Differential phosphorylation of Ca2+-permeable channel CYCLIC NUCLEOTIDE–GATED CHANNEL20 modulates calcium-mediated freezing tolerance in Arabidopsis (2024)

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Yue Peng

State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University

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Beijing 100193

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China

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Yuhang Ming

State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University

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Beijing 100193

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China

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Bochen Jiang

State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University

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Beijing 100193

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China

Present address: Department of Chemistry, The University of Chicago, Chicago, IL 60637, USA.

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Xiuyue Zhang

State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University

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Beijing 100193

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China

Present address: State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.

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Diyi Fu

State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University

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Beijing 100193

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China

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Qihong Lin

State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University

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Beijing 100193

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China

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Xiaoyan Zhang

State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University

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Beijing 100193

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China

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Yi Wang

State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University

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Beijing 100193

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China

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Yiting Shi

State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University

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Beijing 100193

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China

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Zhizhong Gong

State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University

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Beijing 100193

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China

School of Life Science, Institute of Life Science and Green Development, Hebei University

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Baoding, Hebei 071002

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China

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Yanglin Ding

State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University

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Beijing 100193

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China

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Shuhua Yang

State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University

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Beijing 100193

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China

Author for correspondence: yangshuhua@cau.edu.cn

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The Plant Cell, Volume 36, Issue 10, October 2024, Pages 4356–4371, https://doi.org/10.1093/plcell/koae177

Published:

14 June 2024

Article history

Received:

29 April 2024

Accepted:

07 June 2024

Published:

14 June 2024

Corrected and typeset:

22 July 2024

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    Yue Peng, Yuhang Ming, Bochen Jiang, Xiuyue Zhang, Diyi Fu, Qihong Lin, Xiaoyan Zhang, Yi Wang, Yiting Shi, Zhizhong Gong, Yanglin Ding, Shuhua Yang, Differential phosphorylation of Ca2+-permeable channel CYCLIC NUCLEOTIDE–GATED CHANNEL20 modulates calcium-mediated freezing tolerance in Arabidopsis, The Plant Cell, Volume 36, Issue 10, October 2024, Pages 4356–4371, https://doi.org/10.1093/plcell/koae177

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Abstract

Plants respond to cold stress at multiple levels, including increasing cytosolic calcium (Ca2+) influx and triggering the expression of cold-responsive genes. In this study, we show that the Ca2+-permeable channel CYCLIC NUCLEOTIDE–GATED CHANNEL20 (CNGC20) positively regulates freezing tolerance in Arabidopsis (Arabidopsis thaliana) by mediating cold-induced Ca2+ influx. Moreover, we demonstrate that the leucine-rich repeat receptor-like kinase PLANT PEPTIDE CONTAINING SULFATED TYROSINE1 RECEPTOR (PSY1R) is activated by cold, phosphorylating and enhancing the activity of CNGC20. The psy1r mutant exhibits decreased cold-evoked Ca2+ influx and freezing tolerance. Conversely, COLD-RESPONSIVE PROTEIN KINASE1 (CRPK1), a protein kinase that negatively regulates cold signaling, phosphorylates and facilitates the degradation of CNGC20 under prolonged periods of cold treatment, thereby attenuating freezing tolerance. This study thus identifies PSY1R and CRPK1 kinases that regulate CNGC20 activity and stability, respectively, thereby antagonistically modulating freezing tolerance in plants.

© The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.

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