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Systematics of Bark-Inhabiting Species Of ©2009 Luis Carlos Mejía Franco ALL RIGHTS RESERVED SYSTEMATICS AND EVOLUTION OF BARK-INHABITING SPECIES OF THE GNOMONIACEAE (DIAPORTHALES, ASCOMYCOTA) WITH EMPHASIS ON THE GENERA CRYPTOSPORELLA AND PLAGIOSTOMA By LUIS CARLOS MEJÍA FRANCO 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, 2009 ABSTRACT OF THE DISSERTATION SYSTEMATICS AND EVOLUTION OF BARK-INHABITING SPECIES OF THE GNOMONIACEAE (DIAPORTHALES, ASCOMYCOTA) WITH EMPHASIS ON THE GENERA CRYPTOSPORELLA AND PLAGIOSTOMA By LUIS CARLOS MEJÍA FRANCO Dissertation Director: Dr. James F. White Jr. The Gnomoniaceae (Diaporthales, Ascomycota) comprise microfungi that grow on leaves and woody tissues of a range of plant families, mostly hardwood trees from temperate zones of the northern hemisphere. Many dominant endophytes of trees in North America and Europe are species of Gnomoniaceae. Several emerging and devastating diseases of forest trees are caused by pathogenic species of Gnomoniaceae. Despite their abundance and impact in forest ecosystems, the Gnomoniaceae have not received modern taxonomic review and phylogenetic study. Most morphologically defined genera in this family are polyphyletic when analyzed with molecular data, therefore new circumscription of genera is needed. The objectives of this work are to: 1) define monophyletic genera and determine species limits for bark-inhabiting fungi in the Gnomoniaceae; and 2) infer the phylogeny of bark-inhabiting genera of Gnomoniaceae (e.g. Cryptosporella, and Plagiostoma). To ii achieve these objectives fresh specimens were collected in locations in Europe, North, Central and South America, and China. Specimens from herbaria and living collections from culture repositories were included in the study. The methods integrate a comparison of morphological characters of specimens in natural substrates such as the arrangement, shape, and size of perithecia and the shape and size of asci and ascospores with molecular characters, i.e. DNA sequences from multiple loci (β-tubulin, ITS, LSU, rpb2, and tef1-α) analyzed by Bayesian inference, Maximum Likelihood, Neighbor Joining, and Parsimony. This research resulted in the recircumscription of the genera Cryptosporella and Plagiostoma and the definition of a new genus Occultocarpon gen. nov. A total of 32 taxonomic novelties were defined. More specifically, 17 new species, a new genus of bark-inhabiting Gnomoniaceae, and 14 new name combinations were described. This project has shown that host identity is a better predictor than geographic location for finding species of Gnomoniaceae. By documenting species of Gnomoniaceae from the Neotropics, South America, and subtropical China, results from this project have changed the previous assumption that the Gnomoniaceae only occur in temperate zones of the Northern Hemisphere. Finally, the phylogenies obtained suggest a long evolutionary relationship between Cryptosporella and Betulaceae and a subclade of Plagiostoma with the Salicaceae. iii ACKNOWLEDGEMENTS This work was funded by the National Science Foundation Partnerships for Enhancing Expertise in Taxonomy (NSF 03-28364). Additional funding for field work was received through the Neyra Fund and the Spencer Davis Research Award from the Department of Plant Biology and Pathology, and from a Special Study Support Award and a Graduate School Travel Award from the Graduate School, Rutgers University, New Brunswick; through the Backus Award from the Mycological Society of America; and through a Short-Term Research Fellowship from the Smithsonian Tropical Research Institute. Most of the laboratory work presented here was done at the Systematic Mycology and Microbiology Laboratory (SMML), USDA-Agricultural Research Service, Beltsville, Maryland. My greatest acknowledgement goes to Lisa A. Castlebury, Amy Y. Rossman, and James F. White Jr. for introducing me to the beautiful Gnomoniaceae, for training on systematics, for their guidance and for extraordinary support throughout this project. Also special acknowledgments are extended to the other two members of my dissertation committee: Thomas Gianfagna and Lena Struwe for their valuable advice and inputs to this research. Thanks to Mikhail Sogonov for training on the digital image processing software employed in this work and for stimulating discussions about the Gnomoniaceae. Thanks to all the members of the SMML for making a pleasant work environment and for sharing their valuable expertise on several aspects of the systematics and taxonomy of fungi, especially Gary Samuels and Stephen