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), [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

@article{838c17858a0a42fdb31b7d3dd1047b34,

title = "Structure and activity of SLAC1 channels for stomatal signaling in leaves",

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}",

note = "Funding Information: ACKNOWLEDGMENTS. We thank Dr. Guang-zhe Yang for suggestions on electrophysiological experiments and De-lin Li, Ling-min Yuan, and other colleagues for expression screening in the early stages of the project. We are also grateful to the staff at the Center for Biological Imaging, Institute of Biophysics, Chinese Academy of Sciences. This project was financially supported by the National Key Research and Development Program of China (Grants 2016YFA0500503 and 2020YFA0509903), the Strategic Priority Research Program of the Chinese Academy of Sciences (Precision Seed Design and Breeding, Grant XDA24020305), and the National Natural Science Foundation of China (Grants 31470728, 31322005, and 31872721) to Y.-h.C., by NIH Grant R35GM134920-01 and NSF Grant MCB-1934628 to F.L., and by NIH Grants R01GM107462 and P41GM116799 to W.A.H. Publisher Copyright: {\textcopyright} 2021 National Academy of Sciences. All rights reserved.",

year = "2021",

month = may,

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doi = "10.1073/pnas.2015151118",

language = "English (US)",

volume = "118",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

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TY - JOUR

T1 - Structure and activity of SLAC1 channels for stomatal signaling in leaves

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

N1 - Funding Information: ACKNOWLEDGMENTS. We thank Dr. Guang-zhe Yang for suggestions on electrophysiological experiments and De-lin Li, Ling-min Yuan, and other colleagues for expression screening in the early stages of the project. We are also grateful to the staff at the Center for Biological Imaging, Institute of Biophysics, Chinese Academy of Sciences. This project was financially supported by the National Key Research and Development Program of China (Grants 2016YFA0500503 and 2020YFA0509903), the Strategic Priority Research Program of the Chinese Academy of Sciences (Precision Seed Design and Breeding, Grant XDA24020305), and the National Natural Science Foundation of China (Grants 31470728, 31322005, and 31872721) to Y.-h.C., by NIH Grant R35GM134920-01 and NSF Grant MCB-1934628 to F.L., and by NIH Grants R01GM107462 and P41GM116799 to W.A.H. Publisher Copyright: © 2021 National Academy of Sciences. All rights reserved.

PY - 2021/5/4

Y1 - 2021/5/4

N2 - 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.

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.

KW - Abscisic acid signaling

KW - Channel activation

KW - Cryo-EM

KW - Electrophysiology

KW - Phosphorylation

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U2 - 10.1073/pnas.2015151118

DO - 10.1073/pnas.2015151118

M3 - Article

C2 - 33926963

AN - SCOPUS:85105129357

VL - 118

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 18

M1 - 2015151118

ER -

Structure and activity of SLAC1 channels for stomatal signaling in leaves

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