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An Abstract of the Thesis Of AN ABSTRACT OF THE THESIS OF Lilah Gonen for the degree of Master of Science in Botany and Plant Pathology presented on December 9, 2020. Title: Community Ecology of Foliar Fungi and Oomycetes of Pseudotsuga menziesii on the Pacific Northwest Coast. Abstract approved: ______________________________________________________________________ Andy Jones Jared LeBoldus Pseudotsuga menziesii var. menziesii (coast Douglas-fir) is a tree of ecological, economic, and cultural value in its native North American Pacific Northwest (PNW) distribution. P. menziesii is host to a variety of well- documented endophytic foliar microorganisms, including the fungus Nothophaeocryptopus gaeumannii, the causal agent of Swiss needle cast (SNC), and the oomycete Phytophthora pluvialis, which causes cryptic disease symptoms in P. menziesii. Little is understood about how entire foliar microbial communities are structured by geography, climate, and host lineage, nor how foliar fungi and oomycetes interact at the tree level. This study used a large-scale reciprocal transplant experiment, next-generation sequencing (NGS), and culture-based methods to characterize the diversity and structure of foliar fungi and oomycetes of P. menziesii across three sites on the PNW coast. Fungal community composition within trees was structured by host location (p = 1e-4, 1.5e-3) as well as interactions between host location and lineage (p = 0.02, 6.4e- 3, 8e-4). Oomycete communities were dominated by a single OTU, assigned to Phytophthora cacuminis, a recently described species in Australia. An undescribed Pythium species was isolated in culture from 18 trees throughout the study sites. Generalized linear mixed models revealed that fungal community richness was positively correlated to oomycete community richness among trees (estimated coefficient = 0.14, p = 8.3e-16), and that presence of P. cacuminis negatively predicted presence of N. gaeumannii (estimated coefficient = -0.65, p = 0.03). This raises questions about P. cacuminis’ presence and origins in the PNW as well as its effects on tree health. This study is among the first to use NGS to describe P. menziesii’s foliar fungal community and to characterize nonpathogenic oomycetes residing in P. menziesii needle tissue. It illustrates the need for further experimental research to identify biotic drivers of microbial community assembly, as well as the downstream implications for forest management. ©Copyright by Lilah Gonen December 9, 2020 All Rights Reserved Community Ecology of Foliar Fungi and Oomycetes of Pseudotsuga menziesii on the Pacific Northwest Coast by Lilah Gonen A THESIS submitted to Oregon State University in partial fulfillment of the requirements for the degree of Master of Science Presented December 9, 2020 Commencement June 2021 Master of Science thesis of Lilah Gonen presented on December 9, 2020 APPROVED: Major Professor, representing Botany and Plant Pathology Head of the Department of Botany and Plant Pathology Dean of the Graduate School I understand that my thesis will become part of the permanent collection of Oregon State University libraries. My signature below authorizes release of my thesis to any reader upon request. Lilah Gonen, Author ACKNOWLEDGEMENTS First, I must thank my advisors and committee: Jared LeBoldus, Andy Jones, Posy Busby, and Dave Shaw for your mentorship, patience, respect, and, importantly, funding of my time and energy at OSU. I feel very lucky to now have the intellectual foundations of both a forest ecologist and pathologist and I do believe I’ll take the diversity of thought and methodology that these four have instilled in me far into my career. Second, to the lab members who offered me so much in my two plus years at OSU. Chiefly, Kelsey Søndreli, for keeping the lab clean and functional, ordering most of my equipment, and patiently helping with virtually all of my laboratory tasks; Patrick Bennett, for going on an overnight sampling trip with me to Washington, driving the whole way, and keeping a good attitude despite falling a lot; Devin Leopold, for your instrumental help in bioinformatics; Paul Reeser and Wendy Sutton, for being some of the best resources in the world (truly) on oomycete biology, culturing, and sequencing; Kyle Gervers, for your enthusiasm in all things microbiome, and your involvement in everything from sampling trips to troubleshooting library prep to diving deeply into ecological theory; Kayla Delventhal for the statistical breakthroughs, commiseration, and friendship; Javier Tabima, for teaching me many things including how to write a manuscript, how to use the cluster, and how to ask stupid questions; and finally Shawn McMurtrey, for washing all of our dishes and making me laugh. Third, to the US Forest Service for granting me access to the SSMT sites, assisting me in the field, and sharing valuable data with me. Those folks include Brad St. Clair, Connie Harrington, Chris Poklemba, Beverly Luke, Leslie Brody, and Dave Thornton. Fourth, to the lifelong friendships I made at Shrub House: Kat, Cedar, Meredith, and Allie. Fifth, to Lauren, Livi, and dear Gordon, for the important stuff. And finally, a profound acknowledgement to the Kalapuya people and the Confederated Tribes of the Grand Ronde and Siletz, on whose stolen land I was raised and OSU sits. TABLE OF CONTENTS Page 1. General Introduction ........................................................................................................................ 1 1.1 Literature Cited ................................................................................................................12 2. Community Ecology of Foliar Fungi and Oomycetes of Pseudotsuga menziesii on the Pacific Northwest Coast ..............................................................................................................20 2.1 Abstract ...............................................................................................................................21 2.2 Introduction ......................................................................................................................22 2.3 Materials and methods..................................................................................................28 2.3.1 Study sites ........................................................................................................28 2.3.2 Sample collection...........................................................................................29 2.3.3 Culturing and sequencing oomycetes ...................................................30 2.3.4 Sequencing fungal and oomycete communities ................................33 2.3.5 Bioinformatics ................................................................................................35 2.3.6 Statistical analysis .........................................................................................37 2.4 Results .................................................................................................................................40 2.4.1 Oomycete isolates .........................................................................................40 2.4.2 Community composition of fungi and oomycetes ............................41 TABLE OF CONTENTS (Continued) 2.4.3 Fungal diversity in response to biotic and abiotic predictors .....43 2.5 Discussion ..........................................................................................................................45 2.5.1 Foliar fungal communities are structured by local environmental conditions ....................................................................................................................45 2.5.2 Foliar oomycete communities are dominated by one OTU...........50 2.5.3 Presence of foliar fungi can be predicted by the presence of foliar oomycetes ...................................................................................................................52 2.6 Conclusions ........................................................................................................................54 2.7 Literature Cited ................................................................................................................57 2.8 Figures .................................................................................................................................67 2.9 Tables ...................................................................................................................................82 3. General Conclusions ........................................................................................................................86 3.1 Literature Cited ................................................................................................................92 4. Bibliography .......................................................................................................................................96 LIST OF FIGURES Figure Page 2.1 Locations of seed source region (SSR) (left) and study sites (right). Seed was collected from 2 maternal trees (inset) in each of 5 locations within each SSR. Each SSR was composed of 10 lines of half-siblings (families). Adapted from Wilhelmi et al. (2017)........................................................................................................................................................67 2.2 Example of study site layout. Each site was divided into 4 blocks, where each SSR was randomly assigned a plot. Each SSR plot contained 2 replicates of the 10
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