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Fungal Diversity in a Transgenic Poplar Plantation and the Role of Ectomycorrhizal Fungi for Tree Performance Under

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Fungal Diversity in a Transgenic Poplar Plantation and the Role of Ectomycorrhizal Fungi for Tree Performance Under Fungal diversity in a transgenic poplar plantation and the role of ectomycorrhizal fungi for tree performance under field and controlled drought stress conditions Dissertation zur Erlangung des Doktorgrades der Mathematisch-Naturwissenschaftlichen Fakultät der Georg-August-Universität Göttingen Vorgelegt von Dipl. Biologin Lara Danielsen aus Flensburg Göttingen, Oktober 2012 Referent: Prof. Dr. Andrea Polle Koreferent: Prof. Dr. Stefan Scheu Tag der mündlichen Prüfung: 30. November 2012 Table of contents Table of Contents Summary………………………………………………………………………………………. V Zusammenfassung………………………………………………………………………….. VIII 1 Introduction…………………………………………………………………................... 1 1.1 Populus spp. as model organism …………………...…….…….………………… 2 1.2 Biodiversity and fungal community structure………….……….…………………. 2 1.3 Mycorrhizal fungi………………………………………………..…………………… 4 1.4 Functional traits of ECM fungi…………………………… ……………………….. 5 1.5 Research topics addressed in this thesis..……………………………………….. 6 1.6 References…………………………………………………………………………... 7 2 Fungal soil communities in a young transgenic poplar plantation form a rich reservoir for fungal root communities……………………………………………… 12 Abstract……………………………………………………………………………………. 13 2.1 Introduction………………………………………………………………………….. 14 2.2 Material and Methods...……...…………………………………………………….. 16 2.2.1 Plant material and study site…………………………………………………. 16 2.2.2 Sampling strategy……………...……………………………………………… 17 2.2.3 Soil analyses……………...…………………………………………………… 17 2.2.4 DNA extraction and quality check…………………………........................... 18 2.2.5 Amplicon generation and 454 pyrosequencing…….................................... 19 2.2.6 Bioinformatics and OUT clustering…………………………………………... 19 2.2.7 Morphotyping on root tips………………………………………………….….. 20 2.2.8 Cloning and sequencing of ectomycorrhizal species…………………….… 20 2.2.9 Data analyses…………………………...……………………………………... 20 2.3 Results……………………………………………………………………………….. 21 2.3.1 Fungal species richness and diversity in soil and roots…..…………….…. 21 2.3.2 Fungal community structure in different habitats and poplar genotypes…………………………………………………………………….... 23 2.3.3 Fungal family abundance and distribution across soil and root samples………………………………………………………………….…...... 25 2.3.4 Ecological groups in soil and root samples………………………………… 28 2.3.5 Dynamic of the ectomycorrhizal community on poplar roots……………... 29 2.4 Discussion…………………………………………………………………………... 30 2.4.1 Massive 454 pyrosequencing reveals surprisingly high fungal species I Table of contents richness in a young short rotation plantation……………………………….. 30 2.4.2 Roots and soil constitute distinct ecological fungal biomes………….…… 30 2.4.3 Deep sequencing reveals host effects on the priority of ECM root colonization………………………………………………………………….…. 32 2.4.4 Transgenic poplars with suppressed CAD activity do not affect soil, root or ECM communities ...………………….…………...................................... 33 2.5 Conclusions……………………………………………………………………….… 34 2.6 References………………………………………………………………….…..…... 35 2.7 Supporting Information...……………………...…………………………….….….. 39 3 Biomass production of genetically modified clones of Populus × canescens grown in short rotation coppices in relation to ectomycorrhizal colonization and diversity………………...................................................................................... 62 Abstract……………………………………………………………………………………. 63 3.1 Introduction……………………………………………………………………..…… 64 3.2 Material and Methods……………...………………………………………….…… 65 3.2.1 Plant material and field site…………………………...…………………….… 65 3.2.2 Sampling of soil cores for analyses of roots and soil……………….…….... 66 3.2.3 Fungal soil communities analyzed by denaturing gradient gel electrophoresis (DGGE)……………………….……………………………... 67 3.2.4 Free amino acids, nitrate and ammonium in soil samples…………....…... 68 3.2.5 Ectomycorrhizal colonization and morphotyping………..…………...…..…. 68 3.2.6 Sanger sequencing of the fungal ITS region…………………………….….. 69 3.2.7 Stem heights and biomass…………………………………………………… 69 3.2.8 Nutrient element and δ13C analyses ……………………………………….… 70 3.2.9 Statistical analyses………………………………………..………………....... 70 3.3 Results…………………………………………………………………………….… 71 3.3.1 Absence of fungal clusters and nutrient patches in the soil of a poplar plantation………………………………...………………………………..…..… 71 3.3.2 Ectomycorrhizal colonization show temporal dynamics and genotype but not gene specific effects in GM poplars….…….………………………..….. 73 3.3.3 Early genotype specific variation of growth is related to stem N concentrations and ectomycorrhizal root colonization…..………….…….... 77 3.4 Discussion………………………………………………………………..…………. 