Dissection of general and specific regulatory mechanism of sulfur metabolism in Arabidopsis thaliana
Final Report Abstract
Sulfur is an essential macronutrient for plants. Its deficiency in agricultural European soils is becoming an increasingly urgent issue, mainly due to successful clean-air legislation drastically reducing atmospheric sulfur deposition. This emerging challenge highlights the need for a deeper understanding of how plants respond to mineral nutrient limitations at the molecular level. In contrast to most animals, plants are able to respond to environmental challenges such as pathogen infections and abiotic stress by undergoing significant developmental changes. This developmental plasticity allows them to acclimate and survive under stress. Under prolonged sulfur nutrient deprivation plants arrest the growth of the shoot and transfer resources to help the root finding new sulfate in the soil. This goes along with massive shifts of biomass ratios between shoot and root, but the molecular and cellular mechanism of this important ability were unknown. This project revealed that a central sensing kinase, target of rapamycin (TOR), that is conserved in all eukaryotes, is differentially regulated between shoot and root cells during sulfur deficiency. We found that TOR probably receives upstream signals from another general sensor kinase (SnRK1), but also primary metabolites. Repression of TOR in shoots was essential for induction of autophagy (‘self-eating’, a process that recycles cell components and provides sugars that are exported to the roots. The sugar supply keeps TOR active, triggering downstream processes relevant for growth, including suppression of autophagy and root apical meristem activity, thus resulting in maintained root extension during sulfur deficiency. The shoot was shown to be in control of transport processes and root development using grafting of shoot and root of mutant plants with altered sulfur metabolism. The intermediate of cysteine synthesis, O-acetylserine, was not only integral part of the canonical sulfur deficiency response, but found to be linked to regulation of photosynthesis. In summary, the links between mineral deficiency of sulfur and TOR regulation contribute to our understanding of plant acclimation to their environment.
Publications
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Information on nutrients and stress is integrated into specific growth responses. R. Hell, Conference of the Japanese Society for Plant Physiology, Nagoya 2019
R. Hell
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The role of autophagy for nutrient stress-induced developmental plasticity, M. Wirtz, 1. International Conference on Plant Proteostasis, Freiburg University, Germany, 2019
M. Wirtz
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TOR kinase tunes autophagy and meristem activity for nutrient stress-induced developmental plasticity. R. Hell, Meeting of the American Society of Plant Biology, San José 2019
R. Hell
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TOR – a sensor kinase controlling cell proliferation, translation and nutrient recycling, M. Wirtz, Seminar Series UoG, University of Göttingen, Germany, 2019
M. Wirtz
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A molecular switch in sulfur metabolism to reduce arsenic and enrich selenium in rice grain. Nature Communications, 12(1).
Sun, Sheng-Kai; Xu, Xuejie; Tang, Zhong; Tang, Zhu; Huang, Xin-Yuan; Wirtz, Markus; Hell, Rüdiger & Zhao, Fang-Jie
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Metabolite Profiling in Arabidopsisthaliana with Moderately Impaired Photorespiration Reveals Novel Metabolic Links and Compensatory Mechanisms of Photorespiration. Metabolites, 11(6), 391.
Timm, Stefan; Nunes-Nesi, Adriano; Florian, Alexandra; Eisenhut, Marion; Morgenthal, Katja; Wirtz, Markus; Hell, Rüdiger; Weckwerth, Wolfram; Hagemann, Martin; Fernie, Alisdair R. & Bauwe, Hermann
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Micrografting Provides Evidence for Systemic Regulation of Sulfur Metabolism between Shoot and Root. Plants, 10(8), 1729.
Forieri, Ilaria; Aref, Rasha; Wirtz, Markus & Hell, Rüdiger
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An unexpected function of the highly conserved SERAT3 isoforms in the cytosol of Arabidopsis, W. Leemhuis, 12th International Sulfur Workshop, London, Canada, 2022
W. Leemhuis
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Novel links between energy sensor kinases and the assimilatory sulfate reduction pathway, M. Wirtz, 12th International Sulfur Workshop, London, Canada, 2022
M. Wirtz
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The plant TOR kinase tunes autophagy and meristem activity for nutrient stress-induced developmental plasticity. The Plant Cell, 34(10), 3814-3829.
Dong, Yihan; Aref, Rasha; Forieri, Ilaria; Schiel, David; Leemhuis, Wiebke; Meyer, Christian; Hell, Ruediger & Wirtz, Markus
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Why sulfur? A Roadtrip Through the World of Sulfur Metabolism. R. Hell, 35. Conference on Molecular Biology of Plants, Hennef 2022.
R. Hell
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Differential modulation of Target of Rapamycin activity under single and combined iron and sulfur deficiency in tomato plants. The Plant Journal, 115(1), 127-138.
Coppa, Eleonora; Vigani, Gianpiero; Aref, Rasha; Savatin, Daniel; Bigini, Valentina; Hell, Ruediger & Astolfi, Stefania
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Dynamic association of the plastid localized cysteine synthase complex is vital for efficient cysteine production, photosynthesis, and granal thylakoid formation in transgenic tobacco. Journal of Experimental Botany, 74(11), 3379-3394.
Wirtz, Markus; Leemhuis, Wiebke & Hell, Ruediger
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Molecular insights into sulfate-induced stomatal closure in response to environmental stimuli, M. Wirtz, Seminar Series of CEPLAS Cluster, University of Cologne, Germany, 2023
M. Wirtz
