) can help producers em ambas as espécies (em média 37%). O nitrogênio foi lixiviado to reduce the use of peat and chemical fertilizers as well as the risk principalmente como nitrato-nitrogênio (89% em Petunia e 97% of contamination by chemicals, mainly nitrate. em Pelargonium). Na Petunia a lixiviação de fósforo também foi reduzida (30%) para o tratamento com 10% de V e 4% de B, enquanto a lixiviação de potássio em substrato contendo 20% de V e 12% de B aumentou em 100%. Nossos resultados mostram que esses dois materiais orgânicos testados (V e B) podem ajudar os produtores a reduzir o uso de turfa e fertilizantes químicos, bem como diminuir o risco de contaminação por substâncias químicas, principalmente nitrato. Keywords: Petunia hybrida, Pelargonium peltatum, peat Palavras-chave: Petunia hybrida, Pelargonium peltatum, replacement, water contamination, nitrate, phosphate. substituição de turfa, contaminação da água, nitrato, fosfato. Received on March 22, 2018; accepted on November 16, 2018 Containerized ornamental plants First, the use of peat as growing materials, mainly from the recycling production has increased all over media is increasingly weighed. Around of organic wastes and by-products. the world (AIPH, 2017). Growers have 10 to 11 million kg of this material Vermicompost (V) and biochar (B) are to face several environmental challenges are used annually in the world for good candidates to substitute peat as both to compile legal requirements and horticultural production (US, 2016). growing media, since it has been proven the increasing environmental demands Since peat is considered a non-renewable that, used in the right proportions, they of their customers. We can mention three resource and its use is questioned by the do not reduce, even can improve, the obstacles on which the producer will drainage of peatlands (Keddy, 2010). In commercial quality of the produced have sooner or later to make decisions the frame of the circular economy there plants (Alvarez et al., 2017, 2018). about. is a growing demand to use renewable Vermicompost is a product derived from Hortic. bras., Brasília,v.37, n.1, January-March 2019 47

JM Alvarez et al. the accelerated biological degradation Showers. These species were also density (Db), water holding capacity of organic wastes by earthworms and chosen for their different nutrients needs (WHC), total porosity (Pt) and air space microorganisms. Biochar is a by- and rusticity as well as on their salt (As) were determined at the beginning of product of the C-negative pyrolysis tolerance, being Petunia more tolerant the experiment following the procedures technology for bio-energy production than Pelargonium (Monk & Wiebe, for determining physical properties of from organic materials. 1961; Do & Scherer, 2013), since horticultural substrates using the NCSU vermicompost (V) and biochar (B) could porometer (Fonteno & Bilderback, Second, there is increasing awareness modify mineral nutrients availability, 1993). Soluble nutrients, pH and electric of the need to mitigate the effects of electrical conductivity and pH (Alvarez conductivity (EC) were determined in climate change. The use of recycled et al., 2017). aqueous extracts (1:6 volume fraction) materials and alternative energies to taken from fresh mixtures samples in fossil fuels are often the main changes Commercial products available advance of plants cultivation: nitrate that the ornamental plant production in the market were used to make and ammonium by spectrophotometry industry introduces when it decides to up the growing media, biochar (B), in a flow autoanalyser (AA III, Bran study and maintain a strategy to track the vermicompost (V) and a peat-based + Luebbe, Norderstedt, Germany) carbon footprint of its products (Barrett substrate (S). The biochar is called (Ansorena Miner, 1994); potassium, et al., 2016). Soil Reef Pure 02 (Biochar Solutions sulfate and phosphate by ICP-OES Inc., Co, USA) and was produced (Dahlquist & Knoll, 1978); EC and pH Finally, due to the peculiarities of by high temperature pyrolysis, 600 by a pH-meter/conductimeter (Acumet® this type of containerized ornamental to 800ºC, of Pinus monticola wood. Ap85, USA) (Ansorena Miner, 1994). plants production (Ruter, 1993), The vermicompost is named Black irrigation and fertilization management Diamond Vermicompost (Black Petunia and Pelargonium seeds were should be adequate to avoid nutrients Diamond Vermicompost, Ca, USA) germinated in 100 plug trays (21.8 cm3/ leaching to public waters adjacent to and was produced by pre-composting cell) and two seeds were added per cell. the area of the production facilities and for two weeks the solid fraction of After germination, just one seedling was their eventual contamination (Cabrera, bovine manure using