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Reaction of wild Solanaceae rootstocks to the parasitism of (Meloidogyne javanica)

Reação de porta-enxertos de Solanáceas silvestres ao parasitismo (de Meloidogyne javanica)

ABSTRACT

Intensive production of vegetables in greenhouses can increase the amount of inoculum of soil-borne pathogens, such as the root-knot nematode. Thus, in this study we aimed to evaluate the potential of Solanaceae as rootstocks resistant to Meloidogyne javanica nematodes as an alternative to tomato grafting. The experiment consisted of seven treatments: wild species joá-vermelho (Solanum capsicoides), joá-bagudo (Solanum palinacanthum), joá-bravo (Solanum viarum), jurubeba (Solanum spp.) and the commercial tomato cultivars Santa Cruz Kada, Batalha and Guardião. The analyzed variables were gall index; egg mass index; final nematode population; reproduction factor (FR) and reaction: susceptibility, resistance and immunity; fresh shoot and root mass and number of eggs per gram of roots. The wild species joá-vermelho, joá-bagudo and jurubeba showed resistance, with the lowest indexes of galls, egg mass, final population of nematodes and number of eggs per gram of root, not differing from the resistant control treatment (hybrid rootstock Guardião), with a reproduction factor less than 1, showing potential to be used as a resistant rootstock to M. javanica. Joá-bravo species showed susceptibility to the root-knot nematode, with a FR>1, not differing from the susceptible tomato Santa Cruz Kada. These results confirm the resistance of wild species to nematode parasitism, which can prove the viability of use as possible alternative rootstocks, and reinforce the idea that more studies should be carried out aiming to provide more viable options for farmers and plantlet producers.

Keywords:
Solanum lycopersicum; root-knot nematode; grafting; resistance

RESUMO

A produção intensiva de hortaliças em ambiente protegido pode aumentar a quantidade de inóculo de patógenos habitantes do solo, a exemplo dos nematoides das galhas. Dessa forma, objetivou-se avaliar o potencial de solanáceas como porta-enxertos resistentes ao nematoide Meloidogyne javanica como alternativa à enxertia em tomateiro. O experimento foi constituído de sete tratamentos: as espécies silvestres joá-vermelho (Solanum capsicoides), joá-bagudo (Solanum palinacanthum), joá-bravo (Solanum viarum), jurubeba (Solanum spp.) e os tomateiros comerciais Santa Cruz Kada, Batalha e Guardião. As variáveis analisadas foram índice de galhas; índice de massas de ovos; população final de nematoides; fator de reprodução e reação: de suscetibilidade, resistência e imunidade; matéria da parte aérea fresca, matéria de raiz fresca e número de ovos por grama de raiz. As espécies joá-vermelho, joá-bagudo e jurubeba foram resistentes, apresentando os menores índices de galhas, massa de ovos, população final de nematoides e número de ovos por grama de raiz, não diferindo do tratamento testemunha resistente (porta-enxerto híbrido Guardião), com um fator de reprodução menor que 1, indicando potencial de utilização como porta-enxerto resistente a M. javanica. A espécie joá-bravo mostrou-se suscetível ao nematoide 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.

Palavras-chave:
Solanum lycopersicum; nematoide das galhas; enxertia; resistência

O ne of the main challenges faced by horticulture these days is to meet the growing demand for food due to global population growth (Rouphael et al., 2018ROUPHAEL, Y; KYRIACOU, MC; PETROPOULOS, SA; PASCALE, S; COLLA, G. 2018. Improving vegetable quality in controlled environments. Scientia Horticulturae 234: 275-289.), as well as to produce fresh, high-quality and free-chemical-residue food in order to meet the demands of consumers (Bisbis et al., 2018BISBIS, MB; GRUDA, N; BLANKE, M. 2018. Potential impacts of climate change on vegetable production and product quality - A review. Journal of Cleaner Production 170: 1602-1620.).

Vegetable production in the state of Parana showed an increase of 77% from 2,000 to 2,016, due to an increase in crop productivity, as a result of the producer organization and investment in technology (Salvador, 2017SALVADOR, CA. 2017. Olericultura - análise da conjuntura agropecuária - novembro de 2017. Secretaria da agricultura e do abastecimento (SEAB). Available at Available at http://www.agricultura.pr.gov.br . Accessed June, 2018.
http://www.agricultura.pr.gov.br...
). According to Instituto Paranaense de Assistência Técnica e Extensão Rural, these vegetables are grown essentially by family farmers, on average areas of approximately 3 hectares, in about 13% of family properties in the state (EMATER, 2016EMATER. 2016. A agricultura familiar e a olericultura no Paraná. Disponível em Disponível em http://www.emater.pr.gov.br/modules/noticias/article.php?storyid=4624 . Accessed on June, 2018.
http://www.emater.pr.gov.br/modules/noti...
).

