CPK1 activates CNGCs through phosphorylation for Ca2+ signaling to promote root hair growth in Arabidopsis

Abstract Cyclic nucleotide-gated channel 5 (CNGC5), CNGC6, and CNGC9 (CNGC5/6/9 for simplicity) control Arabidopsis root hair (RH) growth by mediating the influx of external Ca2+ to establish and maintain a sharp cytosolic Ca2+ gradient at RH tips. However, the underlying mechanisms for the regulati...

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Main Authors: Meijun Zhu, Bo-Ya Du, Yan-Qiu Tan, Yang Yang, Yang Zhang, Yong-Fei Wang
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-56008-4
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author Meijun Zhu
Bo-Ya Du
Yan-Qiu Tan
Yang Yang
Yang Zhang
Yong-Fei Wang
author_facet Meijun Zhu
Bo-Ya Du
Yan-Qiu Tan
Yang Yang
Yang Zhang
Yong-Fei Wang
author_sort Meijun Zhu
collection DOAJ
description Abstract Cyclic nucleotide-gated channel 5 (CNGC5), CNGC6, and CNGC9 (CNGC5/6/9 for simplicity) control Arabidopsis root hair (RH) growth by mediating the influx of external Ca2+ to establish and maintain a sharp cytosolic Ca2+ gradient at RH tips. However, the underlying mechanisms for the regulation of CNGCs remain unknown. We report here that calcium dependent protein kinase 1 (CPK1) directly activates CNGC5/6/9 to promote Arabidopsis RH growth. The loss-of-function mutants cpk1-1, cpk1-2, cngc5-1 cngc6-2 cngc9-1 (shrh1/short root hair 1), and cpk1 shrh1 show similar RH phenotypes, including shorter RHs, more RH branching, and dramatically attenuated cytosolic Ca2+ gradients at RH tips. The main CPK1-target sites are identified as Ser20, Ser27, and Ser26 for CNGC5/6/9, respectively, and the corresponding alanine substitution mutants fail to rescue RH growth in shrh1 and cpk1-1, while phospho-mimic versions restore the cytosolic Ca2+ gradient at RH apex and rescue the RH phenotypes in the same Arabidopsis mutants. Thus we discover the CPK1-CNGC modules essential for the Ca2+ signaling regulation and RH growth in Arabidopsis.
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institution Kabale University
issn 2041-1723
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publishDate 2025-01-01
publisher Nature Portfolio
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spelling doaj-art-e334407776414be4952e5329fb3992632025-01-19T12:32:05ZengNature PortfolioNature Communications2041-17232025-01-0116112010.1038/s41467-025-56008-4CPK1 activates CNGCs through phosphorylation for Ca2+ signaling to promote root hair growth in ArabidopsisMeijun Zhu0Bo-Ya Du1Yan-Qiu Tan2Yang Yang3Yang Zhang4Yong-Fei Wang5State Key Laboratory of Plant Trait Design, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences (CAS)State Key Laboratory of Plant Trait Design, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences (CAS)State Key Laboratory of Plant Trait Design, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences (CAS)State Key Laboratory of Plant Trait Design, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences (CAS)State Key Laboratory of Plant Trait Design, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences (CAS)State Key Laboratory of Plant Trait Design, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences (CAS)Abstract Cyclic nucleotide-gated channel 5 (CNGC5), CNGC6, and CNGC9 (CNGC5/6/9 for simplicity) control Arabidopsis root hair (RH) growth by mediating the influx of external Ca2+ to establish and maintain a sharp cytosolic Ca2+ gradient at RH tips. However, the underlying mechanisms for the regulation of CNGCs remain unknown. We report here that calcium dependent protein kinase 1 (CPK1) directly activates CNGC5/6/9 to promote Arabidopsis RH growth. The loss-of-function mutants cpk1-1, cpk1-2, cngc5-1 cngc6-2 cngc9-1 (shrh1/short root hair 1), and cpk1 shrh1 show similar RH phenotypes, including shorter RHs, more RH branching, and dramatically attenuated cytosolic Ca2+ gradients at RH tips. The main CPK1-target sites are identified as Ser20, Ser27, and Ser26 for CNGC5/6/9, respectively, and the corresponding alanine substitution mutants fail to rescue RH growth in shrh1 and cpk1-1, while phospho-mimic versions restore the cytosolic Ca2+ gradient at RH apex and rescue the RH phenotypes in the same Arabidopsis mutants. Thus we discover the CPK1-CNGC modules essential for the Ca2+ signaling regulation and RH growth in Arabidopsis.https://doi.org/10.1038/s41467-025-56008-4
spellingShingle Meijun Zhu
Bo-Ya Du
Yan-Qiu Tan
Yang Yang
Yang Zhang
Yong-Fei Wang
CPK1 activates CNGCs through phosphorylation for Ca2+ signaling to promote root hair growth in Arabidopsis
Nature Communications
title CPK1 activates CNGCs through phosphorylation for Ca2+ signaling to promote root hair growth in Arabidopsis
title_full CPK1 activates CNGCs through phosphorylation for Ca2+ signaling to promote root hair growth in Arabidopsis
title_fullStr CPK1 activates CNGCs through phosphorylation for Ca2+ signaling to promote root hair growth in Arabidopsis
title_full_unstemmed CPK1 activates CNGCs through phosphorylation for Ca2+ signaling to promote root hair growth in Arabidopsis
title_short CPK1 activates CNGCs through phosphorylation for Ca2+ signaling to promote root hair growth in Arabidopsis
title_sort cpk1 activates cngcs through phosphorylation for ca2 signaling to promote root hair growth in arabidopsis
url https://doi.org/10.1038/s41467-025-56008-4
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