GORK K+ channel structure and gating vital to informing stomatal engineering

Abstract The Arabidopsis GORK channel is a major pathway for guard cell K+ efflux that facilitates stomatal closure. GORK is an outwardly-rectifying member of the cyclic-nucleotide binding-homology domain (CNBHD) family of K+ channels with close homologues in all other angiosperms known to date. Its...

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Main Authors: Xue Zhang, William Carroll, Thu Binh-Anh Nguyen, Thanh-Hao Nguyen, Zhao Yang, Miaolian Ma, Xiaowei Huang, Adrian Hills, Hui Guo, Rucha Karnik, Michael R. Blatt, Peng Zhang
Format: Article
Language:English
Published: Nature Portfolio 2025-02-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-57287-7
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author Xue Zhang
William Carroll
Thu Binh-Anh Nguyen
Thanh-Hao Nguyen
Zhao Yang
Miaolian Ma
Xiaowei Huang
Adrian Hills
Hui Guo
Rucha Karnik
Michael R. Blatt
Peng Zhang
author_facet Xue Zhang
William Carroll
Thu Binh-Anh Nguyen
Thanh-Hao Nguyen
Zhao Yang
Miaolian Ma
Xiaowei Huang
Adrian Hills
Hui Guo
Rucha Karnik
Michael R. Blatt
Peng Zhang
author_sort Xue Zhang
collection DOAJ
description Abstract The Arabidopsis GORK channel is a major pathway for guard cell K+ efflux that facilitates stomatal closure. GORK is an outwardly-rectifying member of the cyclic-nucleotide binding-homology domain (CNBHD) family of K+ channels with close homologues in all other angiosperms known to date. Its bioengineering has demonstrated the potential for enhanced carbon assimilation and water use efficiency. Here we identify critical domains through structural and functional analysis, highlighting conformations that reflect long-lived closed and pre-open states of GORK. These conformations are marked by interactions at the cytosolic face of the membrane between so-called voltage-sensor, C-linker and CNBHD domains, the latter relocating across 10 Å below the voltage sensor. The interactions center around two coupling sites that functional analysis establish are critical for channel gating. The channel is also subject to putative, ligand-like interactions within the CNBHD, which leads to its gating independence of cyclic nucleotides such as cAMP or cGMP. These findings implicate a multi-step mechanism of semi-independent conformational transitions that underlie channel activity and offer promising new sites for optimizing GORK to engineer stomata.
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spelling doaj-art-e135de858c3145c5ba592bf01669d8e82025-08-20T02:16:40ZengNature PortfolioNature Communications2041-17232025-02-0116111310.1038/s41467-025-57287-7GORK K+ channel structure and gating vital to informing stomatal engineeringXue Zhang0William Carroll1Thu Binh-Anh Nguyen2Thanh-Hao Nguyen3Zhao Yang4Miaolian Ma5Xiaowei Huang6Adrian Hills7Hui Guo8Rucha Karnik9Michael R. Blatt10Peng Zhang11National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and EcologyLaboratory of Plant Physiology and Biophysics and School of Molecular Biosciences, Bower Building, University of GlasgowLaboratory of Plant Physiology and Biophysics and School of Molecular Biosciences, Bower Building, University of GlasgowLaboratory of Plant Physiology and Biophysics and School of Molecular Biosciences, Bower Building, University of GlasgowNational Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and EcologyNational Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and EcologyNational Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and EcologyLaboratory of Plant Physiology and Biophysics and School of Molecular Biosciences, Bower Building, University of GlasgowNational Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and EcologyLaboratory of Plant Physiology and Biophysics and School of Molecular Biosciences, Bower Building, University of GlasgowLaboratory of Plant Physiology and Biophysics and School of Molecular Biosciences, Bower Building, University of GlasgowNational Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and EcologyAbstract The Arabidopsis GORK channel is a major pathway for guard cell K+ efflux that facilitates stomatal closure. GORK is an outwardly-rectifying member of the cyclic-nucleotide binding-homology domain (CNBHD) family of K+ channels with close homologues in all other angiosperms known to date. Its bioengineering has demonstrated the potential for enhanced carbon assimilation and water use efficiency. Here we identify critical domains through structural and functional analysis, highlighting conformations that reflect long-lived closed and pre-open states of GORK. These conformations are marked by interactions at the cytosolic face of the membrane between so-called voltage-sensor, C-linker and CNBHD domains, the latter relocating across 10 Å below the voltage sensor. The interactions center around two coupling sites that functional analysis establish are critical for channel gating. The channel is also subject to putative, ligand-like interactions within the CNBHD, which leads to its gating independence of cyclic nucleotides such as cAMP or cGMP. These findings implicate a multi-step mechanism of semi-independent conformational transitions that underlie channel activity and offer promising new sites for optimizing GORK to engineer stomata.https://doi.org/10.1038/s41467-025-57287-7
spellingShingle Xue Zhang
William Carroll
Thu Binh-Anh Nguyen
Thanh-Hao Nguyen
Zhao Yang
Miaolian Ma
Xiaowei Huang
Adrian Hills
Hui Guo
Rucha Karnik
Michael R. Blatt
Peng Zhang
GORK K+ channel structure and gating vital to informing stomatal engineering
Nature Communications
title GORK K+ channel structure and gating vital to informing stomatal engineering
title_full GORK K+ channel structure and gating vital to informing stomatal engineering
title_fullStr GORK K+ channel structure and gating vital to informing stomatal engineering
title_full_unstemmed GORK K+ channel structure and gating vital to informing stomatal engineering
title_short GORK K+ channel structure and gating vital to informing stomatal engineering
title_sort gork k channel structure and gating vital to informing stomatal engineering
url https://doi.org/10.1038/s41467-025-57287-7
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