In order to meet market demand, farmers use intensive production in protected environment, reducing, partially, the negative effects provided by harsh climatic conditions (Araújo et al., 2009ARAÚJO, JS; ANDRADE, AP; RAMALHO, CL; AZEVEDO, CAV. 2009. Cultivo do pimentão em condições protegidas sob diferentes doses de nitrogênio via fertirrigação. Revista Brasileira de Engenharia Agrícola e Ambiental 13: 559-565.; King et al., 2010KING, SR; DAVIS, AR; ZHANG, X; CROSBY, K. 2010. Genetics, breeding and selection of rootstocks for Solanaceae and Cucurbitaceae. Scientia Horticulturae 127: 106-111.; Bisbis et al., 2018BISBIS, MB; GRUDA, N; BLANKE, M. 2018. Potential impacts of climate change on vegetable production and product quality - A review. Journal of Cleaner Production 170: 1602-1620.). However, intensive vegetable cultivation under greenhouses may increase inoculums of soil pathogen, due to the fact that, when the producer specializes in growing one vegetable species, performs successive cultivation in this environment, limiting crop rotation (King et al., 2010; Rosa et al., 2013ROSA, JMO; WESTERICH, JN; WILCKEN, SRS. 2013. Reprodução de Meloidogyne javanica em olerícolas e em plantas utilizadas na adubação verde. Tropical Plant Pathology 38: 133-141.; Pinheiro et al., 2014PINHEIRO, JB; MENDONÇA, JL; RODRIGUES, CS; PEREIRA, RB; SUINAGA, FA. 2014. Avaliação de Solanum stramonifolium para reação a Meloidogyne enterolobii. Brasília: Embrapa Hortaliças (Boletim de Pesquisa e Desenvolvimento, 124). Available at Available at https://ainfo.cnptia.embrapa.br/digital/bitstream/item/117999/1/BPD-124.pdf . Accessed January, 2017.
https://ainfo.cnptia.embrapa.br/digital/...
).

Among the species, grown in protected environment, the tomato crop stands out due to its high sensitivity to inclement weather (Gusmão et al., 2006GUSMÃO, MTA; GUSMÃO, SAL; ARAÚJO, JAC. 2006. Produtividade de tomate tipo cereja cultivado em ambiente protegido e em diferentes substratos. Horticultura Brasileira 24: 431-436.; Bergougnoux et al., 2014BERGOUGNOUX, V. 2014. The history of tomato: From domestication to biopharming. Biotechnology Advances 32: 170-189.; Çelik et al., 2017ÇELIK, Ö; AYAN, A; ATAK, Ç. 2017. Enzymatic and non-enzymatic comparison of two different industrial tomato (Solanum lycopersicum) varieties against drought stress. Botanical Studies 58: 1-13.) and susceptibility to several pests and diseases, which makes this cultivation difficult, with economic and environmental risk factors, caused by excessive use of chemical products (Luz et al., 2007LUZ, JMQ; SHINZATO, AV; SILVA, MAD. 2007. Comparação dos sistemas de produção de tomate convencional e orgânico em cultivo protegido. Bioscience Journal 23: 7-15.; Loos et al., 2008LOOS, RA; SILVA, DJH; FONTES, PCR; PICANÇO, MC. 2008. Identificação e quantificação dos componentes de perdas de produção do tomateiro em ambiente protegido. Horticultura Brasileira 26: 281-286.).

