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Mycelial Compatibility in Amylostereum Areolatum

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Mycelial Compatibility in Amylostereum Areolatum Mycelial compatibility in Amylostereum areolatum Magrieta Aletta van der Nest © University of Pretoria © University of Pretoria Mycelial compatibility in Amylostereum areolatum by Magrieta Aletta van der Nest Promotor: Prof. B.D. Wingfield Co-promotor: Prof. M.J. Wingfield Prof. B. Slippers Prof. J. Stenlid Submitted in partial fulfilment of the requirements for the degree of Philosophiae Doctor in the Faculty of Natural and Agricultural Sciences, Department of Genetics at the University of Pretoria. September 2010 © University of Pretoria DECLARATION I, Magrieta Aletta van der Nest, declare that this thesis, which I hereby submit for the degree Philosophiae Doctor at the University of Pretoria, is my own work and has not been submitted by me at this or any other tertiary institution. SIGNATURE: DATE: © University of Pretoria TABLE OF CONTENTS ACKNOWLEDGEMENTS ................................................................................................... i PREFACE ............................................................................................................................... ii CHAPTER 1 ........................................................................................................................... 1 LITERATURE REVIEW: The molecular basis of vegetative incompatibility in fungi, with specific reference to Basidiomycetes CHAPTER 2 ......................................................................................................................... 44 Genetics of Amylostereum species associated with Siricidae woodwasps CHAPTER 3 ......................................................................................................................... 61 Characterization of the systems governing sexual and self-recognition in the white rot homobasidiomycete Amylostereum areolatum CHAPTER 4 ......................................................................................................................... 101 Genetic linkage map for Amylostereum areolatum reveals an association between vegetative growth and sexual and self recognition CHAPTER 5 ......................................................................................................................... 137 Influence of symbiosis on the evolution and mode of reproduction of two white rot fungi CHAPTER 6 .................................................................................................................................... 184 Gene expression associated with vegetative incompatibility in Amylostereum areolatum SUMMARY ........................................................................................................................ 244 © University of Pretoria Acknowledgments I want to thank the following people and institutions: My study leaders Professors Brenda Wingfield, Mike Wingfield, Bernard Slippers and Jan Stenlid for their encouragement, guidance and patience. My mother (Trisce Jane van der Nest), my grandparents (Grieta and Lambert van der Nest), Emma Steenkamp, Tuan Duong, Karlien van Zyl and Markus Wilken for their help and support. The Fabians for their advice, help and support, especially the people in the Shaw laboratory. FABI support staff Helen Doman, Eva Muller, Jenny Hale, Rose Louw and Martha Mahlangu, Valentina Nkosi, Maretha van der Merwe and Lydia Twala, as well as the staff at the DNA sequence facility Renate Zipfel and Gladys Mthembu for technical assistance. The National Research Foundation (NRF), members of the Tree Protection Co- operative Programme (TPCP) and the THRIP initiative of the Department of Trade and Industry (DTI), South Africa for financial support. The Department of Genetics at the University of Pretoria for the use of their facilities. i © University of Pretoria Preface Amylostereum areolatum is a basidiomycete fungus that lives in symbiotic relationship with Siricid woodwasps. Like other fungi, A. areolatum utilizes a range of mechanisms to recognize individuals of its own and other species. Our current knowledge of the processes underlying these recognition mechanisms are based almost exclusively on the recognition systems of the model fungi. Even less is known for the recognition systems of fungi involved in symbiotic relationships with other eukaryotes and specifically insects. The research in this thesis focuses specifically on interactions among A. areolatum individuals, as well as how its biology and evolution could have been influenced by the association of woodwasps. The thesis is presented as six chapters, each of which is written as independent units (two of which have already been published). Thus there has been some obvious repetition of certain aspects among the chapters. Two independent systems regulate interactions among A. areolatum individuals. The one system (referred to as sexual compatibility) regulates mycelial compatibility between homokaryons and is controlled by the genes encoded at the mating type (mat) loci, while the second system (referred to as vegetative compatibility) regulates mycelial compatibility between heterokaryons and is controlled by the genes encoded at the heterokaryon incompatibility (het) loci. Sexual recognition in fungi has been well-studied and is thoroughly documented in the literature. The existing literature also addresses specific key issues regarding sexual recognition, including literature about the origins and evolution of the mat genes and molecular processes involved in sexual recognition. Although good reviews regarding fungal vegetative compatibility are available, the current literature has a gap regarding the processes and pathways involved in vegetative incompatibility. The first chapter of this thesis, therefore, presents a critical review of literature on the molecular mechanisms underlying vegetative incompatibility in fungi. The focus is on Basidiomycetes and a discussion of the possible processes and pathways associated with this phenomenon is included. The second chapter of this thesis provides a brief review on the research that has broadened our knowledge regarding the phylogenetics, population genetics and biology of Amylostereum spp. and in particular A. areolatum. Much of the existing literature on these issues was generated due the fact that A. areolatum and its symbiont, the Sirex noctilio woodwasp, threaten pine forestry in countries where they have been introduced. Despite ii © University of Pretoria considerable efforts to control the wasp, the Amylostereum-Sirex complex continues to kill significant numbers of trees. In this chapter, research that increased our understanding of the biology of Amylostereum spp., as well as their taxonomy and evolution, are considered. The diversity of these fungi and their interactions with the wasp and host plant are also discussed. Characterization of the sexual mating systems of Basidiomycetes has almost exclusively been limited to the model fungi. Almost no information is available about the het genes of Basidiomycetes. The aim of Chapter 3 of the thesis was, therefore, to characterize the mat and het loci in the non-model homobasidiomycete A. areolatum. We were able to determine the number of het loci in A. areolatum, as well as obtain portions of a putative pheromone receptor encoded at the mat-B locus and a gene (mitochondrial intermediate peptidase) linked to the mat-A locus of this fungus. Findings from this chapter provided some insight into the structure, organization, function and evolution of the recognition loci in Basidiomycetes, as well as the role these loci play in the development and evolution of these and other fungi. Genetic linkage maps have been used to study the recognition loci of eukaryotes. In a similar way, the aim of Chapter 4 of this thesis was to position the recognition loci (mat and het) of A. areolatum on a genetic linkage map. For this purpose amplified fragment length polymorphisms (AFLPs) were used for map construction, and AFLP-based bulked segregant analysis (BSA) was used to identify markers closely linked to the recognition loci. As has been shown previously for other eukaryotes, the recognition loci of A. areolatum are subject to evolutionary forces that are markedly different from those acting on the rest of the genome. The findings were analysed in terms of the in vitro growth rate of the fungus, which showed a possible association between the recognition loci and the genes involved in fitness. A possible explanation for the association between fitness and the recognition loci could be attributed to the evolutionary forces acting on these loci that keep them highly diverse. The aim of the study presented in Chapter 5 was to explore the evolutionary forces acting on the genes governing sexual recognition in A. areolatum. For this purpose, DNA sequence information was obtained from the pheromone receptor gene (RAB1) encoded at the mat-B locus and two nuclear regions (i.e. the eukaryotic translation elongation factor 1α gene and the ribosomal RNA internal transcribed spacer region). For comparative purposes, A. chailletii was included in this study. The findings suggest that balancing selection, but not positive selection, is keeping the mat genes of these fungi diverse. The aim of the study presented in Chapter 6 was to increase our understanding of the molecular mechanisms underlying vegetative incompatibility in A. areolatum. For this purpose, genes selectively expressed during incompatibility were identified using suppression iii © University of Pretoria subtractive hybridization, 454-based pyrosequencing and quantitative
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