First report of a genetic map and evidence of QTL for resistance to CABMV in a segregating population of Passiflora

  • Eileen Azevedo SantosEmail author
  • Alexandre Pio Viana
  • Fernando Henrique de Barros Walter
  • Josie Cloviane de Oliveira Freitas
  • Helaine Christine Cancela Ramos
  • Marcela Santana Bastos Boechat


The fruit woodiness disease induced by the cowpea aphid-borne mosaic virus (CABMV) is considered to be of the greatest economic importance in the Passiflora crop. There are no reports of resistance to CABMV identified in P. edulis, and none of the Passiflora cultivars registered thus far are resistant to the virus. On this basis, breeding programs have resorted to wild species to identify sources of resistance that can be efficiently transferred to the cultivated species via interspecific crossing. A preliminary map for a segregating population of Passiflora based on seven microsatellite markers and 43 inter-simple sequence repeat markers was constructed using a BC1 population composed of 187 individuals. The map was generated using JoinMap software and the linkage groups were formed and ranked using a lod score of 3.0 and a maximum recombination value of 40%. The linkage map consisted of 50 markers - 43 ISSR and seven SSR. The generated map covered 1017.1 cM, with one larger linkage group of 211.2 cM and eight smaller groups ranging from 1.8–179.3 cM. Each linkage group contained 3–12 markers, with one marker occurring at every 20.34 cM. Of the total markers, 55% were mapped, and 40.68% of the Passiflora map was covered. Seven small-effect QTL were detected for resistance to CABMV in seven linkage groups. The phenotypic variation rate ranged from 1.45 to 4.68%, totaling 21.81%. This is the first report involving QTL mapping for resistance to CABMV in a segregating population of Passiflora obtained from interspecific crossing.