81 3.4.1 Influence of gene modification on mycorrhizal colonization and community structure…………………………………..…………………........ 81 3.4.2 The link between ECM colonization and diversity and tpoplar II Table of contents dendromass and nutrient status …………………………………………….. 82 3.5 Conclusion…………………………...……………………………………...…….. 84 3.6 References……………………………………………………………………...…. 85 3.7 Supplementary data…………………………………...………………………..... 92 4 Paxillus involutus improves poplar nutrition and foster an early dehydration avoidance strategy in Populus × canescens under drought conditions……………………………...………………………………………………. 105 4.1 Introduction………………………………………...………………………….….. 106 4.2 Material & Methods…………………………...………………………………..… 107 4.2.1 Plant material and cultivation of fungi………………………………….…. 107 4.2.2 Mycorrhizal inoculation and plant growth conditions………………….… 108 4.2.3 Drought stress and harvest time points……………………………….….. 109 4.2.4 Physiological measurements………………………………………....…… 109 4.2.5 Harvest………………………………………………………………....……. 110 4.2.6 Determination of mycorrhizal colonization of root tips……………....….. 110 4.2.7 Quantitative Real Time PCR (qRT-PCR)………………………………… 110 4.2.8 Element analysis……………………………………………………………. 112 4.2.9 Carbohydrate analysis……………………………………………………... 113 4.2.10 Osmolyte content………………………………………………..…..…… 113 4.2.11 Statistical analysis…………………………………………………….….. 114 4.3 Results……………………………………………………………………….…… 115 4.3.1 Effect of drought and mycorrhiza on soil water content and physiological parameters……………………………………………………………….…. 115 4.3.2 Mycorrhizal colonization and vitality index………………………………. 118 4.3.3 Effect of drought and mycorrhiza on growth performance……………... 119 4.3.4 Effect of drought and mycorrhiza on water status………………………. 123 4.3.5 Effect of drought and mycorrhiza on carbohydrates and osmolality……………………………………………………………….…… 124 4.3.6 Effect of drought and mycorrhiza on nutrient status of plants……….…. 127 4.3.7 Effect of drought and mycorrhiza on expression of stress related genes……………………………………………………………………….... 132 4.4 Discussion………………………………………………………………………... 132 4.4.1 Paxillus involutus affects the water status of P. × canescens under drought stress conditions………………………………………………….. 132 4.4.2 Paxillus involutus affects physiology and nutrition of P. × canescens under drought stress conditions…………………..…………………….... 135 III Table of contents 4.5 Conclusion………………………………………………………………….……. 137 4.6 References…………………………………………………………………..……. 138 4.7 Supplemental Data………………………..……………………...………..…….. 143 5 Overall Conclusion………….…………...……………………………………..…… 146 Acknowledgments……………………….……….……………………………………… 150 Curriculum vitae……………………………………………………………………...….. 152 Eidesstattliche Erklärung………………………………………………………………. 154 IV Summary Summary The w orldw ide increasing energy demand comes along w ith diminishing fossil fuel resources. Thus, research on alternative bioenergy sources is urgently needed. Poplars w ith optimized properties for bioethanol production are available and have to be tested for sustainable usage in field experiments. It is an important issue to study possible environmental impacts of transgenic poplars on the biodiversity of associated organisms. Fungi play an important role in ecosystem functioning and information on their composition in the soil and on poplar roots of biomass plantations is rare. Poplars gain nutritional benefits from ectomycorrhizal (ECM) symbiosis and there is emerging evidence that ECM fungi could lead to enhanced water stress resistance in their host plants. The role of ECM symbiosis for poplar productivity and stress resistance is an important topic of research, especially in biomass plantations. In this w ork, fungal biodiversity in soil and roots of a poplar plantation w ere analyzed. In addition the role of ECM fungal diversity for poplar productivity and the potential role of ECM in amelioration of drought resistance in poplar w ere investigated. The follow ing research goals w ere pursued: (I) The fungal communities in a short rotation plantation w ith P. × canescens w ildtype (WT) and tw o transgenic lines w ith suppressed cinnamyl alcohol dehydrogenase (CAD) activity were investigated to elucidate (1) if the fungal composition in the soil served as a large species-rich reservoir for the establishment of the fungal composition in roots of WT and the tw o transgenic lines and (2) if the fungal community in soil and roots was affected by the modification of the two transgenic lines in comparison to the WT. To investigate the soil/root fungal communities of WT and tw o transgenic CAD poplar lines, the pyrosequencing approach w as used and to detect temporal dynamics of ECM communities on roots pyrosequencing w as combined w ith the morphotyping/ Sanger- sequencing technique. Estimated species richness was highest in soil and decreased in the habitat order soil > root > root associated ECM. It w as also shown that the soil serves as a fungal-rich
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