Resistance to triazole fungicides in <i>Pyricularia</i> species associated with invasive plants from wheat fields in Brazil
Resumo
Triazole fungicides have not been effective for managing the wheat blast disease in Brazil. A broad analysis across six geographical populations of Pyricularia graminis-tritici in central-southern Brazil indicated a high level of resistance to triazole fungicides. Since P. graminis-tritici is also associated with others poaceous species, here, we analyzed whether triazole-resistant isolates of the blast pathogen could be recovered from other poaceous hosts that are invasive of sprayed wheat fields. In addition to P. graminis-tritici (Pygt), we also evaluated the levels of sensitivity of three other grass-associated blast pathogens, which included P. grisea (Pg), P. pennisetigena (Pp), and P. urashimae (Pu). Resistance to the triazole fungicides tebuconazole and epoxiconazole was assessed phenotypically based on EC50 values and molecularly by analysis of the presence of mutations in the CYP51A gene, which encodes for the target enzyme 14-alpha-demethylase. We detected triazole-resistant Pyricularia spp. (Pg, Pp, Pu and Pygt) that is associated with Avena sativa, Cenchrus echinatus, Chloris distichophylla, Cynodon sp., Digitaria horizontalis, D. sanguinalis, Panicum maximum or Urochloa spp. The major outcome from our study was the evidence that invasive poaceous species from wheat fields could be an important source of triazole resistant fungal inoculum for the initial phases of the wheat blast epidemics.
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Referências
Abou Ammar, G., Tryono, R., Doll, K., Karlovsky, P., Deising, H. B., & Wirsel, S. G. (2013). Identification of ABC transporter genes of Fusarium graminearum with roles in azole tolerance and/or virulence. PLoS ONE, 8(11), e79042. DOI: 10.1371/journal.pone.0079042
Brunner, P. C., Stefanato, F. L., & McDonald, B. A. (2008). Evolution of the CYP51 gene in Mycosphaerella graminicola: evidence for intragenic recombination and selective replacement. Molecular Plant Pathology, 9(3), 305-316. DOI: 10.1111/j.1364-3703.2007.00464.x
Buchenauer, H., & Hellwald, K. H. (1985). Resistance of Erysiphe graminis on barley and wheat to sterol C-14-demethylation inhibitors. EPPO Bulletin, 15(4), 459-466, DOI: 10.1111/j.1365-2338.1985.tb00255.x
Callaway, E. (2016). Devastating wheat fungus appears in Asia for first time. Nature, 532(7600), 421–422. DOI: 10.1038/532421a
Castroagudin, V. L., Ceresini, P. C., De Oliveira, S. C., Reges, J. T., Maciel, J. L., Bonato, A. L., ... McDonald, B. A. (2015). Resistance to QoI fungicides is widespread in Brazilian populations of the wheat blast pathogen Magnaporthe oryzae. Phytopathology, 105(3), 284-94. DOI: 10.1094/PHYTO-06-14-0184-R
Castroagudin, V. L., Moreira, S. I., Pereira, D. A. S., Moreira, S. S., Brunner, P. C., Maciel, J. L. N., … Ceresini, P. C. (2016). Pyricularia graminis-tritici, a new Pyricularia species causing wheat blast. Persoonia, 37(1), 199–216. DOI: 10.3767/003158516x692149
Ceresini, P. C., Castroagudín, V. L., Rodrigues, F. A., Rios, J. A., Aucique-Pérez, C. E., Moreira, S. I., ... Maciel, J. L. N. (2018). Wheat blast: past, present, and future. Annual Review of Phytopathology, 56(1), 20.1–20.30. DOI: 10.1146/annurev-phyto-080417-050036
Clement, M., Posada, D., & Crandall, K. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9(10), 1657-1660.
