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TAXONOMY, SYSTEMATICS, ECOLOGY, AND EVOLUTIONARY BIOLOGY OF THE GNOMONIACEAE (DIAPORTHALES), WITH EMPHASIS ON GNOMONIOPSIS AND OPHIOGNOMONIA by DONALD MATTHEW WALKER A Dissertation submitted to the Graduate School-New Brunswick Rutgers, The State University of New Jersey in partial fulfillment of the requirements for the degree of Doctor of Philosophy Graduate Program in Plant Biology written under the direction of Dr. James F. White, Jr. and approved by ________________________ ________________________ ________________________ ________________________ ________________________ New Brunswick, New Jersey October, 2012 TAXONOMY, SYSTEMATICS, ECOLOGY, AND EVOLUTIONARY BIOLOGY OF THE GNOMONIACEAE (DIAPORTHALES), WITH EMPHASIS ON GNOMONIOPSIS AND OPHIOGNOMONIA By DONALD MATTHEW WALKER Dissertation Director: Dr. James F. White, Jr. The Gnomoniaceae (Diaporthales, Sordariomycetes, Ascomycota) are a family of perithecial ascomycetes that occur as endophytes, pathogens, or saprobes on growing and overwintered leaves and twigs of hardwood trees, shrubs, and herbaceous host plants. Many species of Gnomoniaceae cause serious diseases in agricultural and ornamental plants. Despite their economic importance, the biodiversity, evolutionary biology, ecology, and host plant relationships are largely unknown. The objectives of this study were to: 1) infer species level phylogenies of the genera Gnomoniopsis and Ophiognomonia; 2) design primers for newly identified single- copy protein-coding genes to be used as phylogenetic markers for species-level systematics in the Sordariomycetes; 3) integrate host association and environmental data with a phylogenetic analysis of Ophiognomonia to better understand speciation events in this genus. To achieve these objectives, herbarium and freshly collected specimens were compared using morphology, host association, and phylogenetic analyses of multiple molecular markers. Microscopic measurements of morphological characters such as ii ascospore size and septation were integrated with molecular approaches to define species of Gnomoniopsis and Ophiognomonia. Fungal genome sequences were mined for single- copy orthologous genes, primers designed, gene regions sequenced, and phylogenetic informativeness of each marker assessed. The performance of the newly identified markers was then compared to other markers commonly used in fungal phylogenetics. In addition, the program Spatial Evolutionary and Ecological Vicariance Analysis (SEEVA) was used to study patterns of host plant specificity and ecological vicariance using a multi-gene phylogeny of Ophiognomonia. This research resulted in the recircumscription of the genera Gnomoniopsis and Ophiognomonia in the Gnomoniaceae along with an account of each species in these genera. A total of 32 taxonomic novelties were defined including 26 new species and 6 new combinations. Primer sets for two newly identified markers were developed that should be useful for ascomycete systematists. Host specificity and environmental influences were hypothesized as mechanisms contributing to speciation patterns in Ophiognomonia. A visual and statistically solid understanding of evolutionary mechanisms influencing speciation events, host switches, and ecological divergence in the genus Ophiognomonia is presented and discussed. This a comprehensive report of the taxonomy, evolutionary biology, and ecology of the genus Ophiognomonia. iii ACKNOWLEDGEMENTS This work was funded by the National Science Foundation Partnerships for Enhancing Expertise in Taxonomy (NSF 03-28364) and USDA-ARS Systematic Mycology and Microbiology Laboratory. Additional funding to attend conferences and conduct field work was received through the C. Reed Funk award and Conference Travel Support award from Rutgers University; also through the Backus, Everett Lutrell, and National/International Travel Awards from the Mycological Society of America; through the Organization for Tropical Studies for travel and research in Costa Rica. I would like to extend a very special thank you to Amy Rossman, Lisa Castlebury, James White, Lena Struwe, and Peter Oudemans for their extraordinary guidance, support, and encouragement throughout this project and helpful discussions about the Gnomoniaceae. I would like to thank Luis Mejía and Mikhail Sogonov for teaching me how to collect, observe, and document the Gnomoniaceae and for the excellent times on several exciting collection trips. Thank you to Adam Bazinet, Jo Anne Crouch, Karl Kjer, and Steve Rehner for helpful discussions about data analysis, primer design, and species concepts. Thank you to Drew Minnis for nomenclatural advice. I am grateful for the laboratory support provided by Tunesha Phipps, Sasha Allen, and Ryan Vo at SMML and Marshall Bergen at Rutgers