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The Evolution of Necrotrophic Parasitism in the Sclerotiniaceae

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The Evolution of Necrotrophic Parasitism in the Sclerotiniaceae THE EVOLUTION OF NECROTROPHIC PARASITISM IN THE SCLEROTINIACEAE by Marion Andrew A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto © Copyright by Marion Andrew 2011 THE EVOLUTION OF NECROTROPHIC PARASITISM IN THE SCLEROTINIACEAE Marion Andrew Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto 2011 ABSTRACT Given a shared toolbox of pathogenicity-related genes among a set of species, why is one species a biotroph and specialist while another is a necrotroph and generalist? Is it the result of selection on primary sequence, or on proteins, or alternatively, differences in the timing and magnitude of gene expression? The Sclerotiniaceae (Ascomycota, Leotiomycetes, Helotiales) is a relatively recently evolved family of fungi whose members include host generalists and host specialists, and the spectrum of trophic types. Based on a phylogeny inferred from three, presumably evolutionarily conserved housekeeping genes, the common ancestor of the Sclerotiniaceae was necrotrophic, with at least two shifts from necrotrophy to biotrophy. Phylogenies inferred from eight pathogenicity-related genes, involved in cell wall degradation and the oxalic acid pathway, were incongruent with the presumably neutral phylogeny. Site-specific likelihood analyses, which estimate the rate of nonsynonymous to synonymous substitutions (dN/dS), showed evidence for purifying selection acting on all pathogenicity- related genes, and positive selection on sites within five of eight genes. Rate-specific likelihood analyses showed no differences in dN/dS rates between necrotrophs and biotrophs, and between host generalists and host specialists, indicating that selection acting on the genes does not drive divergence toward changes in trophic type or host association. In vitro screens for oxalic acid production demonstrated that all necrotrophic generalists produce oxalic acid by 72 hours, while production was either absent or ii delayed among biotrophs and host specialists. This pattern was also observed during the course of Arabidopsis thaliana infection, in which large spikes of expression were seen in the oxalic acid pathway-related gene, oah, within eight hours of inoculation among necrotrophic generalists only. Results suggest that necrotrophic generalists can be distinguished from biotrophs and host specialists in the Sclerotiniaceae by the ability to produce abundant amounts of oxalic acid early in infection and to cause large proliferating lesions on A. thaliana. iii ACKNOWLEDGMENTS I would like to thank my advisor, Linda Kohn, for encouraging me to see beyond pattern and towards process. This has been tremendous helpful in seeing the big questions, and has allowed me to explore the biology and genomics of fungi with hypotheses-driven research. I would like to acknowledge my committee members who have always been helpful and supportive. I thank Jim Anderson for his enthusiasm and creativity about science. Thank you to Nick Provart for his advice and support, and for always having an open door policy. I thank Keiko Yoshioka for her encouragement and insight, especially when thinking about the photosynthetic partner of the host-pathogen conflict. Thank you to Steve Short for all the time spent in your lab, and all the time spent in your office, troubleshooting qPCR – your advice has been invaluable and your help will always be appreciated. This project would not have been possible without some excellent assistance. I would like to acknowledge all the help and patience that Cindy Short provided in helping me battle qPCR. Reeta Barua has made significant contributions to this project, and in performing virulence tests and indicator plate assays she really took it upon herself to understand my project as a whole so she could help with troubleshooting. I would like to also thank my current and former lab mates in the Kohn lab and the Anderson lab who always answered my innumerable questions, and made the lab such great environment for science – especially Megan Saunders, Lucas Parreiras, Jeremy Dettman and Caroline Sirjusingh. There have been a number of people at University of Toronto that I would like to recognize for guidance. Jean-Marc Moncalvo has provided insightful comments and helped shaped my research project. Peter Kotanen has provided his expertise in statistics, for which I am incredibly grateful. Sa!a Stefanovi" has allowed me to use his lab, and has always asked intellectually stimulating questions. Heath O’Brien and Stephanie Diezmann have provided immense support and encouragement, and even some lively debates. Thomas Braukmann and Anuar Rodrigues are my rocks, with