Considering soil pathogens, the root-knot nematode belonging to the genus Meloidogyne is of great economic importance for tomato crop (Carvalho et al., 1999CARVALHO, JWA; MALUF, WR; FIGUEIRA, AR; GOMES, LAA. 1999. Obtenção de linhagens de tomateiro de crescimento determinado com resistência múltipla a nematóides de galhas e a tospovírus. Ciência e Agrotecnologia 23: 593-607.; Podestá et al., 2016PODESTÁ, GS; AMORA, DX; MAFFIA, LA; NASU, ÉGC; FERRAZ, S; FREITAS, LG. 2016. Effect of time between soil infestation with Pochonia chlamidosporia and planting on the efficacy of the fungus in managing Meloidogyne javanica. Crop Protection 90:77-83.). Its popular name derives from the main symptom presented by plants when affected by these pathogens, which consists of nourishing cells (gall nematodes), which act as a permanent feeding place, providing nutrients for the nematode development and interfering negatively in nutritional and water absorption by plants (Jones et al., 2013JONES, JT; HAEGEMAN, A; DANCHIN, EGJ; GAUR, HS; HELDER, J; MG H; KIKUCHI, T; MANZANILLA-LÓPEZ, R; PALOMARES-RIUS, JE; WESEMAEL, WML; PERRY, RN. 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14: 946-961.; Karssen et al., 2013KARSSEN, G; WESEMAEL, W; MOENS, M. 2013. Root-knot nematodes. In: PERRY, RN; MOENS, M (eds). Plant Nematology. 2nd edition, CAB International, Wallingford, UK, 73-108; Kepenekci et al., 2018KEPENEKCI, I; HAZIR, S; OKSAL, E; LEWIS, EE. 2018. Application methods of Steinernema feltiae, Xenorhabdus bovienii and Purpureocillium lilacinum to control root-knot nematodes in greenhouse tomato systems. Crop Protection 108: 31-38.).

The reaction of plants to the root-knot nematode can vary according to species and cultivar, being that the crop rotation, duration of the development cycle, planting season, population density and kind of soil also interfere in damage severity (Jones et al., 2013JONES, JT; HAEGEMAN, A; DANCHIN, EGJ; GAUR, HS; HELDER, J; MG H; KIKUCHI, T; MANZANILLA-LÓPEZ, R; PALOMARES-RIUS, JE; WESEMAEL, WML; PERRY, RN. 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14: 946-961.). Generally, these observed symptoms include reduced fruit yield and quality, slow growth, yellowish leaves, wilting in the hottest hours of the day, and decreased resistance to other biotic and abiotic factors (Jones et al., 2013; Podestá et al., 2016PODESTÁ, GS; AMORA, DX; MAFFIA, LA; NASU, ÉGC; FERRAZ, S; FREITAS, LG. 2016. Effect of time between soil infestation with Pochonia chlamidosporia and planting on the efficacy of the fungus in managing Meloidogyne javanica. Crop Protection 90:77-83.; Kepenekci et al., 2018KEPENEKCI, I; HAZIR, S; OKSAL, E; LEWIS, EE. 2018. Application methods of Steinernema feltiae, Xenorhabdus bovienii and Purpureocillium lilacinum to control root-knot nematodes in greenhouse tomato systems. Crop Protection 108: 31-38.).

The root-knot nematodes are mandatory endoparasites, which may be native or inserted into new production regions, through contaminated soils, root remnants or infected plants (Louws et al., 2010LOUWS, FJ; RIVARD, CL; KUBOTA, C. 2010. Grafting fruiting vegetables to manage soilborne pathogens, foliar pathogens, arthropods and weeds. Scientia Horticulturae 127: 127-146.). Although crop rotation with non-host species and soil fumigation are used to control these pathogens, resistance is still the most employed and sustainable strategy (Louws et al., 2010LOUWS, FJ; RIVARD, CL; KUBOTA, C. 2010. Grafting fruiting vegetables to manage soilborne pathogens, foliar pathogens, arthropods and weeds. Scientia Horticulturae 127: 127-146.).

