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(Theobroma Cacao L.) Fungus Moniliophthora Roreri (Cif.) Evans Et Al

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(Theobroma Cacao L.) Fungus Moniliophthora Roreri (Cif.) Evans Et Al Origin, biogeography, genetic diversity and taxonomic affinities of the cacao (Theobroma cacao L.) fungus Moniliophthora roreri (Cif.) Evans et al. as determined using molecular, phytopathological and morpho-physiological evidence A thesis submitted by Wilbert Phillips-Mora for the degree of Doctor of Philosophy May, 2003 Department of Agricultural Botany, School of Plant Sciences, The University of Reading, RG6 6AS, UK i ABSTRACT The origin, genetic diversity, biogeography and taxonomic affinities of the neotropical cacao pathogen M. roreri were studied through the application of various molecular, morpho-physiological and phytopathological methodologies to 96 isolates collected from throughout its geographic range. AFLP, ISSR and ITS sequence analyses revealed that this fungus has a considerable genetic variation, although regions of comparative genetic uniformity were also identified in Central America, central Ecuador and Peru. The highest variability was observed in north-eastern Colombia indicating that this region represents the centre of diversity for the fungus. The pattern of declining variability outside this area also suggests that M. roreri originated in this country, possibly within or close to the Medium Magdalena. Five major subspecific groupings were identified, with each exhibiting a characteristic distribution: Bolívar and Co-West groups being widespread, whereas Co-Central and Co-East groups apparently endemic to Colombia and the Gileri group being restricted to Ecuador. ITS was useful to define two subspecific groups and to reinforce some of the AFLP/ISSR findings. The morpho-physiological variation of 88 isolates and the effect of three in vitro temperature regimes were studied by evaluating eleven variables for which significant divergence was noted. Significant differences were observed between genetic groups for most variables, suggesting the variability may have a genetic basis. The virulence of seven Colombian isolates representing four genetic groups was determined by artificially inoculating pods of five cacao clones in Colombia. Genetic variation detected between isolates was not matched by similar diversity in their virulence. There was apparently only limited variation in virulence between them. Phylogenetic analysis of three different portions of the M. roreri genome (ITS regions, nLSU-rDNA, mtSSU-rDNA) confirmed that this fungus is a Basidiomycete and strongly suggest that it belongs to the order Agaricales, possibly belonging to the family Tricholomataceae. Sequences analysis also demonstrated that M. roreri is closely related to the witches’ broom pathogen of cacao Crinipellis perniciosa. ii ACKNOWLEDGEMENTS This thesis was kindly financed by the Department of Agriculture of the United States (USDA) and supported by the Tropical Agricultural Research and Higher Education Centre (CATIE, Costa Rica), CABI Bioscience (UK) and the University of Reading. I would like to express my sincere gratitude to the administrative, technical, academic and field personnel of these institutions for all their assistance. I wish to express special thanks to Dr Eric Rosenquist (USDA), to my institution (CATIE) and to its current and former Directors General Drs. Pedro Ferreira and Rubén Guevara for their permanent support. I am greatly indebted to my supervisor Dr. Mike Wilkinson for his enthusiasm, advice and critical revision of this manuscript, and to Drs Ulrike Krauss and Harry Evans from CABI for their support and revision of some chapters. A special recognition to the following persons for their invaluable and unconditional collaboration: José Castillo, Carlos Astorga, Allan Meneses, Tony Alfaro and Karol Alpízar (CATIE); Moy Robson and George Gibbings (the University of Reading); Dr. Julie Flood (CABI), Jesús Sánchez (FHIA, Honduras); Dr. María Chacón and Ricardo Castillo (Colombia); Sergio Cadavid (Compañía Nacional de Chocolates, Medellín); Carlos Ruales (Nestlé, Ecuador); Dr. Victor Merchán (ICA, Colombia); Dr. Carmen Suárez (INIAP, Ecuador); Dr. Pablo Buritica (Universidad Nacional, Medellín); Sergio Cedeño (Industrial y Agrícola Cañas S.A., Ecuador) and Dr. Juan Carlos Motamayor (MARS/USDA). Many thanks also to Gustavo López and Drs. Gilberto Paéz and Julio Di Rienzo for their help with data analysis. I wish to express my sincere gratitude to the following persons: From the Colombian Corporation for Agricultural and Livestock Research (CORPOICA): Eleonora Rodríguez, Luis Mejía, Orlando Argüello, Gabriel Cubillos, Jairo Alvarado, Jaime Morales, Nelson Díaz, Orlando Guiza, Jesús Toloza, Danny Williams, Guillermo Pico, Hernando Castro and Guillermo Jaimez. iii In Ecuador: Esteban Quirola, Julio