Coleman, J. J., & Mylonakis, E. (2009). Efflux in fungi: la piece de resistance. PLoS Pathogens, 5(6), e1000486. DOI: 10.1371/journal.ppat.1000486
Cools, H. J., & Fraaije, B. A. (2013). Update on mechanisms of azole resistance in Mycosphaerella graminicola and implications for future control. Pest Management Science, 69(2), 150-155. DOI: 10.1002/ps.3348
Crous, P. W., Wingfield, M. J., Burgess, T. I., Hardy, G. E., Crane, C., Barrett, S., …Groenewald, J. Z. (2016). Fungal Planet description sheets: 469-557. Persoonia, 37(1), 218-403. DOI: 10.3767/003158516X694499
Debona, D., Favera, D. D., Corte, G. D., Domingues, L. S., & Balardin, R. S. (2009). Controle químico da ferrugem da folha em cultivares de trigo submetidas a diferentes níveis de adubação nitrogenada. Revista da FZVA, 16(1), 52-65.
Deising, H. B., Reimann, S., & Pascholati, S. F. (2008). Mechanisms and significance of fungicide resistance. Brazilian Journal of Microbiology, 39(2), 286-295. DOI: 10.1590/S1517-838220080002000017
Fan, J., Urban, M., Parker, J. E., Brewer, H. C., Kelly, S. L., Hammond-Kosack, K. E., … Cools, H. J. (2013). Characterization of the sterol 14alpha-demethylases of Fusarium graminearum identifies a novel genus-specific CYP51 function. New Phytologist, 198(3), 821-35. DOI: 10.1111/nph.12193
Hawkins, N. J., Cools, H. J., Sierotzki, H., Shaw, M. W., Knogge, W., Kelly, S. L., ... Fraaije, B. A. (2014). Paralog re-emergence: a novel, historically contingent mechanism in the evolution of antimicrobial resistance. Molecular Biology and Evolution, 31(7), 1793-802. DOI: 10.1093/molbev/msu134
Igarashi, S. (1986). Ocorrência de Pyricularia spp. no estado do Paraná. Fitopatologia Brasileira, 11(2), 351-352.
Islam, M. T., Croll, D., Gladieux, P., Soanes, D. M., Persoons, A., Bhattacharjee, P., ... Kamoun, S. (2016). Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae. BMC Biology, 14(84), 1-11, DOI: 10.1186/s12915-016-0309-7
Jiang, J., Liu, X., Yin, Y., & Ma, Z. (2011). Involvement of a velvet protein FgVeA in the regulation of asexual development, lipid and secondary metabolisms and virulence in Fusarium graminearum. PLoS ONE, 6(11), e28291. DOI: 10.1371/journal.pone.0028291
Lucas, J. A., Hawkins, N. J., & Fraaije, B. A. (2015). The evolution of fungicide resistance. Advances in Applied Microbiology, 90, 29-92. DOI: 10.1016/bs.aambs.09.001
Ma, Z., Yoshimura, M. A., Holtz, B. A., & Michailides, T. J. (2005). Characterization and PCR-based detection of benzimidazole-resistant isolates of Monilinia laxa in California. Pest Management Science, 61(5), 449-457. DOI: 10.1002/ps.982
Maciel, J. L. N. (2011). Magnaporthe oryzae, the blast pathogen: current status and options for its control. Plant Science Review, 6(50), 233-240. DOI: 10.1079/PAVSNNR20116050
Maciel, J. L. N., Ceresini, P. C., Castroagudin, V. L., Zala, M., Kema, G. H., & McDonald, B. A. (2014).Population structure and pathotype diversity of the wheat blast pathogen Magnaporthe oryzae 25 years after its emergence in Brazil. Phytopathology, 104(1), 95-107. DOI: 10.1094/PHYTO-11-12-0294-R
Maciel, J. L. N., Paludo, E. A., Silva, M. S., Scheeren, P. L., & Caierão, E. (2008). Reação à brusone de genótipos de trigo do programa de melhoramento da Embrapa Trigo no estádio de planta adulta. Embrapa Trigo. Boletim de Pesquisa e Desenvolvimento Online, 64, 1-14.
Milgroom, M. G., & Fry, W. E. (1988). A simulation analysis of the epidemiological principles for fungicide resistance management in pathogen populations. Phytopathology, 78(5), 565-570.
