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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

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Abstract

The potyvirus-induced passion fruit woodiness disease (PWD) is considered the most important limiting factor for passion fruit production in several countries. In Brazil, PWD is caused by the Cowpea aphid-borne mosaic virus (CABMV), and to date there are no reports on the existence of P. edulis genotypes resistant to this virus. Thus, resistance gene introgression from wild Passiflora species for a commercial species, via interspecific hybridization, is one of the strategies adopted in order to control the disease. The current study’s goals were to: confirm CABMV occurrence under field conditions; assess the resistance to CABMV in 178 Passiflora genotypes constituted by interspecific hybrids and their parents (P. edulis and P. setacea), as well as to estimate genetic parameters for the area under the disease progress curve (AUDPC), in order to obtain cultivars of sour passion fruit resistant to CABMV in future. The experimental design was set according to unbalanced randomized blocks with two repetitions. Data referring to the AUDPC were analyzed by means of the mixed models methodology (REMI/BLUP). CABMV infections were confirmed in sour passion fruit plants and in interspecific hybrids by observing foliar mosaic symptoms and by PTA-ELISA with specific antiserum against CABMV. There was a difference on the intensity of symptoms induced by CABMV for the 178 Passiflora genotypes assessed under natural occurrence conditions. The higher AUDPC values were obtained for 41 hybrids and for all P. edulis genotypes. In turn, lower values were estimated for 115 hybrid genotypes and for all P. setacea individuals. Of the 31 genotypes assessed by PTA-ELISA, 28 were considered resistant, out of those three P. setacea genotypes and 25 hybrids. Estimated AUDPC heritability values (0.99) and accuracy (0.99) enable inferring that resistance to CABMV within the assessed population was highly inheritable, allowing high selective efficiency. Resistant hybrid plants will be able to be selected and recombined with P. edulis genotypes and, again, assessed in order to corroborate the resistance to the virus, providing means of following up with the breeding genetic program on CABMV resistance.

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References

  • Al-Kaff, N. S., Covey, S. N., Kreike, M. M., Pinder, R., & Dale, P. J. (1998). Transcriptional and post transcriptional plant gene silencing in response to a pathogen. Science, 279, 2113–2115.

    Article  CAS  PubMed  Google Scholar 

  • Alves, R. M., Resende, M. D., Bandeira, B. D. S., Pinheiro, T. M., & Farias, D. C. R. (2009). Evolução da vassoura-de-bruxa e avaliação da resistência em progênies de cupuaçuzeiro. Revista Brasileira de Fruticultura Jaboticabal, 31(4), 1022–1032.

    Article  Google Scholar 

  • Barros, D. R., Alfenas, Z. P., Beserra, J. E. A., Antunes, T. F. S., & Zerbini, F. M. (2011). Comparative analysis of the genomes of two isolates of Cowpea aphid-borne mosaic virus (CABMV) obtained from different hosts. Archives of Virology, 156(6), 1085–1091.

    Article  CAS  PubMed  Google Scholar 

  • Bernacci, L. C.,Cervi, A. C., Milward-De-Azevedo, M. A., Nunes, T. S., Imig, D. C., Mezzonato, A. C. (2013) Passifloraceae In: Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. Disponível em: http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB128567

  • Beserra Júnior, J. E., Maluf, W. R., Figueira, A. R., & Barguil, B. M. (2006). Herança da Resistência ao Watermelon mosaic virus em Melancia (Citrullus lanatus L.). Fitopatologia Brasileira, 31(3), 1–4.

    Article  Google Scholar 

  • Campbell, C., & Madden, L. V. (1990). Introduction to plant disease epidemiology. New York: Wiley.

    Google Scholar 

  • Cavichioli, J. C., Corrêa, L. D. S., Narita, N., Kasai, F. S., et al. (2011). Incidência e Severidade do vírus do endurecimento dos frutos em maracujazeiros enxertados em pé-franco. Revista Brasileira de Fruticultura, 33, 411–414.

  • Cerqueira-Silva, C. B. M., Moreira, C. N., Figueira, A. R., Corrêa, R. X., Oliveira, A. C., et al. (2008). Detection of a resistance gradient to Passion fruit woodiness virus and selection of “yellow” passion fruit plants under field conditions. Genetics and Molecular Research, 7(4), 1209–1216.