Rehner. Thanks to Andrew Minnis for providing a specimen from which a new species of Plagiostoma was described. Also my gratitude goes to Tunesha Phipps and Sasha Allen for laboratory support at the SMML. I sincerely iv appreciate the following people for hosting my visit to collecting places and for facilitating the shipment of specimens: Michael Giraurd, Adriana Hladki, Tina Hoffman, Christian Lechat, Christophe Lecuru, and Ralph Mangelsdorff. Special thanks to Zhu LiangYang for hosting me and providing such great support on my collection trip in China. Also special thanks to Donald Walker with whom I had the pleasure to explore the Pacific Northwest and share the excitement of finding Gnomoniaceae and for great logistical support during collection trips in the USA. I express my appreciation to the staff of the Plant Biology and Pathology Department at Rutgers for helping me when I needed them. Thanks to Marshal Bergen for laboratory support and for caring about my English while at Rutgers. Thanks to Joseph Bischoff who was the first to tell me about the possibility to work on an NSF-PEET project at Rutgers. Finally I want to thank the following people for providing me with extraordinary support and encouragement to come to the graduate school and pursue this dream: Anne Elizabeth Arnold, Prakash Hebbar, and Edward Allen Herre. v DEDICATION This work is dedicated to the most special people in my life: my son Carlos Manuel and my wife Enith; my mom Elia Judith, my dad Carlos, my sister Sara, and my brothers Horacio and Isaac. Thanks for your patience and for being very supportive. vi TABLE OF CONTENTS Abstract of the dissertation………………………………………………………….……ii Acknowledgements…………………………………………………..…………………..iv Dedication……………………………………………………………………….……….vi Table of Contents……………………………………………………………….……….vii List of Tables…………………………………………………………………………….ix List of Figures………………………………………………………………………….…x CHAPTER 1. Review of the Diaporthales with emphasis on the Gnomoniaceae………..1 Literature cited…………………………………………………………..………………12 CHAPTER 2. Phylogeny of Gnomoniaceae including Occultocarpon, a new monotypic genus on Alnus nepalensis from China ………………………………………………….15 Literature cited……………………………………………………………………..……26 CHAPTER 3. Phylogenetic placement and taxonomic review of the genus Cryptosporella and its synonyms Ophiovalsa and Winterella (Gnomoniaceae, Diaporthales)………….28 Literature cited…………………………………………………………………………...63 CHAPTER 4. New species, phylogeny, host associations, and geographic distribution of the genus Cryptosporella Sacc. (Gnomoniaceae, Diaporthales)………………………...66 Literature cited……………………………………………………………………….....107 CHAPTER 5. Systematic review of the genus Plagiostoma Fuckel (Gnomoniaceae) based on morphology, host-associations, and a four-gene phylogeny………………....110 Literature cited……………………………………………………………………….…182 CHAPTER 6. Bark-inhabiting species of Gnomoniaceae, final remarks.……………...185 Literature cited……………………………………………………………………….....192 vii APPENDIX. Fungal endophytes: defensive characteristics and its agricultural applications……………………………………………………………………….….…193 CURRICULUM VITA………………………………………………………...……….229 viii LIST OF TABLES Table 1.1 - Species richness in the Gnomoniaceae……………………………………….8 Table 1.2 - Source of DNA sequences used in nrLSU phylogeny of the Diaporthales presented in Figure 1.1. …………………………………………………………….….…9 Table 3.1 - Isolates in the phylogenetic analyses of Cryptosporella and related members of the Diaporthales……………………………………………………………………….60 Table 4.1 - Source of isolates and specimens used in the phylogenetic analyses of Cryptosporella……………………………………………………………………….…..99 Table 4.2 - Summary of Cryptosporella species and their host associations…………..102 Table 5.1 - Isolates included in the phylogenetic analyses of Plagiostoma………..…..179 ix LIST OF FIGURES Figure 1.1 - Phylogeny of the Diaporthales based on nrLSU gene………………….…..10 Figure 2.1 - Fifty percent majority rule phylogram derived from Bayesian analysis of gnomoniaceous taxa using model GTR+I+G on gene regions tef1-α, rpb2, and nrLSU (total of 2730 characters)………………………………………………………………...23 Figure 2.2 – Morphology on natural substrate. Occultocarpon ailaoshanense. A-C,G,H= BPI879253 (holotype), D-E=BPI979255, F=BPI879254. Scale: (A-E) 100 μm; (G-F) 10 100 μm………………………………………………………………………………..….25 Figure 3.1 - Single most parsimonious tree based on analysis of 2831 bp representing a combination of three different loci (LSU, ITS and RPB2) of 24 gnomoniaceous taxa using species of Melanconis and Cryphonectria as outgroup taxa (CI = 0.246, RI = 0.552, RC = 0.236,
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