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Lichens, Earth Tongues, and Endophytes : Evolutionary Patterns Inferred from Phylogenetic Analyses of Multiple Loci

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AN ABSTRACT OF THE DISSERTATION OF Jamie L. Platt for the degree of Doctor of Philosophy in Molecular and Cellular Biology presented on September 24 1999. Title: Lichens, Earth Tongues, and Endophytes: Evolutionary Patterns Inferred from Phylogenetic Analyses of Multiple Loci. Redacted for Privacy Abstract approved: ---" ­ Joseph W. Spatafora The inoperculate discomycete order Helotiales (Ascomycota) is a diverse and complex group of fungi which include lichens, earth tongues, and endophytes. Cladistic analyses of multiple loci were used to test and construct phylogenetic hypotheses and to examine the evolution of various life history strategies adopted by these fungi. Several prominent patterns of convergent evolution were revealed. Within the lichenized Helotiales, nuclear SSU and LSU rDNA data inferred two distinct lineages (i.e., Baeomycetaceae and Icmadophilaceae) representing potential independent gains of the lichen symbiosis. The common "baeomycetoid" morphology of these fungi, was shown to be the result of convergent evolution between these two distinct lineages. The correspondence of phylogenetic hypotheses from independent, multiple loci also presented reciprocal corroboration for convergent evolution of sporocarp morphology among the earth tongues. At least four independent lineages which possess the earth tongue fruitbody morphology were inferred from the three independent data sets of SSU rDNA, combined SSD and LSD rDNA, and RPB2. The close phylogenetic relationship between the earth tongues, Cudonia and Spathularia (Helotiales) and some endophytes represented by members of the Rhytismatales was particularly provocative due to vast differences in sporocarp morphology, but was nonetheless well-supported and corroborated with these forms of independent molecular phylogenetic evidence. Phylogenetic hypotheses constructed from analyses of multiple loci inferred that the Helotiales are polyphyletic, a finding not consistent with the character of inoperculate asci being a synapomorphy for this group. Rather, polarization of this ascus character suggested that inoperculate asci may be symplesiomorphic for many of the euascomycetes. Other life history strategies were also examined within the lichenized Helotiales including the loss of sexual reproduction. Analyses of nuclear SSD and LSD rDNA prompted a proposal to emend the Icmadophilaceae to include the nonsexual genera Siphula and Thamnolia which were previously classified in the Lecanorales. Other revised classifications were proposed. The Geoglossaceae are redefined to include Geoglossum, Sarcoleotia, and Trichoglossum, but to exclude Microglossum, Cudonia, and Spathularia. The effect of fungal intragenic SPY on maximum parsimony was also examined. ©Copyright by Jamie L. Platt September 24, 1999 All Rights Reserved Lichens, Earth Tongues, and Endophytes: Evolutionary Patterns Inferred from Phylogenetic Analyses of Multiple Loci by Jamie L. Platt A DISSERTATION submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Presented September 24, 1999 Commencement June 2000 Doctor of Philosophy dissertation Jamie L Platt presented on September 24, 1999 APPROVED: Redacted for Privacy Major Redacted for Privacy Redacted for Privacy Dean of Gfaduate School I understand that my dissertation will become part of the permanent collection of Oregon State University libraries. My signature below authorizes release of my dissertation to any reader upon request. Redacted for Privacy Jamie L. Platt, Author ACKNOWLEDGEMENTS I wish to thank all current and past members of my graduate committee. Firstly, I owe sincere thanks to my dissertation advisor, Joey Spatafora who patiently guided me along the phylogenetics learning curve and provided an intellectually stimulating environment during my graduate career. I thank Aaron Liston who provided valuable advice regarding phylogenetic analyses and guidance in pointing out the relevant current literature. I am particularly grateful to Jeff Stone for his support and mentorship. Although Jeff was not initially a member of my committee, he showed enthusiasm for my project and my professional development. I thank Bruce McCune for his expertise in lichenology and for challenging me to think and communication broader terms. I am grateful to Kate Field for her support throughout my graduate career and for her ability to pose insightful and provoking questions. Finally, I would like to thank Barbara Roth for her role as my graduate representative. Over the years many people have contributed to this project in ways ranging from technical advice to personal support and encouragement. lowe a great deal of thanks to Ankie Camacho