The chemical nematicides generally used to control these pathogens are of high costs and present potential risks for beneficial soil microorganisms (Huang et al., 2014), environment and human health (Fournet et al., 2012FOURNET, S; KERLAN, MC; RENAULT, L; DANTEC, JP; ROUAUX, C; MONTARRY, J. 2012. Selection of nematodes by resistant plants has implications for local adaptation and cross‐virulence. Plant Pathology 62: 184-193.; Jones et al., 2013JONES, JT; HAEGEMAN, A; DANCHIN, EGJ; GAUR, HS; HELDER, J; MG H; KIKUCHI, T; MANZANILLA-LÓPEZ, R; PALOMARES-RIUS, JE; WESEMAEL, WML; PERRY, RN. 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14: 946-961.; Becker, 2014BECKER, JO. 2014. Plant health management: crop protection with nematicides. In: NEAL, KA. Encyclopedia of Agriculture and Food Systems. Oxford: Academic Press, p.400-407.; Onkendi et al., 2014ONKENDI, EM; KARIUKI, G; MARAIS, M; MOLELEKI, LN. 2014. The threat of root‐knot nematodes (Meloidogyne spp.) in Africa: a review. Plant Pathology 63: 727-737.; Kyriacou et al., 2017KYRIACOU, MC; ROUPHAEL, Y; COLLA, G; ZRENNER, R; SCHWARZ, D. 2017. Vegetable grafting: the implications of a growing agronomic imperative for vegetable fruit quality and nutritive value. Frontiers in Plant Science 8: 1-23.). Moreover, the increasing market for organic tomatoes does not allow the use of agrochemicals (López-Pérez et al., 2006LÓPEZ-PÉREZ, JALE; STRANGE, M; KALOSHIAN, I; PLOEG, AT. 2006. Differential response of Mi gene-resistant tomato rootstocks to root-knot nematodes (Meloidogyne incognita). Crop Protection 25: 382-388.; Lee et al., 2010LEE, JM; KUBOTA, C; TSAO, SJ; BIE, Z; ECHEVARRIA, PH; MORRA, L; ODA, M. 2010. Current status of vegetable grafting: diffusion, grafting techniques. Scientia Horticulturae 127: 93-105.).

Giving up growing tomato in areas infested with root-knot nematode is not a viable option for the farmer, especially when this area is the only option for cultivation. Thus, more sustainable strategies are necessary to make production in areas infested with these pathogens viable (Huang et al., 2016HUANG, 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.).

Grafting can be a technique used in an integrated management system aiming to minimize damage caused by root-knot nematode (Peil, 2003PEIL, RM. 2003. A enxertia na produção de mudas de hortaliças. Ciência Rural 33: 1169-1177.; Krumbein & Schwarz, 2013KRUMBEIN, A; SCHWARZ, D. 2013. Grafting: a possibility to enhance health-promoting and flavor compounds in tomato fruits of shaded plants? Scientia Horticulturae 149: 97-107.; Verdejo-Lucas et al., 2013VERDEJO-LUCAS, S; BLANCO, M; CORTADA, L; SORRIBAS, FJ. 2013. Resistance of tomato rootstocks to Meloidogyne arenaria and Meloidogyne javanica under intermittent elevated soil temperatures above 28 C. Crop Protection 46: 57-62.). This practice improves the crop quality, with more efficient water and nutritional use, increase in plant vigor and harvest time, making the tomato plant more tolerant to pathogen attack, such as phytonematods (Rizzo, et al., 2004RIZZO, AAN; CHAVES, FCM; LAURA, VA; GOTO, R. 2004. Avaliação de métodos de enxertia e porta-enxertos para melão rendilhado. Horticultura Brasileira 22: 808-810.; Lee et al., 2010LEE, JM; KUBOTA, C; TSAO, SJ; BIE, Z; ECHEVARRIA, PH; MORRA, L; ODA, M. 2010. Current status of vegetable grafting: diffusion, grafting techniques. Scientia Horticulturae 127: 93-105.; Kyriacou et al., 2017KYRIACOU, MC; ROUPHAEL, Y; COLLA, G; ZRENNER, R; SCHWARZ, D. 2017. Vegetable grafting: the implications of a growing agronomic imperative for vegetable fruit quality and nutritive value. Frontiers in Plant Science 8: 1-23.).

Although the genetic basis of rootstocks for tomato crop seems to be wide, considering the great quantity of species related to the crop which could be used, the current genetic basis is limited (King et al., 2010KING, SR; DAVIS, AR; ZHANG, X; CROSBY, K. 2010. Genetics, breeding and selection of rootstocks for Solanaceae and Cucurbitaceae. Scientia Horticulturae 127: 106-111.). Most commercially available rootstocks are high-cost hybrids, produced by specialized companies (King et al., 2010KING, SR; DAVIS, AR; ZHANG, X; CROSBY, K. 2010. Genetics, breeding and selection of rootstocks for Solanaceae and Cucurbitaceae. Scientia Horticulturae 127: 106-111.; Lopes et al., 2015LOPES, CA; BOITEUX, LS; ESCHEMBACK, V. 2015. Eficácia relativa de porta-enxertos comerciais de tomateiro no controle da murcha-bacteriana. Horticultura Brasileira 33: 125-130.).

