Molecular Phylogeny and Population Genetics of Microcyclus Ulei, Causal Agent of the South American Leaf Blight of Hevea Brasiliensis

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Molecular Phylogeny and Population Genetics of Microcyclus Ulei, Causal Agent of the South American Leaf Blight of Hevea Brasiliensis BRAZ TAVARES DA HORA JÚNIOR Molecular phylogeny and population genetics of Microcyclus ulei, causal agent of the South American leaf blight of Hevea brasiliensis Tese apresentada à Universidade Federal de Viçosa, como parte das exigências do Programa de Pós-Graduação em Fitopatologia, para obtenção do título de Doctor Scientiae. VIÇOSA MINAS GERAIS – BRASIL 2012 Aos meus pais, Braz Tavares e Liana Maria, e ao meu filho Vitor da Hora, dedico. ii AGRADECIMENTOS Ao Prof. Dr. Eduardo Seiti Gomide Mizubuti, meu orientador, pela oportunidade, confiança e amizade. Aos pesquisadores da Michelin, Carlos Raimundo Reis Mattos e Eric Cavaloc pela oportunidade, confiança e amizade. Aos pesquisadores do Cirad, em especial ao Dr. Dominique Garcia, Vincent Le Guen e Frank Rivano pelo apoio e amizade. Ao Prof. Dr. Robert Weingart Barreto e ao Dr. Harold Charles Evans, pela orientação e amizade. A Profa. Dra. Karla Suemy Clemente Yotoko, pelo apoio e amizade. Aos amigos das Plantações Michelin da Bahia pela amizade, pelos ensinamentos e pela colaboração nos trabalhos. Aos meus colegas e amigos do Laboratório de Biologia de Populações de Fitopatógenos, pela amizade, pelos ensinamentos e pelo convívio. Aos meus colegas e amigos do PPGFito/UFV, pela amizade, pelos ensinamentos e pelo convívio. Aos professores e técnicos do PPGFito/UFV, pelos ensinamentos e pela amizade. À Carine Rezende Cardoso pelo amor e incentivo. À minha família, em especial meus irmãos André e Diogo e minha sobrinha Letícia, Helenice e Vinícius, pela compreensão, amor e incentivo. À CAPES e ao CNPq, pela concessão da bolsa de estudo, e à Plantações Michelin da Bahia pelo apoio financeiro a este projeto. iii SUMÁRIO SUMÁRIO ............................................................................................................................... iii RESUMO ................................................................................................................................ vi ABSTRACT .......................................................................................................................... viii INTRODUÇÃO GERAL ...................................................................................................... 10 REFERENCES .................................................................................................................... 13 CAPÍTULO 1 ........................................................................................................................ 15 Unraveling critical characteristics of the life cycle of Microcyclus ulei, a highly destructive fungal pathogen of the rubber tree (Hevea brasiliensis) ....................... 15 ABSTRACT .......................................................................................................................... 16 INTRODUCTION ................................................................................................................. 18 MATERIAL AND METHODS ............................................................................................. 22 RESULTS ............................................................................................................................. 27 DISCUSSION ....................................................................................................................... 29 TAXONOMY ......................................................................................................................... 34 ACKNOWLEDGEMENTS .................................................................................................. 35 REFERENCES .................................................................................................................... 36 FIGURE LEGENDS ............................................................................................................ 49 SUPPORTING INFORMATION ........................................................................................ 58 CAPÍTULO 2 ........................................................................................................................ 69 Spatial pattern and population biology of Microcyclus ulei in Hevea agricultural landscapes in Brazil ........................................................................................................ 69 ABSTRACT .......................................................................................................................... 70 INTRODUCTION ................................................................................................................. 72 MATERIAL AND METHODS ............................................................................................. 76 RESULTS ............................................................................................................................. 80 DISCUSSION ....................................................................................................................... 83 ACKNOWLEDGEMENTS .................................................................................................. 89 iv REFERENCES .................................................................................................................... 90 FIGURE LEGENDS ............................................................................................................ 99 SUPPORTING INFORMATION ...................................................................................... 108 CAPÍTULO 3 ...................................................................................................................... 111 Influence of hosts with partial resistance on the genetic structure of the pathogen Microcyclus ulei in Hevea spp. .................................................................................... 111 ABSTRACT ........................................................................................................................ 112 INTRODUCTION ............................................................................................................... 114 MATERIAL AND METHODS ........................................................................................... 118 RESULTS ........................................................................................................................... 123 DISCUSSION ..................................................................................................................... 127 ACKNOWLEDGEMENTS ................................................................................................ 131 REFERENCES .................................................................................................................. 132 FIGURE LEGENDS .......................................................................................................... 141 SUPPORTING INFORMATION ...................................................................................... 151 CONCLUSÃO GERAL ...................................................................................................... 158 v RESUMO HORA JÚNIOR, Braz Tavares, D.Sc., Universidade Federal de Viçosa, Agosto de 2012. Filogenia molecular e genética de populações de Microcyclus ulei, agente causal do mal das folhas de Hevea brasiliensis. Orientador: Eduardo Seiti Gomide Mizubuti. Co- orientadores: Luiz Antonio Maffia e Robert Weingart Barreto. O mal das folhas da seringueira, doença causada pelo fungo Microcyclus ulei, impediu o desenvolvimento de Hevea spp. em áreas de monoculturas na região amazônica e, consequentemente, acarretou perdas na produção de borracha natural em sistemas agrícolas na América Tropical. O uso de clones de seringueira com resistência parcial ao mal das folhas é a melhor opção para o manejo da doença. Embora o mal das folhas seja conhecido desde o início do século 20, aspectos básicos da classificação filogenética e da estrutura genética da população do patógeno são desconhecidos. Quatro regiões genômicas (LSU rRNA, mtSSU, MCM7 e ITS) foram usadas em estudos de reconstrução filogenética que suportam a classificação de M. ulei na família Mycosphaerellaceae s. str., ordem Capnodiales, em Ascomycota, proximamente relacionado às espécies de Mycosphaerella. Da mesma forma o seu anamorfo Fusicladium heveae é melhor acomodado em Pseudocercospora s. str. A partir desta perspectiva evolutiva, propomos um modelo de ciclo de vida que inicia com espermogônias em folhas próximas à maturidade levando a ascósporos maduros em pseudotécios dentro dos estromas. A variabilidade genética do patógeno em plantações comerciais de seringueiras foi analisada em grande e pequena escalas, utilizando 17 locos microssatélites. Quinze populações locais da Amazônia e de regiões vi produtoras no Brasil foram analisadas em larga escala. Constatou-se alta diversidade gênica e associação aleatória de alelos. Algumas populações geograficamente distantes foram geneticamente relacionadas. Isolamento por distância foi evidente apenas para as populações da região amazônica. Os padrões espaciais da variação genética de M. ulei são o resultado de fluxo gênico, provavelmente, afetado por fatores antrópicos e deriva genética por falha de conectividade entre os seringais. O estudo em pequena escala foi feito para caracterizar a variabilidade intraespecífica da população do patógeno a partir de isolados coletados de clones de seringueira suscetíveis e resistentes. A análise bayesiana de agrupamento revelou agrupamento de isolados de acordo com o nível de resistência sugerindo que seleção desempenha um papel importante na evolução do M. ulei. Além disso,
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