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A dual function of SnRK2 kinases in the regulation of SnRK1 and plant growth

Abstract

Adverse environmental conditions trigger responses in plants that promote stress tolerance and survival at the expense of growth1. However, little is known of how stress signalling pathways interact with each other and with growth regulatory components to balance growth and stress responses. Here, we show that plant growth is largely regulated by the interplay between the evolutionarily conserved energy-sensing SNF1-related protein kinase 1 (SnRK1) protein kinase and the abscisic acid (ABA) phytohormone pathway. While SnRK2 kinases are main drivers of ABA-triggered stress responses, we uncover an unexpected growth-promoting function of these kinases in the absence of ABA as repressors of SnRK1. Sequestration of SnRK1 by SnRK2-containing complexes inhibits SnRK1 signalling, thereby allowing target of rapamycin (TOR) activity and growth under optimal conditions. On the other hand, these complexes are essential for releasing and activating SnRK1 in response to ABA, leading to the inhibition of TOR and growth under stress. This dual regulation of SnRK1 by SnRK2 kinases couples growth control with environmental factors typical for the terrestrial habitat and is likely to have been critical for the water-to-land transition of plants.

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Fig. 1: SnRK1 sesquiα2 mutants show defective growth repression in ABA.
Fig. 2: SnRK2s interact with SnRK1 in a PP2CA-dependent manner.
Fig. 3: SnRK2s regulate TOR and growth via SnRK1.
Fig. 4: A dual function of SnRK2 kinases in the regulation of SnRK1 and growth.

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Data availability

All data supporting the findings of this study are available in the main text or the Supplementary Information. Additional data related to this study are available from the corresponding author upon request. All biological materials used in this study are available from the corresponding author on reasonable request. Source data are provided with this paper.

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Acknowledgements

We thank J.-K. Zhu for the snrk2 mutants, M. Bennett for the SnRK2.2-GFP line, C. Koncz for the SnRK1-GFP line, X. Li for the SnRK2.3-FLAG OE line, J. Schroeder for the GFP-His-FLAG and SnRK2.6-His-FLAG OE lines, C. Mackintosh for the TPS5 antibody and the Nottingham Arabidopsis stock centre for T-DNA mutant seeds. The IGC Plant Facility (Vera Nunes) is thanked for excellent plant care. This work was supported by Fundação para a Ciência e a Tecnologia through the R&D Units UIDB/04551/2020 (GREEN-IT—Bioresources for Sustainability) and UID/MAR/04292/2019, FCT project nos. PTDC/BIA-PLA/7143/2014, LISBOA-01-0145-FEDER-028128 and PTDC/BIA-BID/32347/2017, and FCT fellowships/contract nos. SFRH/BD/122736/2016 (M.A.), SFRH/BPD/109336/2015 (A.C.), PD/BD/150239/2019 (D.R.B.), and IF/00804/2013 (E.B.G.). Work in P.L.R.’s laboratory was funded by MCIU grant no. BIO2017-82503-R. C.M. thanks the LabEx Paris Saclay Plant Sciences-SPS (ANR-10-LABX-040-SPS) for support. B.B.P. was funded by Programa VALi+d GVA APOSTD/2017/039. This project has received funding from the European Union Horizon 2020 research and innovation programme (grant agreement no. 867426—ABA-GrowthBalance—H2020-WF-2018-2020/H2020-WF-01-2018, awarded to B.B.P.). This work is dedicated to the memory of our beloved friend and colleague Américo Rodrigues.

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Authors

Contributions

B.B.P., M.A. and C.V. designed and performed experiments, and analysed and interpreted data. L.J.F. performed and analysed the root phenotyping experiments in low light and AZD. A.C. generated and characterized molecularly the sesquiα2 mutant lines and provided strong conceptual support. D.R.B. performed protein immunoprecipitation from protoplasts and in vitro kinase assays. A.R. contributed to the general conception of the project and the initial exploratory experiments. C.M. contributed the phospho-RPS6 antibody and expertise on molecular and plant phenotype assays related to TOR activity. P.L.R. contributed tools and expertise on PP2C–SnRK2 interactions and ABA signalling, and actively supported the conceptual work. B.B.P. and E.B.G. prepared the figures and wrote the manuscript. E.B.G. conceived the project and directed and supervised all of the research. All authors read and approved the manuscript.

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Correspondence to Elena Baena-González.

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Belda-Palazón, B., Adamo, M., Valerio, C. et al. A dual function of SnRK2 kinases in the regulation of SnRK1 and plant growth. Nat. Plants 6, 1345–1353 (2020). https://doi.org/10.1038/s41477-020-00778-w

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