University. Thank you to Kentaro Hosaka, Shinobu Inoue, Takao Kobayashi, Tsuyoshi Hosoya, and Yousuke Degawa for hosting a collecting trip to Japan. I would like to thank Yuuri Hirooka for coordinating my trip to Japan and for the wonderful experience collecting fungi in Michigan. I would like to extend a special thank iv you to Alex Weir, June Wang, and Tom Horton who were my mycological mentors at SUNY ESF and primary reason for pursuing a graduate degree in mycology. v DEDICATION This work is dedicated to the very special people who have supported, encouraged, and believed in me over the last five years: my wife Lisa, my dad Donald, my mom Lynn, and sisters Danielle and April; also to the late Donald E. Walker and Robert D. Hartinger, you will be forever missed. Thank you for your love, patience, and support. vi TABLE OF CONTENTS Abstract of the dissertation………………………………………………………………..ii Acknowledgements…………………………………………………..…………………...iv Dedication……………………………………………………………………….………..vi Table of Contents……………………………………………………………….…….….vii List of Tables……………………………………………………………………………..ix List of Figures………………………………………………………………………….…xi CHAPTER 1. Introduction to the taxonomy, systematics, ecology, and evolutionary biology of the Gnomoniaceae (Diaporthales), with emphasis on Gnomoniopsis and Ophiognomonia……………………………………………………………………………1 Literature cited…………………………………………………………..………………...6 CHAPTER 2. Systematics of genus Gnomoniopsis (Gnomoniaceae, Diaporthales) based on a three gene phylogeny, host associations and morphology.............................………11 Literature cited…………………………………………………………..…………….....54 CHAPTER 3. New molecular markers for fungal phylogenetics: Two genes for species- level systematics in the Sordariomycetes (Ascomycota)...................................................57 Literature cited……………………………………………………………………..…...108 CHAPTER 4. Systematics of the genus Ophiognomonia (Gnomoniaceae, Diaporthales) based on a three gene phylogeny, host associations, and morphology ............………...114 Literature cited………………………………………………………………………….249 CHAPTER 5. Host conservatism or host specialization? Patterns of fungal diversification are influenced by host specificity in Ophiognomonia (Gnomoniaceae, Diaporthales)……………………………………………………………………………254 vii Literature cited……………………………………………………………………….....288 CHAPTER 6. Environmental influences on speciation and niche evolution in the fungal genus Ophiognomonia (Gnomoniaceae, Diaporthales).....................................……......292 Literature cited……………………………………………………………………….…339 CURRICULUM VITA………………………………………………………...……….343 viii LIST OF TABLES Table 2.1 Specimens and cultures of Gnomoniaceae sequenced for this study…………52 Table 3.1. Isolates sequenced for this study……………………………………………..88 Table 3.2. Primers designed for current study and respective PCR protocols for each gene…………………………………………………………………………………........91 Table 3.3. Alignment properties from analyses of individual markers for Gnomoniopsis and Ophiognomonia……………………………………………………………………...92 Table 3.4. Summary of support values from Maximum Parsimony Boostrap (MP BS), Maximum Likelihood (ML BS), and Bayesian (PP) analyses…………………………...93 Table 3.5. Phylogenetic performance of individual markers……………………………95 Supplementary Table 3.1. Support values from Maximum Parsimony Boostrap (MP BS), Maximum Likelihood (ML BS), and Bayesian (PP) analyses of Gnomoniopsis…..96 Supplementary Table 3.2. ModelTest Results………………………………………..100 Supplementary Table 3.3. Summary of all evaluated genes regions for molecular marker development…………………………………………………………………….105 Table 4.1. Specimens and cultures of Gnomoniaceae sequenced for this study……….242 Table 4.2. Phylogenetic Species Recognition………………………………………….247 Supplementary Table 4.1. jModelTest results……………………………….………..248 Table 5.1. Host plant relationships and geographic distribution of Ophiognomonia…..283 Table 6.1. Index of divergence (D) from the SEEVA analysis of Clade 1 in Ophiognomonia using four temperature-based variables………………………………326 Table 6.2. Index of divergence (D) from the SEEVA analysis of Clade 1 in Ophiognomonia using four precipitation-based variables……………………………...327 ix Table 6.3. Index of divergence (D) from the SEEVA analysis of Clade 2 in Ophiognomonia using four temperature-based variables………………………………328 Table 6.4. Index of divergence (D) from the SEEVA analysis of Clade 2 in Ophiognomonia using four precipitation-based variables……………………………...329 Table 6.5. Index of divergence (D) from the SEEVA analysis of Clade 3 in Ophiognomonia using four temperature-based variables………………………………330 Table 6.6. Index of divergence (D) from the SEEVA analysis of Clade 3 in Ophiognomonia using four precipitation-based variables……………………………...331 Table 6.7. Host plant relationships
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