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Spatial and Temporal Ecology of Oak-Associated Fungal Communities Communities II Faticov, M., Desprez-Loustau, M-L., Kiss, L., Massot, M., D'arcier, J

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Spatial and Temporal Ecology of Oak-Associated Fungal Communities Communities II Faticov, M., Desprez-Loustau, M-L., Kiss, L., Massot, M., D'arcier, J Maria Faticov This thesis includes the following chapters: Spatial and temporal ecology of I Faticov, M., Abdelfattah, A., Hambäck, P., Roslin, T. and Tack, A. J. M. Different spatial structure of above- and belowground plant- oak-associated fungal associated fungal communities. Manuscript. fungal communities ecology of oak-associated temporal and Spatial communities II Faticov, M., Desprez-Loustau, M-L., Kiss, L., Massot, M., d'Arcier, J. F., Mutz, J., Németh, M. Z., Roslin, T. and Tack, A. J. M. 2020. Niche differentiation within a cryptic pathogen complex: Maria Faticov climatic drivers and hyperparasitism across spatial scales. Submitted manuscript. III Faticov, M., Abdelfattah, A., Roslin, T., Vacher, C., Hambäck, P., F. Blanchet, G., Lindahl, B. D. and Tack, A. J. M. 2020. Climate warming dominates over plant genotype in shaping the seasonal trajectory of foliar fungal communities on oak. Submitted manuscript. IV Faticov, M., Ekholm, A., Roslin, T. and Tack, A. J. M. 2020. Climate and host genotype jointly shape tree phenology, disease levels and insect attacks. Oikos 129: 391–401. Maria Faticov Ecologist who is fascinated by fungi on trees. ISBN 978-91-7911-412-1 Department of Ecology, Environment and Plant Sciences Doctoral Thesis in Ecology and Evolution at Stockholm University, Sweden 2021 Spatial and temporal ecology of oak-associated fungal communities Maria Faticov Academic dissertation for the Degree of Doctor of Philosophy in Ecology and Evolution at Stockholm University to be publicly defended on Friday 16 April 2021 at 10.00 online via zoom, a link will be published a few days before the defence at https://www.su.se/deep/. Abstract Plants host a large diversity of microorganisms, which includes fungi, bacteria and archaea. Among these, fungi are highly diverse, and known to play a vital role in plant health and in regulation of the essential ecosystem functions. Nevertheless, we still lack a comprehensive understanding of the forces structuring plant-associated fungal communities in space and time. The main aim of this thesis was to decipher the drivers of the spatial patterns and temporal dynamics of fungal communities on plants. To this aim, I focused on Quercus robur and its associated fungi. Using a combination of observational and experimental studies, I assessed i) the distribution and drivers of the above- and belowground fungal communities at the landscape scale; ii) the role of climatic and trophic factors in defining the niches of cryptic species within a pathogen complex on oak and iii) the relative importance of warming, plant genotype and their interaction in shaping oak phenology and the seasonal dynamics of the associated fungal and insect communities. I found that aboveground fungal communities were highly variable among leaves within a single tree, and that belowground fungal communities had a stronger spatial structure than aboveground fungi at the landscape scale. Yet, climate, tree phenology or the distribution of the host tree did not explain spatial patterns in the above- and belowground communities. When focusing on three cryptic powdery mildew species within a pathogen complex on oak, I demonstrated that the climatic dimension is more important than the species interaction dimension for niche differentiation of these cryptic pathogens. A field heating experiment showed strong seasonal change in the structure of the foliar fungal community, with experimental warming playing an important role in driving this change. This experiment also revealed that warming and plant genotype jointly shape plant phenology, disease levels and insect abundance across the growing season. In conclusion, my findings suggest that abiotic forces can override biotic forces in structuring spatial patterns and temporal dynamics of fungal communities associated with plants. The particularly strong impact of warmer temperatures on foliar fungi in some of my studies indicates that climate warming has the potential to structure foliar fungal communities, with important implications for plant health, interactions between plants and other organisms and ecosystem functions. Keywords: abiotic and biotic forces, climate warming, community ecology, foliar fungal community, host genotype, plant microbiome, powdery mildew, seasonal dynamics, warming-by-genotype interaction, Quercus robur, soil fungal community, spatial patterns. Stockholm 2021 http://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-190746 ISBN 978-91-7911-412-1 ISBN 978-91-7911-413-8 Department of Ecology, Environment and Plant Sciences Stockholm University, 106 91 Stockholm