These rootstocks make the production more expensive for farmers and that is why identifying alternative rootstocks, resistant or tolerant, as an alternative to commercial hybrids, is essential. Wild Solanum species are sources of resistance characteristics to various soil pathogens, fruit quality and other important characteristics to be considered in order to improve crops, being possible alternative rootstocks for tomato crop (Keatinge et al., 2014KEATINGE, JDH; LIN, LJ; EBERT, AW; CHEN, WY; HUGHES, JA; LUTHER, GC; WANG, JF; RAVISHANKAR, M. 2014. Overcoming biotic and abiotic stresses in the Solanaceae through grafting: current status and future perspectives. Biological Agriculture & Horticulture 30: 272-287.; Migicovsky & Myles, 2017MIGICOVSKY, Z; MYLES, S. 2017. Exploiting wild relatives for genomics-assisted breeding of perennial crops. Frontiers in Plant Science 8: 460.).

Some studies on wild Solanum species as rootstocks, to control Fusarium oxysporum f. sp., Lycopersici, Verticillium dahliae, Ralstonia solanacearum, and root-knot nematode, have been carried out at Embrapa Hortaliças. These studies showed promising results (Pinheiro et al., 2009PINHEIRO, JB; MENDONÇA, JL; SANTANA, JP. 2009. Solanáceas silvestres: potencial de uso como porta-enxertos resistentes ao nematóide-das-galhas (Meloidogyne spp.). Brasília: Embrapa Hortaliças (Boletim de Pesquisa e Desenvolvimento, 57). Available at https://www.infoteca.cnptia.embrapa.br /bitstream/doc/783050/1/bpd57.pdf. Accessed January, 2017.
https://www.infoteca.cnptia.embrapa.br /...
, 2011PINHEIRO, JB; MENDONÇA, JL; SANTANA, JP. 2011. Wild Solanaceae: potential for the use as rootstocks resistant to root-knot nematode (Meloidogyne spp.). Acta Horticulturae 917: 243-247., 2014PEREIRA, RB; MENDONÇA, JL; AGUIAR, FM; RIBEIRO, MCV; PINHEIRO, JB. 2014. Reação de acessos de jurubeba Juna (Solanum stramonifolium) a Fusarium oxysporum f. sp. lycopersici raça 3. Brasília: Embrapa Hortaliças (Boletim de Pesquisa e Desenvolvimento 113). Available at Available at https://ainfo.cnptia.embrapa.br/digital/ bitstream/item/118235/1/BPD-113.pdf . Accessed June, 2018.
https://ainfo.cnptia.embrapa.br/digital/...
; Pereira et al., 2014PEREIRA, RB; MENDONÇA, JL; AGUIAR, FM; RIBEIRO, MCV; PINHEIRO, JB. 2014. Reação de acessos de jurubeba Juna (Solanum stramonifolium) a Fusarium oxysporum f. sp. lycopersici raça 3. Brasília: Embrapa Hortaliças (Boletim de Pesquisa e Desenvolvimento 113). Available at Available at https://ainfo.cnptia.embrapa.br/digital/ bitstream/item/118235/1/BPD-113.pdf . Accessed June, 2018.
https://ainfo.cnptia.embrapa.br/digital/...
; Lopes & Mendonça, 2016LOPES, CA; BOITEUX, LS; ESCHEMBACK, V. 2015. Eficácia relativa de porta-enxertos comerciais de tomateiro no controle da murcha-bacteriana. Horticultura Brasileira 33: 125-130.). In nematodes, the potential of wild Solanum species had been already proved in relation to parasitism of M. incognita (González et al., 2010GONZÁLEZ, FM; GÓMEZ, L; RODRÍGUEZ, MG; PIÑÓN, M; CASANOVA, A; GÓMEZ, O; RODRÍGUEZ, Y. 2010. Respuesta de genotipos de solanáceas frente a Meloidogyne incognita (Kofoid y White) Chitwood raza 2 y M. arenaria (Neal) Chitwood. Revista de Protección Vegetal 25: 51-57.; Dhivya et al., 2014DHIVYA, R; SADASAKTHI, A; SIVAKUMAR, M. 2014. Response of wild solanum rootstocks to root-knot nematode (Meloidogyne incognita Kofoid and White). International Journal of Plant Sciences 9: 117-122.), M. arenaria (González et al., 2010GONZÁLEZ, FM; GÓMEZ, L; RODRÍGUEZ, MG; PIÑÓN, M; CASANOVA, A; GÓMEZ, O; RODRÍGUEZ, Y. 2010. Respuesta de genotipos de solanáceas frente a Meloidogyne incognita (Kofoid y White) Chitwood raza 2 y M. arenaria (Neal) Chitwood. Revista de Protección Vegetal 25: 51-57.) and M. javanica (Boiteux & Charchar, 1996BOITEUX, LS; CHARCHAR, JM. 1996. Genetic resistance to root-knot nematode (Meloidogyne javanica) in eggplant (Solanum melongena). Plant Breeding 115: 198-200.).