an aerated kept. Trays were placed in a glasshouse 1997, Majsztrik et al., 2011). Actually, composting system, then submitted to for 40 days at 24ºC and 54% average in Europe and the United States there a vermicompost process for a period temperature and relative humidity, is an increasing pressure to reduce of 70 to 80 days. These two renewable respectively under a climate control the leachates of horticultural crops organic materials (B and V) were used system in the greenhouse. Watering was for environmental reasons (Guimera to partially replace a peat-based control done with an automatic micro sprinkler et al., 1995). Nitrate, ammonium and substrate (S) called Farfard 3B mixture irrigation system between dawn and phosphates are the ions considered the (SunGro Horticulture Distribution Inc., dusk. Nozzles were irrigating at 1.8 most problematic irrigation leachates USA). This peat-based substrate is L/h during 15 seconds every 20 min, (Mueller et al., 1995) due to their effect composed by Canadian Sphagnum peat with 2 meter diameter and 1 meter in surface waters and impact in public moss, pine bark, perlite, vermiculite, overlap. After that, thirty seedlings were health (Agegnehu et al., 2017). dolomitic limestone, and a wetting agent, randomly obtained, transplanted into at 6:4:2:1 Peat:Bark:Perlite:Vermiculite 800 cm3 plastic containers and moved Our hypothesis is that the inclusion volume ratio. Farfard 3B received a slow to a glass covered greenhouse (average of these two new materials, biochar and release fertilizer (Scotts Osmocote Plus temperature 20ºC and average humidity vermicompost, in the peat based growing 15-9-12, 5-6 months release at 21ºC, 29% also under a climate control system media could reduce the leaching of at a dosage of 5.9 g L-1). An overview in the glasshouse) for 68 days until nutrients while maintaining an adequate of the main characteristics of these the market size was reached. Standard plant quality. components, and more details appear in propagation protocols for these species table 1 at Alvarez et al. (2017). were followed. The experimental design Manuscript main objective: in this was a completely randomized design study the leaching of nitrogen and Three growing media (mixes) were with two replicas. Each replica consisted other nutrients from peat based blends prepared with the following volume of 5 plants per species and treatment including biochar and vermicompost fractions (S:V:B): 100:00:00, 86:10:04 randomly distributed (5 plants x 3 was assessed in comparison with usual and 68:20:12, being, respectively, the treatments x 2 species = 30 plants per fertilized peat substrates. control treatment and two treatments replica). The two replicas were placed containing a slight and a moderate peat- on separate benches (2 replicas x 15 MATERIAL AND METHODS based substrate replacement. The last plants = 60 plants). Plants were rotated two treatments were selected based on a periodically to minimize variation in Plant material and experimental previous study when 23 different mixes microclimatic conditions. Containers design were compared with S (i.e. S = 100:00:00 were watered manually as needed treatment), and according to the good with distilled water. The water was Two ornamental species very plant growth and flowering obtained added to each pot gradually by using much worldwide used were utilized, (Alvarez et al., 2017). Then, bulk Petunia x hybrida cv. Dreams Neon and Pelargonium peltatum cv. Summer Hortic. bras., Brasília, v.37, n.1, January-March 2019 48

Vermicompost and biochar substrates can reduce nutrients leachates on containerized ornamental plant production a slight volume every time (≤10 cm3) SDW and number of flowers were (100 to 140 kg m-3), except for control. and waiting for a few minutes before recorded in Petunia and Pelargonium All the above met the recommendations adding next volume. As soon as a water plants. In Pelargonium number of open made by Bilderback et al. (2005) and droplet appeared at the bottom of the pot inflorescences and inflorescence-buds Yeager (1997). no more water was added. These few were also counted. Shoot dry weight was water droplets leached from each pot obtained after oven-drying at 55ºC for Figure 1 shows accumulated plants were taken back to the pot. Therefore, 72 h. For SDW and inflorescences, one- biomass and number of flowers per plant water was gradually added trying to way analysis of variance (SPSS Statistics for the two ornamental species grown in avoid leaching and to keep substrate to 17.0) were carried out to determine the three different treatments. Petunia’s field capacity. statistically significant differences SDW and flowering were significantly between treatments, being the treatment higher in mixture 86:10:04 compared