Complex trait Genetic map Quantitative trait loci CABMV P. edulis P. setacea 


Compliance with ethical standards

The authors declare that they have no conflict of interest and certify that this work was carried out in a public research organization and that no potential source of conflict of interest exists with any other public or private research organization. This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Blas, A. L., Yu, Q., Veatch, O. J., Paull, P. E., Moore, P. H., & Ming, R. (2012). Genetic mapping of quantitative trait loci controlling fruit size and shape in papaya. Molecular Breeding, 29, 457–466. Scholar
  2. Braga, M. F. (2011). Mapeamento de QTL (Quantitative Trait Loci) associados à resistência do maracujá-doce à bacteriose. Tese apresentada para obtenção do título de Doutor em Agronomia. Área de concentração: Genética e Melhoramento de Plantas. Piracicaba 2011.Google Scholar
  3. Broman KW and Sen SAA (2009) Guide to QTL Mapping with R/qtl. Springer, New York.Google Scholar
  4. Campbell, C. D., & Madden, L. V. (1990). Introduction to plant disease epidemiology. New York: John Willey.Google Scholar
  5. Carneiro, M. S., Camargo, L. E. A., Coelho, A. G., Vencovsky, R., Leite, R. P., Stenzel, N. M. C., & Vieira, M. L. C. (2002). RAPD-based genetic linkage maps of yellow passion fruit (Passiflora edulis Sims.). Genome, 45, 670–678. Scholar
  6. Cerqueira-Silva, C. B. M., Conceição, L. D. H. C. S., Souza, A. P., & Corrêa, R. X. (2014a). A history of passion fruit woodiness disease with emphasis on the current situation in Brazil and prospects for Brazilian passion fruit cultivation. European Journal of Plant Pathology, 139(2), 255–264. Scholar
  7. Cerqueira-Silva, C. B. M., Santos, E. S. L., & Vieira, J. G. P. (2014b). New microsatellite markers for wild and commercial species of Passiflora (Passifloraceae) and cross-amplification. Applications in Plant Sciences, 2(2).
  8. Cerqueira-Silva, C. B. M., Jesus, O. N., Oliveira, E. J., Santos, E. S. L., & Souza, A. P. (2015). Characterization and selection of passion fruit (yellow and purple) accessions based on molecular markers and disease reactions for use in breeding programs. Euphytica, 202(3), 345–359. Scholar
  9. Freitas, J. C. O., Viana, A. P., Santos, E. A., Silva, F. H. L., Paiva, C. L., Rodrigues, R., Souza, M. M., & Eiras, M. (2015). Genetic basis of the resistance of a passion fruit segregant populationto cowpea aphid-borne mosaicvirus (CABMV). Tropical Plant Pathology, 40, 291–297. Scholar
  10. IBGE. (2016). Instituto Brasileiro de Geografia e Estatística. Banco de dados agregados: produção agrícola municipal. Rio de Janeiro. Disponível Acesso em 06 de junho 2016.
  11. Khan, M. A., & Korban, S. S. (2012). Association mapping in forest tree sand fruit crops. Journal of Experimental Botany, 63(11), 4045–4060. Scholar
  12. Kosambi, D. D. (1944). The estimation of map distance from recombination values. Annuaire of Eugenetics, 12, 172–175.Google Scholar
  13. Kunihisa, M. S., Moriya, K., Abe, K., Okada, T., Haji, T., Hayashi, H., Kim, C., Nishitani, S., & Yamamoto, T. (2014). Identification of QTLs for fruit quality traits in Japanese apples: QTL for early ripening are tightly linked to preharvest fruit drop. Breeding Science, 64, 240–251. Scholar
  14. Lopes, R., Teresa, M., & Lopes, G. (2006). Linkage and mapping of resistance genes to Xanthomonas axonopodis pv.passiflorae in yellow passion fruit. Genome, 49, 17–29. Scholar
  15. Moraes, M. C., Geraldi, I. O., Matta, F. P., & Vieira, M. L. C. (2005). Genetic and phenotypic parameter estimates for yield and fruit quality traits from a single wide cross in yellow passion fruit. Horticultural Science, 40(7), 1978–1981.Google Scholar
  16. Moulin, M. M., Rodrigues, R., Ramos, H. C. C., Bento, C. S., Sudré, C. P., Gonçalves, L. S. A., & Viana, A. P. (2015). Construction of an integrated genetic map for Capsicum baccatum L. Genetics and Molecular Research, 14, 6683–6694. Scholar
  17. Novaes, Q. S., & Rezende, J. A. M. (1999). Possível aplicação do DAS-ELISA indireto na seleção de maracujazeiro tolerante ao ‘Passionfruit Woodiness Virus’. Fitopatologia Brasileira, 24, 76–79.Google Scholar
  18. Oliveira, E. J., Vieira, M. L., Garcia, A. A. F., Munhoz, C. F., Margarido, G. R. A., Matta, P., & Moraes, M. M. (2008). An integrated molecular map of yellow passion fruit based on simultaneous maximum-likelihood estimation of linkage and linkage phases. Journal of the American Society for Horticultural Science, 133(1), 35–41.CrossRefGoogle Scholar
  19. Oliveira, N. N. S., Viana, A. P., Quintal, S. R., Paiva, C. L., & Marinho, C. S. (2014). Análise de distância genética entre acessos do gênero Psidium via marcadores ISSR. Rev. Bras. Frutic. Jaboticabal, 36(4), 917–923. Scholar
  20. Pádua, J. G., Oliveira, E. J., Zucchi, M. I., Oliveira, G. C. X., Camargo, L. E. A., & Vieira, M. L. C. (2005). Isolation and characterization of microsatellite markers from the sweet passion fruit (Passifloraalata Curtis: Passifloraceae). Molecular Ecology Notes, 5, 863–865. Scholar
  21. Pereira, G. S., Nunes, E. S., Laperuta, L. C., Braga, M. F., Penha, H. A., Diniz, A. L., Munhoz, C. F., Gazaffi, R., Garcia, A. A. F., & Vieira, M. L. C. (2013). Molecular polymorphism and linkage analysis in sweet passion fruit, an outcrossing species. Annals of Applied Biology, 162(3), 347–361. Scholar
  22. Pinheiro, C. R. (2015). Mapeamento de QTL (QuantitativeTrait Loci) associados à resposta do maracujá-doce à bacteriose usando a abordagem de modelos mistos, 2015. Universidade de São Paulo “Escola Superior de Agricultura Luís de Queiroz.”Google Scholar
  23. Priyamedha, B. K., Singh, G., Sangha, M. K. K., & Banga, S. S. (2012). RAPD, ISSR and SSR based integrated linkage map from an F2 hybrid population of resynthesized and natural Brassica carinata. National Academy Science Letters, 35, 303–308. Scholar
  24. Qi, X., Pittaway, T. S., Lindup, S., Liu, H., Waterman, E., Padi, F. K., Hash, C. T., Zhu, J., Gale, M. D., & Devos, K. M. (2004). An integrated genetic map and a new set of simple sequence repeat markers for pearl millet, Pennisetum glaucum. Theoretical and Applied Genetics, 109, 1485–1493. Scholar
  25. Santos, L. F., Oliveira, E. J., & Santos Silva, A. (2011). ISSR markers as a tool for the assessment of genetic diversity in Passiflora. Biochemical Genetics, 49(7–8), 540–554. Scholar
  26. Santos, E. A., Viana, A. P., Freitas, J. C. O., Souza, M. M., & Paiva, C. L. (2014). Phenotyping of Passiflora edulis, P. setacea, and their hybrids by a multivariate approach. Genetics and Molecular Research, 13(4), 9828–9845. Scholar
  27. Santos, E. A., Viana, A. P., Freitas, J. C. O., Silva, F. H. L., Rodrigues, R., & Eiras, M. (2015). Resistance to cowpea aphid-borne mosaic virus in species and hybrids of Passiflora: Advances for the control of the passion fruit woodiness disease in Brazil. European Journal of Plant Pathology, 143, 85–98. Scholar
  28. Van Ooijen, J. W. (2006). JoinMap version 4.0: Software for the calculation of genetic link age maps. Kyazma BV, Wageningen, the Netherlands, 23p.Google Scholar
  29. Van Ooijen, J. W., Voorrips, R. E. (2001). Join map version 3.0: Software for the calculation of genetic link age maps (software). Wageningen. Plant Research International, 51p.Google Scholar
  30. Wu, R., Ma, C. X., Painter, I., & Zeng, Z. B. (2002). Simultaneous maximum likelihood estimation of link age and linkage phases in outcrossing species. Theoretical Population Biology (New York), 61, 349–336. Scholar
  31. Yamamoto, T., Terakami, S., Takada, N., Nishio, S., Onoue, N., Nishitani, C., Kunihisa, M., Inoue, E., Iwata, H., Hayashi, T., Itai, A., & Saito, T. (2014). Identification of QTLs controlling harvest time and fruit skin color in Japanese pear (PyruspyrifoliaNakai). Breeding Science, 64, 351–361. Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2019

Authors and Affiliations

  • Eileen Azevedo Santos
    • 1
    Email author
  • Alexandre Pio Viana
    • 1
  • Fernando Henrique de Barros Walter
    • 1
  • Josie Cloviane de Oliveira Freitas
    • 2
  • Helaine Christine Cancela Ramos
    • 1
  • Marcela Santana Bastos Boechat
    • 1
  1. 1.Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), Center of Agricultural Sciences and TechnologyCampos dos GoytacazesBrazil
  2. 2.Universidade Estadual de Goiás (UEG) - Posse CampusPosseBrazil

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