Pappelkommunikation mit der Umwelt
Zusammenfassung der Projektergebnisse
VOCs released by the ectomycorrhizal fungus L. bicolor induce lateral root (LR) formation in the host tree P. x canescens and in the non-host Arabidopsis thaliana. However, it is still unclear which receptors and signaling pathways in plants are involved in L. bicolor-induced LR formation. In the present project, we investigated the downstream molecular responses to L. biolor VOCs in A. thaliana and Populus x canescens. In both species, we characterized at the transcriptome, metabolome, and proteome levels the temporal changes following exposure to volatile terpenes and to in vivo emissions of L. bicolor. Phenotypically, we investigated LR formation in poplar and Arabidopsis roots and complementary "priming" effects of fungal VOCs on induced immunity to a biotrophic pathogen in Arabidopsis. Experiments with different co-cultivation times with fungal mycelium and plants and different amounts of mycelium (1 to 4 plugs) showed that co-cultivation with one fungal plug was sufficient to induce enhanced LR formation. Two fungal plugs resulted in further small increments in LR densities and were also sufficient for the induction of plant systemic immunity (ISR) in Arabidopsis rosettes. Two-day exposure to L. bicolor VOCs were enough to induce LR formation. These results suggest a dose- and time-dependent response in signal transduction. At the level of L. bicolor, we identified several terpene synthases and functionally characterized them in E. coli and yeast. Experiments with poplar showed that (-)-thujopsene exposure to roots stimulated LR formation, whereas ß-caryophyllene, another sesquiterpene did not. On the other hand, ß-caryophyllene induced jasmonate-dependent resistance in Arabidopsis rosettes, an effect that was not found in response to (-)-thujopsene. To gain deeper insights into VOC-induced responses, we used mutant lines with potential functions in LR formation associated with ROS homeostasis (per45 and per59), strigolactone biosynthesis/ signaling (max2 and max4) and germination (germin-like 3) testing the influence of L. bicolor VOCs on LR density. None of the mutants tested showed a different phenotype compared to wild-type plants when exposed to fungal VOCs. However, experiments with an NADPH oxidase inhibitor and in situ staining for ROS showed that ROS play a role in the signaling of fungal VOCs by roots. Furthermore, we investigated a possible involvement of cysteine-rich receptor-like kinases (CRKs) in signal transduction contributing to LR formation. This gene family plays a role in stress, growth, and development. Within a crk knockout library of 42 lines, we found no conclusive results for role of CRK in VOC perception. Using transcriptome analysis, we identified a consistently down-regulated gene with unknown function in Arabidopsis and its homolog in poplar. We used forward and reverse genetic approaches to functionally characterize the role of this gene in LR formation. This work is still ongoing. Transcriptome data also indicated involvement of the phytohormone abscisic acid (ABA). Exposure of ABA mutant lines to L. bicolor VOCs resulted in a reduced LR response in aao3 and pyl8-1 and an enhanced response in aba2 compared with wild type. This is strong evidence that ABA was involved in the perception or signaling of VOCs in plants. Overall, we have shown that LR formation in response to VOCs from L. bicolor in planta is a complex process involving previously unknown proteins, ROS and ABA signaling. Since different sequiterpenes, as well as the complex in vivo VOC pattern (containing more VOCs beside sesquiterpenes) of L. bicolor led to different physiological responses in different tissues, our results suggest that distinct VOCs recruit distinct response mechanisms. Therefore, the quest for receptors has to be expanded from one to multiple compounds.
Projektbezogene Publikationen (Auswahl)
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(2016) Belowground communication: impacts of volatile organic compounds (VOCs) from soil fungi on other soil-inhabiting organisms. Applied Microbiology and Biotechnology 100: 8651-8665
Werner S, Polle A, Brinkmann N
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(2018) Mycorrhiza-triggered transcriptomic and metabolomic networks impinge on herbivore fitness. Plant Physiology 176: 2639-2656
Kaling M, Schmidt A, Moritz F, Rosenkranz M, Witting M, Kasper K, Janz D, Schmitt-Kopplin P, Schnitzler JP, Polle A
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(2019) Contribution of Volatile Signals for Belowground Plant-Microbe Interactions. PhD Thesis, Albert-Ludwigs-Universität Freiburg
Miloradvic van Doorn, Maja
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(2020) Characterization of the Chemical Diversity of Fungal Volatile Organic Compound Emissions Across Taxa and Lifestyles. PhD Thesis, Albert-Ludwigs-Universität Freiburg
Guo, Yuan
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(2020) Down-Stream molecular Responses to Volatile Signaling in Roots. PhD Thesis, University of Goettingen
Jakobi, Mareike
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(2020) Local responses and systemic induced resistance mediated by ectomycorrhizal fungi. Frontiers in Plant Science 11: 590063
Dreischhoff S, Das IS, Jakobi M, Kasper K, Polle A
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Root isoprene formation alters lateral root development. Plant Cell and Environment 43: 2207–2223
Miloradovic van Doorn M, Merl-Pham J, Ghirardo A, Bernhardt J, Polle A, Schnitzler JP, Rosenkranz M
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(2021): Isoprene confers salicylic acid-associated plant immunity. Plant Cell and Environment 44: 1151-1164
Frank L, Wenig M, Ghirardo G, van der Krol A, Vlot AC, Schnitzler JP, Rosenkranz M
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Volatile chemical diversity across fungal taxa and lifestyles. Communications Biology 4: 673
Guo Y, Jud W, Weikl F, Ghirardo A, Junker RR, Polle A, Benz JP, Pritsch K, Schnitzler JP, Rosenkranz M