In this context, the aim of this study was to evaluate the reaction of rootstocks of wild species joá-vermelho (Solanum capsicoides), joá-bagudo (Solanum palinacanthum), joá-bravo (Solanum viarum) and jurubeba (Solanum spp.) to parasitism of Meloidogyne javanica.

MATERIAL AND METHODS

The experiment was carried out in a greenhouse at Centro de Biotecnologia Agropecuária of Paraná State (26°11’43”S, 52°41’12”W). In this study, the authors tested the wild species joá-vermelho (S. capsicoides), joá-bagudo (S. palinacanthum), joá-bravo (S. viarum), jurubeba (Solanum spp.) and tomato Santa Cruz Kada (root-knot-susceptible variety), Batalha (susceptible hybrid) and Guardião (resistant-hybrid tomato rootstock) commercial tomatoes. Each experimental unit consisted of a pot with one plant, in completely randomized experimental design, with 10 replications per treatment.

The inoculum of root knot nematode M. javanica used in the experiment was obtained from a pure population kept in tomato plants, grown in a greenhouse. The nematode eggs were obtained according to the methodology described by Hussey & Barker (1973)BONETTI, JIS; FERRAZ, S. 1981. Modificações do método de Hussey & Barker para extração de ovos de Meloidogyne exígua em raízes de cafeeiro. Fitopatologia Brasileira 6: 553., modified by Bonetti & Ferraz (1981BONETTI, JIS; FERRAZ, S. 1981. Modificações do método de Hussey & Barker para extração de ovos de Meloidogyne exígua em raízes de cafeeiro. Fitopatologia Brasileira 6: 553.). The seedlings of all wild and commercial species were produced in a greenhouse, in polystyrene trays with 128 cells. Plantlets were transplanted 30 days after emergence, in 1-kg-capacity plastic containers, with substrate, soil and sand in the ratio 2:1 (v:v), autoclaved in advance for 1 h at 120˚C, 1 atm, (Ito et al., 2014ITO, LA; GAION, LA; GALATTI, FS; BRAZ, LT; SANTOS, JM. 2014. Resistência de porta-enxertos de cucurbitáceas a nematóides e compatibilidade da enxertia em melão. Horticultura Brasileira 32: 297-302.). One week after seedling transplant, the nematode was inoculated using 2 mL of suspension containing 5,000 eggs of M. javanica through 4 equidistant holes open in soil, close to the plant stem.

Sixty days after nematode inoculation, gall index (IG), egg mass index (IMO), final nematode population (Pf); reproduction factor (FR) and reaction of: susceptibility (S), resistance (R) and immunity (I); fresh shoot mass (MPAF); fresh root mass (MRF); number of eggs per gram of root (NOGR) were evaluated.

In order to determine gall index (IG), the scale proposed by Charchar et al. (2003CHARCHAR, JM; GONZAGA, V; GIORDANO, LB; BOITEUX, LS; REIS, NVB; ARAGÃO, FAS. 2003. Reações de cultivares de tomate à infecção por população mista de Meloidogyne incognita raça 1 e M. javanica em estufa plástica e campo. Nematologia Brasileira 27: 49-54.) was used: after being washed, the roots were graded from 1 to 5 (1= without galls; 2= up to 10 small galls; 3= up to 50 small galls; 4= more than 50 small galls and up to 10 big galls; 5= roots with more than 50 small galls and more than 10 big galls).

The egg mass index (IMO) was calculated following the scale proposed by Huang et al. (1986HUANG, SP; MIRANDA, JEC; MALUF, WR. 1986. Resistance to root-knot nematodes in a Brazilian sweet potato collection. Fitopatologia Brasileira 11: 761-767.), considering a grading scale from 1 to 5 (1= without egg masses; 2= 1 to 5 egg masses; 3= 6 to 15 egg masses; 4= 16 to 30 egg masses; 5= more than 30 egg masses). Coloration methodology was performed according to Rocha et al. (2005ROCHA, FS; MUNIZ, MFS; CAMPOS, VP. 2005. Coloração de fitonematoides com corantes usados na indústria alimentícia brasileira. Nematologia Brasileira 29: 293-297.).