    Article  CAS  PubMed  Google Scholar 

  • Cerqueira-Silva, C. B. M., Melo, J. R. F., Corrêa, R. X., Oliveira, A. C., et al. (2012). Selection of pathometric variables to assess resistance and infectivity in the passion fruit woodiness pathosystem. European Journal of Plant Pathology, 134(3), 489–495.

    Article  Google Scholar 

  • Cerqueira-Silva, C. B. M., Conceição, L. D. H. C. S., Souza, A. P., Corrêa, R. X., et al. (2014). 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.

    Article  Google Scholar 

  • Chagas, C. M., Kitajima, E. W., & Lin, M. T. (1981). Grave moléstia em maracujá amarelo (Passiflora edulis f. flavicarpa) no Estado da Bahia, causado por um isolado do vírus do “woodiness” do maracujá. Fitopatologia Brasileira, 6(2), 259–268.

    Google Scholar 

  • Chagas, C. M., Rezende, J. A. M., Colariccio, A., & Piza, C. T., Jr. (1992). Ocorrência do vírus do endurecimento dos frutos do maracujazeiro (VEFM) no estado de São Paulo. Revista Brasileira de Fruticultura, 14, 187–190.

    Google Scholar 

  • Coimbra, K. G. (2010). Desempenho Agronômico de Progênies de Maracujazeiro-Azedo no Distrito Federal. Dissertação (Mestrado em Agronomia) - Brasília – DF, Universidade de Brasília, 125.

  • Fischer, I. H., Rezende, J. A. M. (2008). Diseases of passion flower (Passiflora spp.). Pest technology, 2(1):1–19.

  • Garcêz, R. M., Silva, L. A., Chaves, A. L. R., Eiras, M., Meletti, L. M. M., Azevedo-Filho, J. A., & Colariccio, A. (2011). Monitoring of the aphid fauna of vector-borne viruses in a newly introduced yellow passion-fruit crop. In: Hemipteran-plant interactions symposium. Anais… Abstract number 39. July 11–14, 2011. Piracicaba, São Paulo, Brazil.

  • Ha, C., Coombs, S., Revill, P. A., Harding, R. M., Vu, M., & Dale, J. L. (2008). Design and application of two novel degenerate primer pairs for the detection and complete genomic characterization of potyviruses. Archives of Virology, 153(1), 25–36.

    Article  CAS  PubMed  Google Scholar 

  • IBGE (2014). Instituto Brasileiro de Geografia e Estatística. Banco de dados agregados: produção agrícola municipal. Rio de Janeiro. Disponível em: http://www.sidra.ibge.gov.br/bda/tabela/listabl.asp?c=1613&z=p&o=33.

  • Inoue, A. K., Mello, R. N., Nagata, T., & Kitajima, E. W. (1995). Characterization of Passion fruit woodness virus isolates from Brasilia and surrounding region, Brazil. Fitopatology, 20, 479–487.

    Google Scholar 

  • Iwai, H., Yamashita, Y., Nishi, N., & Nakamura, M. (2006). The potyvirus associated with the dappled fruit of Passiflora edulis in Kagoshima prefecture, Japan is the third strain of the proposed new species East Asian Passiflora virus (EAPV) phylogenetically distinguished from strains of Passion fruit woodiness virus. Archives of Virology, 151, 811–818.

    Article  CAS  PubMed  Google Scholar 

  • Juhász, A. C. P., Silva, D. J. H., Zerbini Júnior, F. M., et al. (2008). Base genética da resistência de um acesso de tomate silvestre ao mosaico-amarelo do pimentão. Pesquisa Agropecuária Brasileira, 43(6), 713–720.

    Article  Google Scholar 

  • Junqueira, N. T. V., Anjos, J. R. N., Silva, A. P. O., Chaves, R. C., & Gomes, A. C. (2003). Reação as doenças e produtividade de onze cultivares de maracujá-azedo cultivados sem agrotóxicos. Pesquisa Agropecuária Brasileira Brasília, 38(8), 1005–1010.

    Article  Google Scholar 

  • Junqueira, N. T. V., Braga, M. F., Faleiro, F. G., Peixoto, J. R., & Bernacci, L. C. (2005). Potencial de espécies silvestres de maracujazeiro como fonte de resistência a doenças. In F. G. Faleiro, N. T. V. Junqueira, & M. F. Braga (Eds.), Maracujá : Germoplasma e melhoramento genético (pp. 81–108). Embrapa Cerrados: Planaltina.

