Light-induced stomatal opening requires phosphorylation of the C-terminal autoinhibitory domain of plasma membrane H+-ATPase
Abstract Plasma membrane H+-ATPase provides the driving force for light-induced stomatal opening. However, the mechanisms underlying the regulation of its activity remain unclear. Here, we show that the phosphorylation of two Thr residues in the C-terminal autoinhibitory domain is crucial for H+-ATP...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-02-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-45236-9 |
| _version_ | 1797274017105707008 |
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| author | Saashia Fuji Shota Yamauchi Naoyuki Sugiyama Takayuki Kohchi Ryuichi Nishihama Ken-ichiro Shimazaki Atsushi Takemiya |
| author_facet | Saashia Fuji Shota Yamauchi Naoyuki Sugiyama Takayuki Kohchi Ryuichi Nishihama Ken-ichiro Shimazaki Atsushi Takemiya |
| author_sort | Saashia Fuji |
| collection | DOAJ |
| description | Abstract Plasma membrane H+-ATPase provides the driving force for light-induced stomatal opening. However, the mechanisms underlying the regulation of its activity remain unclear. Here, we show that the phosphorylation of two Thr residues in the C-terminal autoinhibitory domain is crucial for H+-ATPase activation and stomatal opening in Arabidopsis thaliana. Using phosphoproteome analysis, we show that blue light induces the phosphorylation of Thr-881 within the C-terminal region I, in addition to penultimate Thr-948 in AUTOINHIBITED H+-ATPASE 1 (AHA1). Based on site-directed mutagenesis experiments, phosphorylation of both Thr residues is essential for H+ pumping and stomatal opening in response to blue light. Thr-948 phosphorylation is a prerequisite for Thr-881 phosphorylation by blue light. Additionally, red light-driven guard cell photosynthesis induces Thr-881 phosphorylation, possibly contributing to red light-dependent stomatal opening. Our findings provide mechanistic insights into H+-ATPase activation that exploits the ion transport across the plasma membrane and light signalling network in guard cells. |
| first_indexed | 2024-03-07T14:52:22Z |
| format | Article |
| id | doaj.art-3a3bc79e042140bcacc8dfb4b70d3c7a |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-07T14:52:22Z |
| publishDate | 2024-02-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-3a3bc79e042140bcacc8dfb4b70d3c7a2024-03-05T19:37:22ZengNature PortfolioNature Communications2041-17232024-02-0115111310.1038/s41467-024-45236-9Light-induced stomatal opening requires phosphorylation of the C-terminal autoinhibitory domain of plasma membrane H+-ATPaseSaashia Fuji0Shota Yamauchi1Naoyuki Sugiyama2Takayuki Kohchi3Ryuichi Nishihama4Ken-ichiro Shimazaki5Atsushi Takemiya6Department of Biology, Graduate School of Sciences and Technology for Innovation, Yamaguchi UniversityDepartment of Biology, Graduate School of Sciences and Technology for Innovation, Yamaguchi UniversityDepartment of Molecular & Cellular BioAnalysis, Graduate School of Pharmaceutical Sciences, Kyoto UniversityGraduate School of Biostudies, Kyoto UniversityGraduate School of Biostudies, Kyoto UniversityDepartment of Biology, Faculty of Science, Kyushu UniversityDepartment of Biology, Graduate School of Sciences and Technology for Innovation, Yamaguchi UniversityAbstract Plasma membrane H+-ATPase provides the driving force for light-induced stomatal opening. However, the mechanisms underlying the regulation of its activity remain unclear. Here, we show that the phosphorylation of two Thr residues in the C-terminal autoinhibitory domain is crucial for H+-ATPase activation and stomatal opening in Arabidopsis thaliana. Using phosphoproteome analysis, we show that blue light induces the phosphorylation of Thr-881 within the C-terminal region I, in addition to penultimate Thr-948 in AUTOINHIBITED H+-ATPASE 1 (AHA1). Based on site-directed mutagenesis experiments, phosphorylation of both Thr residues is essential for H+ pumping and stomatal opening in response to blue light. Thr-948 phosphorylation is a prerequisite for Thr-881 phosphorylation by blue light. Additionally, red light-driven guard cell photosynthesis induces Thr-881 phosphorylation, possibly contributing to red light-dependent stomatal opening. Our findings provide mechanistic insights into H+-ATPase activation that exploits the ion transport across the plasma membrane and light signalling network in guard cells.https://doi.org/10.1038/s41467-024-45236-9 |
| spellingShingle | Saashia Fuji Shota Yamauchi Naoyuki Sugiyama Takayuki Kohchi Ryuichi Nishihama Ken-ichiro Shimazaki Atsushi Takemiya Light-induced stomatal opening requires phosphorylation of the C-terminal autoinhibitory domain of plasma membrane H+-ATPase Nature Communications |
| title | Light-induced stomatal opening requires phosphorylation of the C-terminal autoinhibitory domain of plasma membrane H+-ATPase |
| title_full | Light-induced stomatal opening requires phosphorylation of the C-terminal autoinhibitory domain of plasma membrane H+-ATPase |
| title_fullStr | Light-induced stomatal opening requires phosphorylation of the C-terminal autoinhibitory domain of plasma membrane H+-ATPase |
| title_full_unstemmed | Light-induced stomatal opening requires phosphorylation of the C-terminal autoinhibitory domain of plasma membrane H+-ATPase |
| title_short | Light-induced stomatal opening requires phosphorylation of the C-terminal autoinhibitory domain of plasma membrane H+-ATPase |
| title_sort | light induced stomatal opening requires phosphorylation of the c terminal autoinhibitory domain of plasma membrane h atpase |
| url | https://doi.org/10.1038/s41467-024-45236-9 |
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