Nakaune, R., Adachi, K., Nawata, O., Tomiyama, M., Akutsu, K., & Hibi, T. (1998). A novel ATP-binding cassette transporter involved in multidrug resistance in the phytopathogenic fungus Penicillium digitatum. Applied and Environmental Microbiology, 64(10), 3983–3988.
Navarini, L., & Balardin, R. S. (2012). Doenças foliares e o controle por fungicidas na produtividade e qualidade de grãos de trigo. Summa Phytopathologica, 38(4), 294-299. DOI: 10.1590/S0100-54052012000400004
Pagani, A. P., Dianese, A. C., & Café Filho, A. C. (2014). Management of wheat blast with synthetic fungicides, partial resistance and silicate and phosphite minerals. Phytoparasitica, 42(5), 609–617. DOI: 10.1007/s12600-014-0401-x
Pereira, D. A., McDonald, B. A., & Brunner, P. C. (2016). Mutations in the CYP51 gene reduce DMI sensitivity in Parastagonospora nodorum populations in Europe and China. Pest Management Science, 73(7), 1503-1510. DOI: 10.1002/ps.4486
R Development Core Team. (2011). R: A language and environment for statistical computing. Vienna, AU: R Foundation for Statistical Computing.
Reges, J. T. A., Negrisoli, M. M., Dorigan, A. F., Castroagudin, V. L., Maciel, J. L. N., & Ceresini, P. C. (2016). Pyricularia pennisetigena and P. zingibericola from invasive grasses infect signal grass, barley and wheat. Pesquisa Agropecuária Tropical, 46(2), 206-214. DOI: 10.1590/1983-40632016v4641335
Rozas, J. (2009). DNA sequence polymorphism analysis using DnaSP. Methods in Molecular Biology, 537, 337-350. DOI: 10.1007/978-1-59745-251-9_17
Snelders, E., Karawajczyk, A., Schaftenaar, G., Verweij, P. E., & Melchers, W. J. (2010). Azole resistance profile of amino acid changes in Aspergillus fumigatus CYP51A based on protein homology modeling. Antimicrobial Agents and Chemotherapy, 54(6), 2425-30. DOI: 10.1128/AAC.01599-09
Stammler, G., & Semar, M. (2011). Sensitivity of Mycosphaerella graminicola (anamorph: Septoria tritici) to DMI fungicides across Europe and impact on field performance. EPPO Bulletin, 41(2), 149–155. DOI: 10.1111/j.1365-2338.2011.02454.x
Tormen, N., Lenzii, G., Minuzzi, S., Uebel, J., Cezar, H. S., & Balardin, R. S. (2013). Reação de cultivares de trigo à ferrugem da folha e mancha amarela e responsividade a fungicidas. Ciência Rural, 43(2), 239-246. DOI: 10.1590/S0103-84782013000200008
Urashima, A. S., & Kato, H. (1998). Pathogenic relationship between isolates of Pyricularia grisea of wheat and other hosts at different host developmental stages. Fitopatologia Brasileira, 23(1), p. 30-35.
Vargas, M. H. (2000). ED50plus v1.0. Instituto Nacional de Enfermedades Respiratorias [Computer software]. Mexico, DF, Mexico.
Yan, X., Ma, W. B., Li, Y., Wang, H., Que, Y. W., Ma, Z. H., ... Wang, Z. Y. (2011). A sterol 14alpha-demethylase is required for conidiation, virulence and for mediating sensitivity to sterol demethylation inhibitors by the rice blast fungus Magnaporthe oryzae. Fungal Genetics and Biology, 48(2), 144-53. DOI: 10.1016/j.fgb.2010.09.005
Zhan, J., Stefanato, F. L., & McDonald, B. A. (2006). Selection for increased cyproconazole tolerance in Mycosphaerella graminicola through local adaptation and in response to host resistance. Molecular Plant Pathology, 7(4), 259-68. DOI: 10.1111/j.1364-3703.2006.00336.x
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