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Biotic Filters in Fungal Endophyte Community Assembly BIOTIC FILTERS IN FUNGAL ENDOPHYTE COMMUNITY ASSEMBLY by Megan Saunders A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Graduate Department of Ecology and Evolutionary Biology University of Toronto © Copyright by Megan Saunders 2010 BIOTIC FILTERS IN FUNGAL ENDOPHYTE COMMUNITY ASSEMBLY Degree of Doctor of Philosophy Megan Saunders Graduate Department of Ecology and Evolutionary Biology University of Toronto 2010 ABSTRACT My work focuses on the community ecology of symbioses, specifically of fungal endophytes and their hosts. This thesis describes how plant defense compounds and a seed endophyte influence community structure of maize fungal endophytes. Maize produces benzoxazinoids (BXs), compounds toxic to microbes and insects. I assessed the influence of three factors on endophyte communities: host BX production, host neighbor identity and presence of a BX-detoxifying endophyte, Fusarium verticillioides (FV). To determine the influence of BXs on communities, two BX- producing (BX+) and one BX-nonproducing (BX–) genotype were planted in Ridgetown and Harrow, Ontario (triculture). Fungi were isolated and tested for tolerance to 2-benzoxazolinone (BOA), a toxic BX byproduct. Species and functional diversity (community distribution of BOA tolerance levels) was calculated. In seedling roots and mature leaves, the community proportion with low BOA tolerance was greater in BX– than BX+ plants. Fusarium abundance was up to 35 times higher in mature leaves of BX+ than BX– plants. Next, to assess the effect of host neighbor identity on communities, BX– monocultures were planted, and communities from BX– plants in monoculture and triculture compared. Monoculture root communities had higher species diversity than those in triculture. In vitro experiments were conducted to evaluate the influence of BOA on endophyte species interactions. FV facilitated species with lower BOA tolerance in the presence of BOA. Finally, fields were planted with a BX+ and BX– genotype in Ontario, Canada and Georgia, USA. Seed was inoculated with FV (FV+) or sterilized (FV–). FV abundance was highest in BX+FV+ plants, and Fusarium abundance was greater in ii BX+ than BX– plants in mature leaves. In Georgia, BX+FV+ communities in below ground tissue had lower abundance of BOA sensitive species than BX+FV–. Overall, results suggest that BXs are a habitat filter that increased colonization by horizontally transmitted and seed-born Fusarium species. This invokes the hypothesis that selective breeding for enhanced BX concentrations increased abundance of Fusarium species in maize. The in vitro study indicated that FV could facilitate other species. In contrast, field results suggest that FV interacts competitively with community members, a trait enhanced in the presence of BXs. iii ACKNOWLEDGEMENTS I would first like to thank my advisor, Linda Kohn, who has been there to support and guide me through my graduate school career. Her enthusiasm and dedication to science are an inspiration. I am also grateful to the members of my Ph.D. committee for providing advice on all aspects of becoming a scientist. I thank Jim Anderson for his encouragement and insight throughout this project. Peter Kotanen allowed me to take up residence in his lab for five years, has had unwavering enthusiasm for my work, and was always willing to provide feedback. Thank you to Tony Glenn for hosting me in his lab, and for being a constant source of advice and support over the years. This project would not have been possible without the help of a handful of excellent field and lab assistants. Lisa Hopcroft, Arthur Snare and Bobby Diaz made significant contributions to the project by sequencing fungal DNA and assisting with culture maintenance. Albert Tenuta, Britton Ormiston, and Terry Anderson assisted greatly in the field, and Jeff Brotherton provided the maize seed used in this project. Thank you also to Keith Seifert and John Leslie for providing fungal isolates. I would also like to thank Lorraine Thompson for hosting me while I was in Georgia doing field work. I have been fortunate to share space with labmates that are outstanding both as scientists and as people; I would like to thank members of the Kohn lab, Anderson lab and Kotanen lab for their support. Caroline Sirjusingh always made herself available for technical training. I shared countless scientific discussions over afternoon tea with Andrew MacDonald, Steve Hill and Marion Andrew, which never failed to ignite my excitement about ecology. Finally, I could not have done any of this without the love and support of my family. I am extremely lucky to have loving parents, Lynn and George, who have always believed in my ability to accomplish whatever I put my mind to. Thanks to my sister, Allyson, for doing everything possible to help me be happy. I have been fortunate enough to inherit a Canadian family, the Caradonna family, all of whom have been supportive and caring. My husband Steve has been a constant source of love, encouragement, and comfort from the moment that we met. Thank