OPEN STOMATA1 phosphorylates CYCLIC NUCLEOTIDE-GATED CHANNELs to trigger Ca2+ signaling for ABA-induced stomatal closure in Arabidopsis

Yang Yang; Yan-Qiu Tan; Xinyong Wang; Jia-Jun Li; Bo-Ya Du; Meijun Zhu; Pengcheng Wang; Yong-Fei Wang

doi:10.1093/plcell/koae073

OPEN STOMATA1 phosphorylates CYCLIC NUCLEOTIDE-GATED CHANNELs to trigger Ca2+ signaling for ABA-induced stomatal closure in Arabidopsis

Plant Cell. 2024 Mar 5:koae073. doi: 10.1093/plcell/koae073. Online ahead of print.

Authors

Yang Yang^{1

2}, Yan-Qiu Tan¹, Xinyong Wang^{1

2}, Jia-Jun Li^{1

2}, Bo-Ya Du^{1

2}, Meijun Zhu^{1

2}, Pengcheng Wang³, Yong-Fei Wang^{1

2}

Affiliations

¹ National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
² University of Chinese Academy of Sciences, Shanghai 200032, China.
³ Institute of Advanced Biotechnology and School of Life Sciences, Southern University of Science and Technology, Shenzhen 518055, China.

PMID: 38442317
DOI: 10.1093/plcell/koae073

Abstract

Multiple cyclic nucleotide-gated channels (CNGCs) are abscisic acid (ABA)-activated Ca2+ channels in Arabidopsis (Arabidopsis thaliana) guard cells. In particular, CNGC5, CNGC6, CNGC9, and CNGC12 are essential for ABA-specific cytosolic Ca2+ signaling and stomatal movements. However, the mechanisms underlying ABA-mediated regulation of CNGCs and Ca2+ signaling are still unknown. In this study, we identified the Ca2+-independent protein kinase OPEN STOMATA1 (OST1) as a CNGC activator in Arabidopsis. OST1-targeted phosphorylation sites were identified in CNGC5, CNGC6, CNGC9 and CNGC12. These CNGCs were strongly inhibited by Ser-to-Ala mutations and fully activated by Ser-to-Asp mutations at the OST1-targeted sites. The overexpression of individual inactive CNGCs (iCNGCs) under the UBIQUITIN10 promoter in wild-type Arabidopsis conferred a strong dominant-negative-like ABA-insensitive stomatal closure phenotype. In contrast, expressing active CNGCs (aCNGCs) under their respective native promoters in the cngc5-1 cngc6-2 cngc9-1 cngc12-1 quadruple mutant fully restored ABA-activated cytosolic Ca2+ oscillations and Ca2+ currents in guard cells, and rescued the ABA-insensitive stomatal movement mutant phenotypes. Thus, we uncovered that ABA elicits cytosolic Ca2+ signaling via an OST1-CNGC module, in which OST1 functions as a convergence point of the Ca2+-dependent and -independent pathways in Arabidopsis guard cells.

Keywords: ABA; Arabidopsis; CNGCs; OST1; stomata closure; upstream regulator.