Structure and activity of SLAC1 channels for stomatal signaling in leaves

Ya Nan Deng; Hamdy Kashtoh; Quan Wang; Guang Xiao Zhen; Qi Yu Li; Ling Hui Tang; Hai Long Gao; Chun Rui Zhang; Li Qin; Min Su; Fei Li; Xia He Huang; Ying Chun Wang; Qi Xie; Oliver B. Clarke; Wayne A. Hendrickson; Yu Hang Chen

doi:10.1073/pnas.2015151118

Structure and activity of SLAC1 channels for stomatal signaling in leaves

Ya Nan Deng, Hamdy Kashtoh, Quan Wang, Guang Xiao Zhen, Qi Yu Li, Ling Hui Tang, Hai Long Gao, Chun Rui Zhang, Li Qin, Min Su, Fei Li, Xia He Huang, Ying Chun Wang, Qi Xie, Oliver B. Clarke, Wayne A. Hendrickson, Yu Hang Chen

Biology and Genomics

Research output: Contribution to journal › Article › peer-review

Abstract

Stomata in leaves regulate gas exchange between the plant and its atmosphere. Various environmental stimuli elicit abscisic acid (ABA); ABA leads to phosphoactivation of slow anion channel 1 (SLAC1); SLAC1 activity reduces turgor pressure in aperture-defining guard cells; and stomatal closure ensues. We used electrophysiology for functional characterizations of Arabidopsis thaliana SLAC1 (AtSLAC1) and cryoelectron microscopy (cryo-EM) for structural analysis of Brachypodium distachyon SLAC1 (BdSLAC1), at 2.97-Å resolution. We identified 14 phosphorylation sites in AtSLAC1 and showed nearly 330-fold channel-activity enhancement with 4 to 6 of these phosphorylated. Seven SLAC1-conserved arginines are poised in BdSLAC1 for regulatory interaction with the N-terminal extension. This BdSLAC1 structure has its pores closed, in a basal state, spring loaded by phenylalanyl residues in high-energy conformations. SLAC1 phosphorylation fine-tunes an equilibrium between basal and activated SLAC1 trimers, thereby controlling the degree of stomatal opening.

Original language	English (US)
Article number	2015151118
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	118
Issue number	18
DOIs	https://doi.org/10.1073/pnas.2015151118
State	Published - May 4 2021

Keywords

Abscisic acid signaling
Channel activation
Cryo-EM
Electrophysiology
Phosphorylation

ASJC Scopus subject areas

General

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10.1073/pnas.2015151118

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Deng, Y. N., Kashtoh, H., Wang, Q., Zhen, G. X., Li, Q. Y., Tang, L. H., Gao, H. L., Zhang, C. R., Qin, L., Su, M., Li, F., Huang, X. H., Wang, Y. C., Xie, Q., Clarke, O. B., Hendrickson, W. A., & Chen, Y. H. (2021). Structure and activity of SLAC1 channels for stomatal signaling in leaves. Proceedings of the National Academy of Sciences of the United States of America, 118(18), Article 2015151118. https://doi.org/10.1073/pnas.2015151118

Deng, YN, Kashtoh, H, Wang, Q, Zhen, GX, Li, QY, Tang, LH, Gao, HL, Zhang, CR, Qin, L, Su, M, Li, F, Huang, XH, Wang, YC, Xie, Q, Clarke, OB, Hendrickson, WA & Chen, YH 2021, 'Structure and activity of SLAC1 channels for stomatal signaling in leaves', Proceedings of the National Academy of Sciences of the United States of America, vol. 118, no. 18, 2015151118. https://doi.org/10.1073/pnas.2015151118

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abstract = "Stomata in leaves regulate gas exchange between the plant and its atmosphere. Various environmental stimuli elicit abscisic acid (ABA); ABA leads to phosphoactivation of slow anion channel 1 (SLAC1); SLAC1 activity reduces turgor pressure in aperture-defining guard cells; and stomatal closure ensues. We used electrophysiology for functional characterizations of Arabidopsis thaliana SLAC1 (AtSLAC1) and cryoelectron microscopy (cryo-EM) for structural analysis of Brachypodium distachyon SLAC1 (BdSLAC1), at 2.97-{\AA} resolution. We identified 14 phosphorylation sites in AtSLAC1 and showed nearly 330-fold channel-activity enhancement with 4 to 6 of these phosphorylated. Seven SLAC1-conserved arginines are poised in BdSLAC1 for regulatory interaction with the N-terminal extension. This BdSLAC1 structure has its pores closed, in a basal state, spring loaded by phenylalanyl residues in high-energy conformations. SLAC1 phosphorylation fine-tunes an equilibrium between basal and activated SLAC1 trimers, thereby controlling the degree of stomatal opening.",

keywords = "Abscisic acid signaling, Channel activation, Cryo-EM, Electrophysiology, Phosphorylation",

author = "Deng, {Ya Nan} and Hamdy Kashtoh and Quan Wang and Zhen, {Guang Xiao} and Li, {Qi Yu} and Tang, {Ling Hui} and Gao, {Hai Long} and Zhang, {Chun Rui} and Li Qin and Min Su and Fei Li and Huang, {Xia He} and Wang, {Ying Chun} and Qi Xie and Clarke, {Oliver B.} and Hendrickson, {Wayne A.} and Chen, {Yu Hang}",

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AU - Deng, Ya Nan

AU - Kashtoh, Hamdy

AU - Wang, Quan

AU - Zhen, Guang Xiao

AU - Li, Qi Yu

AU - Tang, Ling Hui

AU - Gao, Hai Long

AU - Zhang, Chun Rui

AU - Qin, Li

AU - Su, Min

AU - Li, Fei

AU - Huang, Xia He

AU - Wang, Ying Chun

AU - Xie, Qi

AU - Clarke, Oliver B.

AU - Hendrickson, Wayne A.

AU - Chen, Yu Hang

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AB - Stomata in leaves regulate gas exchange between the plant and its atmosphere. Various environmental stimuli elicit abscisic acid (ABA); ABA leads to phosphoactivation of slow anion channel 1 (SLAC1); SLAC1 activity reduces turgor pressure in aperture-defining guard cells; and stomatal closure ensues. We used electrophysiology for functional characterizations of Arabidopsis thaliana SLAC1 (AtSLAC1) and cryoelectron microscopy (cryo-EM) for structural analysis of Brachypodium distachyon SLAC1 (BdSLAC1), at 2.97-Å resolution. We identified 14 phosphorylation sites in AtSLAC1 and showed nearly 330-fold channel-activity enhancement with 4 to 6 of these phosphorylated. Seven SLAC1-conserved arginines are poised in BdSLAC1 for regulatory interaction with the N-terminal extension. This BdSLAC1 structure has its pores closed, in a basal state, spring loaded by phenylalanyl residues in high-energy conformations. SLAC1 phosphorylation fine-tunes an equilibrium between basal and activated SLAC1 trimers, thereby controlling the degree of stomatal opening.

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KW - Cryo-EM

KW - Electrophysiology

KW - Phosphorylation

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Structure and activity of SLAC1 channels for stomatal signaling in leaves

Abstract

Keywords

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