Moreno, Fernando Crespo, Karina Solis, Dennis Durango, Grisnel Quijano, Tatiana and Hans Beltrán. In England: Dr. María Albani, Dr. Julie Hawkins, Caroline Ford, Dr. Joel Allainguillaume, Vivien Smith, June Randall, Pauline Harvey, John Cook and Fiona Brown from the School of Plant Sciences (the Reading University); Dr. Allan Buddie, Sally George, Thelma Caine, Cristina West and Iratxe Rodríguez from CABI; Dr. Tony Lass (Cadbury) and Dr. Paul Bridge (Kew Gardens). To the López and Richardson families and to Conchita for their friendship and support. In Nicaragua: Hans Griebe (Promundo Humano), Xavier Escorcia, Ana Rosa Cruz, Rudolf Sollanek and Gerardo Gutiérrez. In Panama: Luis Mejía, Zuleyka Maynard and Enith Rojas from the Smithsonian Institute and Gumercindo Añino from MIDA. In Venezuela: Dr. Maria Marcano, Alexander Vieto and José Gerardo Albarrán from the Universidad de los Andes, Mérida. In Costa Rica: Abel Chacón, William Araya, Maritza Loaiza, Dr. Francisco Jiménez, Sergio Velásquez, Dr. Elizabeth Johnson, my co-workers and friends, in particular to the families Mesén Blanco, Furcal Morera, Garro Flores, Navarro Fumero, Royo Vàsquez and Rodríguez Vargas. Finally, I am deeply grateful to my family, my wife Irma, my children Kevin and Erick, my mom Elsa, my dad Mario, my mother-in-law Nelly and my brothers and sisters for their love, understanding and constant support. This thesis is dedicated to the memory of my brother Mario Ricardo and my nephews Miguel Angel and Edgar Alonso. “Now to the King eternal, immortal, invisible, to God who alone is wise, be honour and glory forever and ever. Amen.” 1 Timothy 1:17 iv CONTENTS ABSTRACT ...................................................................................................... i ACKNOWLEDGEMENTS ............................................................................. ii CONTENTS ...................................................................................................... iv LIST OF TABLES ............................................................................................ xvi LIST OF FIGURES .......................................................................................... xx LIST OF PLATES ............................................................................................ xxiii CHAPTER 1 General Introduction 1.1 INTRODUCTION ....................................................................................... 1 1.2 RESEARCH OBJECTIVES ........................................................................ 2 1.2.1 GENERAL OBJECTIVES .................................................................. 2 1.2.2 SPECIFIC OBJECTIVES .................................................................... 2 1.3 GENERAL FEATURES OF THE FUNGUS AND THE DISEASE ......... 3 1.3.1 HOST RANGE .................................................................................... 3 1.3.2 THE FUNGUS ..................................................................................... 5 1.3.2.1 Etiology and taxonomy ................................................................ 5 1.3.2.2 Dispersal of M. roreri .................................................................. 7 1.3.2.2.1 Sources of inoculum ........................................................ 7 1.3.2.2.2 Mechanisms of dispersal ................................................. 8 1.3.2.2.2.1 Dispersal by wind ................................................ 8 1.3.2.2.2.2 Dispersal by human beings ................................. 9 1.3.2.2.2.3 Dispersal by insects and other animals ............... 10 1.3.2.2.2.4 Dispersal by water ............................................... 10 1.3.3 THE DISEASE .................................................................................... 11 1.3.3.1 Historical development and current economic importance .......... 11 1.3.3.2 Common names ............................................................................ 11 1.3.3.3 Disease symptoms ........................................................................ 12 v 1.4 FUNGAL DIVERSITY AND SYSTEMATICS ......................................... 15 1.4.1 GENETIC DIVERSITY IN FUNGI .................................................... 15 1.4.2 ANALYSIS OF FUNGAL GENETIC DIVERSITY .......................... 17 1.4.3 FUNGAL PHYLOGENETICS ........................................................... 18 1.5 MOLECULAR TECHNIQUES USED FOR GENETIC ANALYSIS OF FUNGI ...................................................................................................... 20 1.5.1 AFLP ANALYSIS ............................................................................... 20 1.5.1.1 General considerations ................................................................. 20 1.5.1.2 Description of AFLP analysis ...................................................... 21 1.5.1.3 AFLP
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