Final nematode population per root (Pf) was obtained according to the methodology described by Hussey & Barker (1973)BONETTI, JIS; FERRAZ, S. 1981. Modificações do método de Hussey & Barker para extração de ovos de Meloidogyne exígua em raízes de cafeeiro. Fitopatologia Brasileira 6: 553., modified by Bonetti & Ferraz (1981BONETTI, JIS; FERRAZ, S. 1981. Modificações do método de Hussey & Barker para extração de ovos de Meloidogyne exígua em raízes de cafeeiro. Fitopatologia Brasileira 6: 553.).

Reproduction factor (FR) was calculated using the ratio between final nematode population (Pf) and initial population (Pi), and classified according to Oostenbrink (1966OOSTENBRINK, M. 1966. Major characteristics of the relation between nematodes and plants. Medelingen Van De Landbouwhogeschool 66: 1-46.), expressed as follows: FR= 0: immune; FR<1: resistant; FR≥ 1: susceptible.

Variable data were submitted to analysis of variance using F test, comparing the treatment averages by Scott-Knott test (p<0.05). For reproduction factor (FR), the averages of treatments using wild Solanaceae were compared to controls (commercial cultivars) by Dunnett test (p<0.05). Analyses were performed using Assistat software (Silva & Azevedo, 2002SILVA, FAS; AZEVEDO, CAV. 2002. Versão do programa computacional Assistat para o sistema operacional Windows. Revista Brasileira de Produtos Agroindustriais 4: 71-78.).

RESULTS AND DISCUSSION

The wild species joá-bagudo and jurubeba showed the lowest gall index values (IG). For egg mass (IMO), jurubeba showed the lowest value, followed by joá-bagudo and joá-vermelho. On the other hand, joá-bravo showed the highest indexes for both variables (Table 1).

Table 1
Average values of gall index (IG), egg mass index (IMO), final nematode population (Pf), fresh shoot mass (MPAF), fresh root mass (MRF) and number of eggs per gram of roots (NOGR) of Meloidogyne javanica on alternative and commercial rootstocks. Pato Branco, UTFPR, 2015.

Final nematode population (Pf) and number of eggs per gram of root (NOGR) of joá-vermelho, joá-bagudo and jurubeba showed lower values (Table 1), in comparison to the other species, proving the lowest root-knot nematode multiplication rate. However, the species joá-bravo showed the highest value for both variables, due to high ratio of Pf/MRF, proving the high susceptibility of this species to nematode M. javanica.Silva et al. (2013SILVA, SLS; SANTOS, TFS; RIBEIRO, NR; SILVÉRIO, AT; MORAIS, TS. 2013. Reação de plantas daninhas a Meloidogyne incognita e M. javanica, Nematologia Brasileira 37: 57-60.) found similar values for Pf in another species of the wild Solanaceae, Maria-pretinha (Solanum americanum), which showed to be susceptible with a final population of 34,720 eggs.

Variable MPAF showed lower value for wild Solanaceae joá-bravo, for its high susceptibility to nematode M. javanica, followed by jurubeba. On the other hand, although the species joa-bagudo presented a higher value when compared to the other wild Solanaceae species, did not differ statistically from joá-vermelho.

The lowest development of shoot area of the plants is related to the highest number of galls which cause interferences on plant roots, which interfere on efficient absorption of nutrients and consequently on plant development (Jones et al., 2013JONES, JT; HAEGEMAN, A; DANCHIN, EGJ; GAUR, HS; HELDER, J; MG H; KIKUCHI, T; MANZANILLA-LÓPEZ, R; PALOMARES-RIUS, JE; WESEMAEL, WML; PERRY, RN. 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14: 946-961.; Karssen et al., 2013KARSSEN, G; WESEMAEL, W; MOENS, M. 2013. Root-knot nematodes. In: PERRY, RN; MOENS, M (eds). Plant Nematology. 2nd edition, CAB International, Wallingford, UK, 73-108; Kepenekci et al., 2018KEPENEKCI, I; HAZIR, S; OKSAL, E; LEWIS, EE. 2018. Application methods of Steinernema feltiae, Xenorhabdus bovienii and Purpureocillium lilacinum to control root-knot nematodes in greenhouse tomato systems. Crop Protection 108: 31-38.). Therefore, plants showing lower MPAF generally show higher susceptibility to M. javanica.