    Google Scholar 

  • Kitajima, E. W., Chagas, C. W., & Crestani, O. A. (1986). Enfermidades de etiologia viral e associadas a organismos do tipo micoplasma em maracujazeiro no Brasil. Fitopatologia Brasileira Brasília, 11(5), 409–432.

    Google Scholar 

  • Leão, R. M. K., Peixoto, J. R., Junqueira, N. T. V., Rezende, R. O., Mattos, J. K. A., & Melo, B. (2006). Reação de progênies de maracujazeiro-azedo ao vírus do endurecimento do fruto (Cowpea aphid-borne mosaic vírus – CABMV) em casa de vegetação. Bioescience Journal Uberlândia, 22(2), 87–92.

    Google Scholar 

  • Maciel, C., Nakano, D. H., Alberto, J., et al. (2009). Screening of Passiflora species for reaction to Cowpea aphid-borne mosaic virus reveals an immune wild species. Scientia Agricola, 66(3), 414–418.

    Article  CAS  Google Scholar 

  • Meletti, L. M. M. (2011). Avanços na cultura do maracujá no Brasil. Revista Brasileira de Fruticultura. Jaboticabal, Especial, E. 083–091.

  • Nascimento, A. V. S., Souza, A. R. R., Alfenas, P. F., Andrade, G. P., Carvalho, M. G., Pio-Ribeiro, G., et al. (2004). Análise filogenética do Potyvirus causando endurecimento dos frutos do maracujazeiro no Nordeste do Brasil. Fitopatologia Brasileira, 29, 378–383.

    Article  Google Scholar 

  • Nascimento, A. V. S., Santana, E. M., Braz, A. S. K., Alfenas, P. F., Pio-Ribeiro, G., Andrade, G. P., et al. (2006). Cowpea aphid borne mosaic virus (CABMV) is widespread in passion fruit Brazil and causes passion fruit woodiness disease. Archives of Virology, 151, 1797–1809.

    Article  CAS  PubMed  Google Scholar 

  • Nicolini, C., Rabelo Filho, F. A. C., Resende, R. O., Andrade, G. P., Kitajima, E. W., Pio-Ribeiro, G., & Nagata, T. (2012). Possible host adaptation as an evolution factor of Cowpea aphid-borne mosaic virus deduced by coat protein gene analysis. Journal of Phytopathology, 160, 82–87.

    Article  Google Scholar 

  • Novaes, Q. S., & Rezende, J. A. M. (1999). Possível aplicação do DAS-ELISA indireto na seleção de maracujazeiro tolerante ao ‘Passion fruit Woodiness Virus’. Fitopatologia Brasileira, 24, 76–79.

    Google Scholar 

  • Novaes, Q. S., & Rezende, J. A. M. (2003). Selected mild strains of passion fruit woodiness virus (PWV) fail to protect pre-immunized vines in Brazil. Scientia Agricola, 60, 699–708.

    Article  Google Scholar 

  • Ochwo-Ssemakula, M., Sengooba, T., Hakiza, J. J., Adipala, E., Edema, R., Redinbaugh, M. G., et al. (2012). Characterization and distribution of a Potyvirus associated with passion fruit woodiness disease in Uganda. Plant Disease, 96, 659–665.

    Article  Google Scholar 

  • Oliveira, E. J., Soares, T. L., Barbosa, C. J., Santos-Filho, H. P., & Jesus, O. N. (2013). Disease severity from passion fruit to identify sources of resistance in field conditions. Revista Brasileira de Fruticultura, 35, 485–492.

    Article  Google Scholar 

  • Pinto, P. H. D., Peixoto, J. R., Junqueira, N. T. V., Resende, R. O., Mattos, J. K. A., & Melo, B. (2008). Reação de genótipos de maracujazeiro-azedo ao vírus do endurecimento do fruto (Cowpea aphid-borne mosaic virus – CABMV). Bioscience Journal Uberlândia, 24(2), 19–26.

    Google Scholar 

  • Prins, M., Laimer, M., Noris, E., Schubert, J., & Tepfer, M. (2008). Strategies for antiviral resistance in transgenic plants. Molecular Plant Pathology, 9, 73–83.