you Steve, for everything. iv TABLE OF CONTENTS ABSTRACT ii ACKNOWLEDGEMENTS iv TABLE OF CONTENTS v LIST OF TABLES ix LIST OF FIGURES xi CHAPTER 1. GENERAL INTRODUCTION 1 Thesis overview 2 Relationship between fungal endophytes and their plant hosts 3 Biotic filters in fungal endophyte community assembly 8 Host plant species 8 Host plant genotype 10 Biochemical plant defense mechanisms 12 Fungal endophyte infection can induce host defense reactions 14 Environmentally acquired plant defense mechanisms 16 Microbial species interactions 17 Objectives of thesis 21 CHAPTER 2. EVIDENCE FOR ALTERATION OF FUNGAL ENDOPHYTE COMMUNITY ASSEMBLY BY HOST DEFENSE COMPOUNDS 24 Abstract 25 Introduction 26 Materials and Methods 28 Maize genotypes 28 Study site and collection times 29 Isolation of fungi from plant tissue 29 Identification of fungal isolates 30 DNA isolation, polymerase chain reaction amplification (PCR) and sequencing 31 v Assignment of isolates to BOA tolerance threshold group 32 Statistical analyses 32 Abundance of Fusarium in 9-wk-old plants 32 Diversity and similarity of fungal endophyte communities 32 BOA tolerance of fungal endophyte communities 34 Results 34 Relative abundance and diversity of endophytes 34 BOA tolerance levels of endophytic fungi 38 Partitioning of endophyte communities by BOA tolerance level 41 Abundance of Fusarium in 9-wk-old plants 41 Discussion 45 Presence of BXs influences endophyte community structure 45 BX+ plants have a higher incidence of Fusarium than BX- plants 48 Commonalities between endophyte community ecology in agricultural and naturally 49 occurring plants Conclusions 50 CHAPTER 3. PRODUCTION OF DEFENSE COMPOUNDS BY PLANT 52 NEIGHBORS DECREASES FUNGAL ENDOPHYTE ABUNDANCE AND DIVERSITY IN MAIZE ROOTS Abstract 53 Introduction 54 Materials and Methods 56 Study site, maize varieties and tissue collection 56 Isolation of fungi from root and leaf tissue 57 Identification of fungal isolates 57 Statistical analyses 58 Results 61 Discussion 64 CHAPTER 4. HOST-SYNTHESIZED SECONDARY COMPOUNDS INFLUENCE 69 THE IN VITRO INTERACTIONS BETWEEN FUNGAL ENDOPHYTES OF MAIZE Abstract 70 Introduction 71 vi Materials and Methods 74 Characterization of BOA tolerance in maize endophytes 74 Strains assessed for BOA tolerance 74 Isolation of fungal endophytes from maize 76 Sequential inoculation experiments 77 Assessment of presence of BOA in the medium 78 Statistical analyses 79 Results 79 Characterization of BOA tolerance 79 Sequential inoculation of species pairs 79 Assessment of biodegradation of BOA in the medium 85 Discussion 85 CHAPTER 5. HOST DEFENSE COMPOUNDS AND THE SEED ENDOPHYTE, 92 FUSARIUM VERTICILLIOIDES, AS FILTERS IN FUNGAL ENDOPHYTE COMMUNITY ASSEMBLY Abstract 93 Introduction 94 Materials and Methods 97 Field experiment 97 Isolation and identification of fungi 98 Species diversity of fungal endophyte communities 100 Functional diversity of fungal endophyte communities 101 Abundance of Fusarium 102 BX concentration of maize plants 102 Results 103 Species diversity of fungal endophyte communities 103 Functional diversity of fungal endophyte communities 109 Abundance of Fusarium 117 BX concentration in maize plants 117 Discussion 120 CHAPTER 6. SUMMARY 125 vii LITERATURE CITED 130 viii LIST OF TABLES Table 2.1. BOA tolerance thresholds of fungal endophyte species or 33 morphotypes isolated from maize (bxbx, B37, W22 genotypes). Table 2.2. Diversity of fungal endophyte communities in maize. 39 Table 2.3. Results of χ2 tests for a difference between proportion of 42 isolates in BOA tolerance threshold groups 0.25 (0.25% BOA tolerance threshold) and 0.50 in endophyte communities from maize bxbx (BX– genotype), W22 and B37 (BX+ genotypes). Table 2.4. Identity of a subset of isolates obtained from 9-wk-old maize 46 tissue plated on BOA medium. Table 3.1. Species isolated from leaf and root tissue of BX- (bxbx) maize 60 grown in monoculture and in triculture. Table 4.1. BOA tolerance threshold (highest concentration of BOA 75 supporting growth) of common maize endophytes. Table 5.1. Abundance of species and morphotypes (with No. designations) 104 isolated from maize in Ontario and Georgia. Table 5.2. BOA tolerance thresholds (highest concentration of BOA 110 supporting growth in mg per ml) of maize fungal endophytes isolated from plants grown in Georgia and Ontario. Table 5.3. MANOVA of BOA tolerance threshold groups with maize 113 genotype (BX+ or BX-) and infection status (FV+ or FV-) as ix factors. Table 5.4. MANOVA of average community BOA tolerance level, and 116 average community BOA tolerance level with Fusarium verticillioides removed from the analysis with maize genotype (BX+ or BX-) and infection status (FV+ or FV-) as factors. Table 5.5. Identity of isolates obtained on BOA medium from plants grown 119 in Ontario and Georgia. Isolates from 2 plants/block were identified. x LIST OF FIGURES Figure 1.1. Movement of species from a regional species pool to a local 7 community. Figure 2.1. Collection data and community bar graphs of isolates obtained 35-37 from root (a) and leaf (b) tissue of maize on PDA.
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