In relation to MRF, the species joá-bravo showed the lowest value (in relation to the other wild Solanaceae species) and did not differ statistically from jurubeba. These results were obtained due to the slow initial growth of jurubeba, which results in a lower development, considering that this species showed reduced number of galls.

The species joá-bagudo, jurubeba and joá-vermelho showed to be resistant to M. javanica, when compared to the susceptible commercial controls (Batalha and Santa Cruz Kada) and similar to resistant-hybrid rootstock Guardião (Table 2), showing FR<1 according to Oostenbrink (1966OOSTENBRINK, M. 1966. Major characteristics of the relation between nematodes and plants. Medelingen Van De Landbouwhogeschool 66: 1-46.). However, the species joá-bravo showed high susceptibility showing FR>1, not differing from susceptible tomato Santa Cruz Kada, which proved viability of the inoculum used in the present study, showing FR>1.

Table 2
Average values of reproduction factor (FR) and rootstock reaction of wild Solanaceae species submitted to Meloidogyne javanica parasitism and comparison with susceptible and resistant controls. Pato Branco, UTFPR, 2015.

The results found in this study corroborate the ones found by Pinheiro et al. (2009PINHEIRO, JB; MENDONÇA, JL; SANTANA, JP. 2009. Solanáceas silvestres: potencial de uso como porta-enxertos resistentes ao nematóide-das-galhas (Meloidogyne spp.). Brasília: Embrapa Hortaliças (Boletim de Pesquisa e Desenvolvimento, 57). Available at https://www.infoteca.cnptia.embrapa.br /bitstream/doc/783050/1/bpd57.pdf. Accessed January, 2017.
https://www.infoteca.cnptia.embrapa.br /...
), who observed that the species S. asperolanatum, S. stramonifolium and Solanum spp., showed to be resistant to Meloidogyne incognita race 1, whereas S. straminifolium, S. paniculatum, and S. subinerme were resistant to Meloidogyne enterolobii, Sin.: M. mayaguensis. Some studies evaluating different accessions of Solanum stramonifolium in relation to parasitism of nematode M. enterolobii, Pinheiro et al. (2014) found 6 accessions of Solanaceae resistant to 17 studied species, being suitable rootstocks for Solanaceae in areas infested with this pathogen. Besides, Dhivya et al. (2014DHIVYA, R; SADASAKTHI, A; SIVAKUMAR, M. 2014. Response of wild solanum rootstocks to root-knot nematode (Meloidogyne incognita Kofoid and White). International Journal of Plant Sciences 9: 117-122.), evaluating rootstocks of wild Solanaceae resistant to M. incognita, obtained similar values for joá-bravo with FR>1, showing to be susceptible, however five from the other evaluated Solanaceae showed to be resistant or moderately resistant to the pathogen.

These results confirm the resistance of wild species (belonging to this family) to nematode parasitism, which can prove the viability of using them as alternative rootstocks, and reinforce the idea that further studies on grafting should be carried out, aiming to provide more viable options for farmers.

Although the wild Solanaceae species (joá-bagudo, joá-vermelho and jurubeba), evaluated in the present study, showed resistance to the nematode M. javanica, the compatibility of these species is another important factor to be taken into account. In this context, Simões (2014SIMÕES, AC. 2014. Compatibilidade de tomateiro sob diferentes portaenxertos e métodos de enxertia em sistema orgânico. Enciclopédia Biosfera 10: 961-972.) obtained compatibility of jiló and jurubeba species as rootstocks for tomato cultivar IPA-6. Farias et al. (2013FARIAS, EAP; FERREIRA, RLF; ARAÚJO NETO, SE; COSTA, FC; NASCIMENTO, DS. 2013. Organic production of tomatoes in the amazon region by plants grafted on wild Solanum rootstocks. Ciência e Agrotecnologia 37: 323-329.) obtained S. gilo, S. lycocarpum and S. stramonifolium as alternative rootstocks compatible with tomato and suitable for conditions in Brazilian Amazon Region. This fact demonstrates feasibility of grafting and the importance of further studies aiming to show the efficiency of these species as alternative rootstocks for tomato crop.

ACKNOWLEDGEMENTS

To Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for scholarship granted to the first author.

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Publication Dates

  • Publication in this collection
    15 Apr 2019
  • Date of issue
    Jan-Mar 2019

History

  • Received
    26 July 2017
  • Accepted
    10 Apr 2018
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