with whom I had numerous discussions that spawned ideas applied to this project as well as to future projects. Ankie also provided a vast amount of technical and personal support. Special thanks to Dave Gernandt who provided valuable Unix expertise and technical advice. I am grateful to Lori Winton for technical assistance, especially with respect to developing DNA extraction methods for pigmented fungi. My labmates Lisa Grubisha, Kathie Hodge, Andrea Humpert, Suzie Holmes, Ron Hamill, Annette Kretzer and Eric Muench also made significant contributions for which I am grateful. The staff at the Central Services Laboratory at the Center for Gene Research and Biotechnology was invaluable. Special thanks to Nanci Adair for her technical expertise in nucleotide sequencing. Several people at the Forest Science Laboratories also contributed to this project through their technical advice and contribution of fungal material. Specifically, thanks to Nancy Weber, Jim Trappe, and Ari Jumponnen for being particularly supportive in this manner. I also thank Tom O'Dell and his crew and Diane Greene for contribution earth tongue collections. I am particularly grateful to the Molecular Systematics Discussion Group for valuable discussions and useful comments on methods of analysis for this project. My interactions with this group were probably one of the most valuable experiences of my graduate career with respect to phylogenetic theory. Franc;ois Lutzoni was also particularly helpful with respect to discussions regarding analyses. The overwhelming majority of funding for this project has come from the discretionary funds of Joey Spatafora. lowe many thanks to Joey for his financial support. I also wish to thank the Friends of the Farlow Herbarium and Harvard University for a fellowship which allowed me to visit and conduct research at the Farlow Herbarium and Library. Special thanks to Don Pfister and his group in this regard. Finally, I thank the Mycological Society of America for partial funding of this project through a MSA Graduate Fellowship and for their generous support through mentorship, student travel awards, and society events. CONTRIBUTION OF AUTHORS Chapter four was co-authored with Francisco J. Camacho and Joseph W. Spatafora. Francisco Camacho made major contributions regarding data analyses, taxon sampling, and study design. All data collection was done in the laboratory of Joseph Spatafora, who also provided the funding for this study from his discretionary funds. Joseph Spatafora also provided expertise in phylogenetic analyses and cladistic theory. Chapter six was co-authored with Joseph Spatafora, David Gemandt, Jeffrey Stone, Jacqui Johnson, and Steve Alderman who all contributed rDNA sequence data and ideas of directed taxon sampling. Much of the data collection was done in the laboratory of Joseph Spatafora who also provided expertise in phylogenetic analyses. Dave Gemandt provided advice on navigating UNIX operating systems. Jeffrey Stone contributed cultures of endophytes and provocative taxonomic discussions. TABLE OF CONTENTS Page CHAPTER 1 INTRODUCTION AND LITERATURE REVIEW ................................. 1 1.1 Abstract................................................................................................... l 1.2 Introduction.............................................................................................2 1.3 Taxon Sampling ......................................................................................7 1.3.1 Historical overview of the Helotiales ...........................................8 1.3.2 Evolution of life history strategies of the Helotiales ................... 12 1.4 Character Sampling ............................................................................... 14 1.4.1 Nuclear ribosomal DNA ........................................................... 15 1.4.1.1 Nuclear SSU ribosomal DNA ..................................... 16 1.4.1.2 Nuclear LSU ribosomal DNA ....................................21 1.4.2 RNA Polymerase II (RPB2) .......................................................23 1.5 Phylogenetic Analyses ..........................................................................24 1.6 Conclusions...........................................................................................25 1.7 Literature Cited .....................................................................................26 CHAPTER 2 A RE-EXAMINATION OF GENERIC CONCEPTS OF BAEOMYCETOID LICHENS BASED ON PHYLOGENETIC ANALYSES OF NUCLEAR SSU AND LSU RIBOSOMAL DNA ........................................................31 2.1 Abstract.................................................................................................32 2.2 Introduction...........................................................................................32
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