SPATIAL AND TEMPORAL ECOLOGY OF OAK-ASSOCIATED FUNGAL COMMUNITIES Maria Faticov Spatial and temporal ecology of oak-associated fungal communities Maria Faticov ©Maria Faticov, Stockholm University 2021 ISBN print 978-91-7911-412-1 ISBN PDF 978-91-7911-413-8 Cover and illustrations by Maria Faticov Drawing of powdery mildew on cover page, in Introduction (p. 10) and on cover of Chapter II by Emilia Regazzoni Printed in Sweden by Universitetsservice US-AB, Stockholm 2021 To Igor, my best friend and deepest love. List of chapters This thesis is based on the following chapters, which are referred to in the text by their Roman numerals. I Faticov, M., Abdelfattah, A., Hambäck, P., Roslin, T. and Tack, A. J. M. Different spatial structure of above- and belowground plant-associated fungal communities. Manuscript. II Faticov, M., Desprez-Loustau, M-L., Kiss, L., Massot, M., d'Arcier, J. F., Mutz, J., Németh, M. Z., Roslin, T. and Tack, A. J. M. 2020. Niche differentiation within a cryptic pathogen complex: climatic drivers and hyperparasitism across spatial scales. Submitted manuscript. III Faticov, M., Abdelfattah, A., Roslin, T., Vacher, C., Hambäck, P., Blanchet, G., Lindahl, B. D. and Tack, A. J. M. 2020. Climate warming dominates over plant genotype in shaping the seasonal trajectory of foliar fungal communities on oak. Submitted manuscript. IV Faticov, M., Ekholm, A., Roslin, T. and Tack, A. J. M. 2020. Climate and host genotype jointly shape tree phenology, disease levels and insect attacks. Oikos 129: 391–401. Contributions I II III IV Idea and design MF, AA, AT MF, AT, MLDL MF, AT, TR MF, AE, AT, TR Data collection MF, AA MF, AT, JM, LK, MF MF, AE MLDL, MN Molecular work MF, AA JdA, MM, MN MF, AA, BL and bioinformatics Analyses MF MF MF, GB MF Manuscript MF MF MF MF preparation Manuscript AA, AT, PH, AT, JM, LK, MM, AA, AT, BL, AE, AT, TR reviewing TR MLDL, MN, TR CV, PH, TR MF = Maria Faticov AA = Ahmed Abdelfattah JM = Jessie Mutz AE = Adam Ekholm LK = Levente Kiss AT = Ayco Tack MLDL = Marie-Laure Desprez-Loustau BL = Björn Lindahl MM = Marie Massot CV = Corinne Vacher MN = Márk Németh GB = Guillaume Blanchet PH = Peter Hambäck JdA = Julie d'Arcier TR = Tomas Roslin Main supervisor: Dr. Ayco Tack, Department of Ecology, Environment and Plant Sciences, Stockholm University, Sweden Co-supervisor: Professor Peter Hambäck, Department of Ecology, Environment and Plant Sciences, Stockholm University, Sweden Contents Abstract ................................................................................................................. 4 1. Introduction .................................................................................................... 6 1.1. Community ecology and forces structuring communities 6 1.2. Plant-associated microbial communities 7 1.3. Forces structuring fungal communities 8 1.4. Oak-associated fungi and insects as model organisms 11 2. Aims of the thesis........................................................................................... 13 3. Methods ......................................................................................................... 15 3.1. Observational data 15 3.2. Heating experiment 16 3.3. Molecular methods 18 4. Insights .......................................................................................................... 20 4.1. Differential imprint of local environment and spatial processes on foliar and soil fungal communities (I) 20 4.2. Climate is more important than species interactions in defining the niches of cryptic powdery mildew species (II) 22 4.3. Climate warming and to lesser extent tree genotype shape foliar fungal communities (III) 23 4.4. Climate warming and tree genotype jointly affect tree phenology, fungal disease levels and insect density (IV) 24 5. Concluding remarks and future directions .................................................... 26 6. Svensk sammanfattning ................................................................................ 29 7. Acknowledgements ....................................................................................... 31 8. References ..................................................................................................... 34 Kappa Abstract Plants host a diverse community of microorganisms, which includes fungi, bacteria and archaea. Among these, fungi are highly diverse, and known to play a vital role in plant health and in regulation of the essential ecosystem functions. Nevertheless, we still lack a comprehensive understanding of the forces structuring plant-associated fungal communities in space and time. The main aim of this thesis was to decipher the drivers of the spatial patterns and temporal dynamics of plant-associated fungal communities. To this aim, I focused on Quercus robur and its associated fungal communities. Using a combination of observational and experimental studies, I assessed i) the distribution and drivers of the above- and belowground
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