    CAS  PubMed  Google Scholar 

  • Resende, R. M. S., Casler, M. D., & Resende, M. D. V. (2013). Selection methods in forage breeding: a quantitative appraisal. Crop Science, 53(5), 1925–1936.

    Article  Google Scholar 

  • Rodrigues, L. K., Silva, L. A., Garcêz, R. M., Chaves, A. L. R., Duarte, L. M. L., Giampani, J. S., Colariccio, A., Harakava, R., & Eiras, M. (2015). Phylogeny and recombination analysis of Brazilian yellow passion fruit isolates of Cowpea aphid-borne mosaic virus: origin and relationship with hosts. Australasian Plant Pathology, 44, 31–41.

    Article  Google Scholar 

  • Sacoman, N. N. (2013). Conservação de germoplasma in vitro e identificação de genótipos de Passiflora setacea resistentes ao Cowpea aphid-borne mosaic virus, Dissertação (Genetics and Plant Breeding) – Campos dos Goytacazes – RJ. Universidade Estadual do Norte Fluminense Darcy Ribeiro.

  • Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular Cloning (2nd ed.). New York: Cold Spring Harbor Press.

    Google Scholar 

  • Sampaio, A. C., Scudeller, N., Fumis, T. F., Almeida, A. M., Pinotti, R. N., Garcia, M. J. M., & Pallamin, M. L. (2008). Manejo cultural do maracujazeiro-amarelo em ciclo anual visando à convivência com o vírus do endurecimento dos frutos: um estudo de caso. Revista Brasileira de Fruticultura Jaboticabal - SP, 30(2), 343–347.

    Article  Google Scholar 

  • Silva, L. A. (2012). Cowpea aphid-borne mosaic virus na cultura do maracujazeiro: avaliação da tolerância de acessos avançados e efeito nutricional . Dissertação (Sanidade, Segurança Alimentar e Ambiental no Agronegócio) - São Paulo - SP, Instituto Biológico, 76p.

  • Trevisan, F., & Mendes, B. M. J. (2006). Resistance to Passion fruit woodiness virus in transgenic passionflower expressing the virus coat protein gene. Plant Disease, 90(8), 1026–1030.

    Article  CAS  Google Scholar 

  • Trindade, D. R., Poltronieri, L. S., Albuquerque, F. C., Rezende, J. A. M., Novaes, Q. S. D., & Kimati, H. (1999). Ocorrência do Passion fruit woodiness vírus (PWV) em maracujazais do Estado do Pará. Fitopatologia Brasileira, 24, 76–79.

    Google Scholar 

  • Vida, J. B., Zambolim, L., Tessmann, D. J., et al. (2004). Manejo de Doenças de Plantas em Cultivo Protegido. Fitopatologia Brasileira, 29(4), 355–372.

    Article  Google Scholar 

  • Wylie, S. J., & Jones, M. G. (2011). The complete genome sequence of a passion fruit woodiness virus isolate from Australia determined using deep sequencing, and its relationship to other potyviruses. Archives of Virology, 156, 479–482.

    Article  CAS  PubMed  Google Scholar 

  • Yamashiro, T., Chagas, C. M. (1979). Ocorrência de grave moléstia virótica em maracujá amarelo no Estado da Bahia. Anais do 5° Congresso Brasileiro de Fruticultura, Sociedade Brasileira de Fruticultura, Pelotas - RS, 915–917.

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Acknowledgments

The authors are thankful to the Graduate Program in Genetics and Plant Breeding and the Coordination of Improvement of Higher Education Personnel (CAPES) for the scholarship of the first author; to the Foundation for Research Support of the State of Rio de Janeiro (FAPERJ), the National Council for Scientific and Technological Development (CNPq) and the Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF) for their financial support to this research; to Dr. Margarete Magalhães de Souza for providing genotypes of P. setacea and the greenhouse to perform the crossovers (Universidade Estadual de Santa Cruz - BA, Brazil). APV, RR and ME are supported by a CNPq research fellowship.

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Santos, E.A., Viana, A.P., de Oliveira Freitas, J.C. et al. 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. Eur J Plant Pathol 143, 85–98 (2015). https://doi.org/10.1007/s10658-015-0667-y

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