whom I have had countless discussions and endless cups of tea. iv I would like to acknowledge the Ontario Graduate Scholarship for funding during my degree. I have also received travel funds from the Mycological Society of America, the Genetics Society of America, and the EEB department. Last, I would like to thank all my friends and family, for without your help this would not be possible. Special thanks to my parents for showing me the trials and tribulations of academia first hand, while always emphasizing the need to love and be passionate about your work. And finally to Jon, my constant source of encouragement, patience and support – words will never be enough to thank you for everything you have given me. v TABLE OF CONTENTS ABSTRACT ii ACKNOWLEDGEMENTS iv TABLE OF CONTENTS v LIST OF TABLES viii LIST OF FIGURES x LIST OF APPENDICES xii CHAPTER 1. GENERAL INTRODUCTION 1 1. Glossary of terms. 2 2. Thesis overview. 3 3. Plant-pathogen interactions. 5 3.1. PAMP-triggered immunity. 6 3.2. Effector-triggered immunity. 8 3.3. Detecting selection in pathogenicity-related genes. 9 3.4. Strategies for biotrophic versus necrotrophic infection. 14 4. Comparative fungal genomics. 18 4.1. Determining differences among genomes of biotrophs and necrotrophs. 18 4.2. The genomic organization of virulence genes – gene clustering and implications for horizontal gene transfer and the evolution of virulence. 24 5. Sclerotiniaceae as a model system for studying interactions between trophic types and host associations. 26 6. Candidate pathogenicity-related genes for studies of the Sclerotiniaceae. 30 7. Objectives of thesis. 32 CHAPTER 2. NECROTROPHIC, HOST-GENERALIST SPECIES IN THE SCLEROTINIACEAE ARE CHARACTERIZED BY EARLY, ABUNDANT OXALIC ACID PRODUCTION DURING PLANT INFECTION 35 vi 1. Abstract. 36 2. Introduction. 37 3. Materials and Methods. 41 3.1. Strains used in this study. 41 3.2. Fungal cultures and DNA extraction. 44 3.3. PCR and sequencing. 44 3.4. DNA sequence alignments and phylogenetic analyses. 47 3.5. General method of screening for positive selection using PAML. 48 3.6. Detection of positive-selection: site-specific selection analyses. 49 3.7. Detection of positive-selection: rate-specific selection analyses across lineages. 49 3.8. Virulence testing. 49 3.9. In vitro indicator bromophenol blue plate screening for oxalic acid. 50 3.10. In planta oxalic acid pathway-related gene expression assay. 50 4. Results. 53 4.1. At least two origins of biotrophy from a necrotrophic ancestor in the Sclerotiniaceae. 53 4.2. Conflict between pathogenicity-related gene trees and the phylogeny inferred from housekeeping genes. 53 4.3. Site-specific likelihood analyses show evidence for purifying selection acting on all pathogenicity-related genes, and positive selection on sites within 5 of 8 genes. 55 4.4. Rate-specific likelihood analyses show no differences in rates of selection between necrotrophs and biotrophs, and host generalists and host specialists. 55 4.5. Necrotrophic generalists caused early lesion formation and expansion on detached A. thaliana leaves, while host specialists and biotrophs either failed to produce disease lesions, or formed smaller lesions later in the infection process. 62 4.6. Screened for constitutive acid production on indicator plates, most strains produced oxalic acid but differed in the timing. 62 4.7. oah and pac1 express constitutively but modulation in magnitude and timing is induced. 64 5. Discussion. 64 vii CHAPTER 3. SUMMARY 78 LITERATURE CITED 86 APPENDIX A 118 viii LIST OF TABLES TABLE 2.1. Host and origin of isolates examined in this study. 42-43 TABLE 2.2. Primer sets for amplification of housekeeping and pathogenicity-related genes in the Sclerotiniaceae. 45 TABLE 2.3. Amplification methods and parameters used for phylogenetic analyses of housekeeping and pathogenicity-related loci. 46 TABLE 2.4. Primer/probe sets for quantitative PCR of two pathogenicity-related loci (oah and pac1) and the reference gene (actin). 52 TABLE 2.5. Site-specific likelihood analyses for eight pathogenicity-related genes and two housekeeping genes. 56 TABLE 2.6. Site-specific likelihood analyses: Log likelihood (lnL) values, number of parameters (np), and parameter estimates for eight pathogenicity-related genes and two housekeeping genes. 57-59 TABLE 2.7. Rate-specific likelihood analyses for lineage-specific comparisons. 60 TABLE 2.8. Rate-specific likelihood analyses: Log likelihood (lnL) values, number of parameters (np), and parameter estimates for six pathogenicity-related genes and two housekeeping genes. 61 TABLE 2.9. Relative virulence of fungal isolates on detached Arabidopsis thaliana leaves. 63 ix TABLE A.1. Isolates and hybridization results for all SNP-based oligonucleotide probes. 124-126 TABLE A.2. Primer
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