Plant growth, leaching parameters a fixed effect. While for leachate nutrient with control. Treatment 86:10:04 and data analysis concentrations and nutrient contents growed up to 37% and produced 43% repeated measured ANOVA were carried more flowers than the standard peat The parameters evaluated were out, since nutrient concentration in the based substrate. Mix 68:20:12 produced shoot dry weight (SDW) of plants, leachate on a specific day depends on 30% more flowers than control. In the and containers leachates volume and the concentration obtained in previous case of Pelargonium, SDW was similar nutrient contents. At the end of the days. Significant differences were in all treatments, but flowering in mix growing period and before measuring established at p= 0.05. To evaluate 86:10:04 significantly and positively shoot dry weight (SDW) of plants, the among treatments comparisons, differed from the control, producing up containers leachates were collected Tukey-HSD or T3-Dunnett tests were to 108% more flowers. during five consecutive days after used in order to differentiate within receiving a daily watering of 200 cm3. homogeneous groups, according to In regard to physical and physico- In order to collect the leachate, both variance homoscedasticity. In addition, chemical characteristics of these three a plastic mesh and a plastic cuvette correlation and regression analyses substrates, only bulk density (Db) was were placed under each container. For were performed in order to establish affected by the addition of V and B, every sampling date, the substrate was the underlying relationships between being the heaviest mixture (68:20:12) moistened to field capacity, as described treatments and measured parameters. only a 10% heavier than the control before, one day before collection of one. The addition of V to peat substrates the samples. Collected volume was RESULTS AND DISCUSSION usually increase Db (Mupondi et al., measured and a sample was taken for 2014; Álvarez et al., 2017), but in subsequent nutrient analysis of nitrate- Physical characteristics of the this study, taking into account the nitrogen (N-NO3-), nitrite-nitrogen (N- substrates and plant growth proportions of V used, it does not seem NO2-), ammonium-nitrogen (N-NH4+), to have negatively affected the plant phosphate-phosphorous (P-PO4-3), total The physical properties at the growth and nursery management. In P, sulfate (SO4-2). The total nitrogen was beginning of the experiment of peat- respect of plant growth and flower calculated as the sum of nitrate-, nitrite-, based substrate (S), and the two different production, our results clearly showed and ammonium-nitrogen. The nutrient mixtures studied are shown in Table 1. that Petunia and Pelargonium growth contents (mg) collected in the leachates Pt and As in all mixtures lied within the and flowering status was enhanced were calculated by multiplying the suggested optimum ranges, 68 to 88% with the inclusion of B and V in peat concentration (mg L-1) by the collected and 6 to 13%, respectively. WHC was based substrate in slight or moderate volume (L). Nutrient analysis was always slightly above the recommended proportions. These results are aligned performed by means of standard methods range 45 to 65%, while Db was also with other species (Graber et al., 2010; using a multiparameter photometer (HI slightly above the recommended range Tian et al., 2012; Mulcahy et al., 2013). 83200, Hanna Instruments®, Italy). For instance, Graber et al. (2010) found an increase in pepper canopy dry weight At the end of the growth period and flowering by the addition of biochar to a coconut fiber:tuff mix; Tian et al. Table 1. Physical properties, mean (SE), of growth media (treatments) used in the experiment. (2012) obtained similar results growing Columbus, OSU, 2016. Calathea rotundifolia plants in 50% green waste pyrolyzed biochar added to S:V:B Db (kg dm-3) WHC (%) Pt (% v/v) As (% v/v) a peat medium, compared to 100% peat; and an improvement in tomato plant 100:00:00 0.140 (0.03) a 70.1 (0.6) a 80.1 (0.2) a 10.3 (0.9) a height in growing medium amended with wood pyrolyzed biochar (1 to 5%, 86:10:04 0.143 (0.05) a 71.5 (0.7) a 80.3 (0.6) a 8.7 (1.2) a weight fraction). 68:20:12 0.154 (0.02) b 72.2 (0.6) a 80.7 (0.8) a 8.2 (0.3) a Leachate properties On average, Pelargonium’s leachate p 0.02 0.12 0.87 0.30 volume per pot and date (50.6 cm3) was Db= bulk density; WHC= water holding capacity; Pt= total porosity; As= air space; S= peat- 49 based substrate; V= vermicompost; B= biochar; Control = 100:00:00. Volume fraction (%). p= significance level. Different letters in numerical columns differ at p≤0.05 (Tukey-HSD test for Va, Pt and As; T3-Dunnett test for Db). Hortic. bras., Brasília, v.37, n.1, January-March 2019