Stomatal opening under high temperatures is controlled by the OST1-regulated TOT3-AHA1 module

Xiangyu Xu; Hongyan Liu; Myrthe Praat; Gaston A Pizzio; Zhang Jiang; Steven Michiel Driever; Ren Wang; Brigitte Van De Cotte; Selwyn L Y Villers; Kris Gevaert; Nathalie Leonhardt; Hilde Nelissen; Toshinori Kinoshita; Steffen Vanneste; Pedro L Rodriguez; Martijn van Zanten; Lam Dai Vu; Ive De Smet

doi:10.1038/s41477-024-01859-w

Stomatal opening under high temperatures is controlled by the OST1-regulated TOT3-AHA1 module

Xiangyu Xu
, Hongyan Liu
, Myrthe Praat
, Gaston A Pizzio
, Zhang Jiang
, Steven Michiel Driever
, Ren Wang
, Brigitte Van De Cotte
, Selwyn L Y Villers
, Kris Gevaert
, Nathalie Leonhardt
, Hilde Nelissen
, Toshinori Kinoshita
, Steffen Vanneste
, Pedro L Rodriguez
, Martijn van Zanten
, Lam Dai Vu
, Ive De Smet^*

^*Corresponding author for this work

Ghent University
Instituto de Biología Molecular y Celular de Plantas
Wageningen University & Research
Aix Marseille University
Nagoya University

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

Abstract

Plants continuously respond to changing environmental conditions to prevent damage and maintain optimal performance. To regulate gas exchange with the environment and to control abiotic stress relief, plants have pores in their leaf epidermis, called stomata. Multiple environmental signals affect the opening and closing of these stomata. High temperatures promote stomatal opening (to cool down), and drought induces stomatal closing (to prevent water loss). Coinciding stress conditions may evoke conflicting stomatal responses, but the cellular mechanisms to resolve these conflicts are unknown. Here we demonstrate that the high-temperature-associated kinase TARGET OF TEMPERATURE 3 directly controls the activity of plasma membrane H+-ATPases to induce stomatal opening. OPEN STOMATA 1, which regulates stomatal closure to prevent water loss during drought stress, directly inactivates TARGET OF TEMPERATURE 3 through phosphorylation. Taken together, this signalling axis harmonizes stomatal opening and closing under high temperatures and/or drought. In the context of global climate change, understanding how different stress signals converge on stomatal regulation allows the development of climate-change-ready crops.

Original language	English
Article number	10485
Pages (from-to)	105-117
Number of pages	13
Journal	Nature Plants
Volume	11
Issue number	1
Early online date	29 Nov 2024
DOIs	https://doi.org/10.1038/s41477-024-01859-w
Publication status	Published - 2025

Bibliographical note

Publisher Copyright:
© The Author(s), under exclusive licence to Springer Nature Limited 2024.

Funding

We thank D. Van Damme and B. De Rybel for critical comments on the manuscript. We thank E. Farmer for providing the ost2-2D seeds, M. B. Palmgren for the aha1-6 seeds and the Eurasian Arabidopsis Stock Centre for providing various seeds. This work was supported by MCIN/AEI/10.13039/501100011033 grant no. PID2020-113100RB (to P.L.R.), Graduate School Green Top Sectors grant no. GSGT.2018.007 of the Netherlands Organization for Scientific Research (to M.P. and M.v.Z.), UGent BOF postdoctoral mandate no. 01P12219 (to L.D.V.), UGent BOF doctoral mandate no. 01CD7122 (to X.X.), China Scholarship Council grant no. 201708340063 (to R.W.), China Scholarship Council grant no. 201706350153 (to X.X.), China Scholarship Council grant no. 201806170025 (to Z.J.) and China Scholarship Council grant no. 202204910025 (to H.L.).

Funders	Funder number
Nederlandse Organisatie voor Wetenschappelijk Onderzoek
Graduate School Green Top Sectors
Universiteit Gent	01CD7122, 01P12219
China Scholarship Council	201806170025, 201708340063, 201706350153, 202204910025

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 13 Climate Action

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10.1038/s41477-024-01859-w

s41477-024-01859-wFinal published version, 3.33 MBLicence: Taverne

Cite this

Xu, X., Liu, H., Praat, M., Pizzio, G. A., Jiang, Z., Driever, S. M., Wang, R., Van De Cotte, B., Villers, S. L. Y., Gevaert, K., Leonhardt, N., Nelissen, H., Kinoshita, T., Vanneste, S., Rodriguez, P. L., van Zanten, M., Vu, L. D., & De Smet, I. (2025). Stomatal opening under high temperatures is controlled by the OST1-regulated TOT3-AHA1 module. Nature Plants, 11(1), 105-117. Article 10485. https://doi.org/10.1038/s41477-024-01859-w

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title = "Stomatal opening under high temperatures is controlled by the OST1-regulated TOT3-AHA1 module",

abstract = "Plants continuously respond to changing environmental conditions to prevent damage and maintain optimal performance. To regulate gas exchange with the environment and to control abiotic stress relief, plants have pores in their leaf epidermis, called stomata. Multiple environmental signals affect the opening and closing of these stomata. High temperatures promote stomatal opening (to cool down), and drought induces stomatal closing (to prevent water loss). Coinciding stress conditions may evoke conflicting stomatal responses, but the cellular mechanisms to resolve these conflicts are unknown. Here we demonstrate that the high-temperature-associated kinase TARGET OF TEMPERATURE 3 directly controls the activity of plasma membrane H+-ATPases to induce stomatal opening. OPEN STOMATA 1, which regulates stomatal closure to prevent water loss during drought stress, directly inactivates TARGET OF TEMPERATURE 3 through phosphorylation. Taken together, this signalling axis harmonizes stomatal opening and closing under high temperatures and/or drought. In the context of global climate change, understanding how different stress signals converge on stomatal regulation allows the development of climate-change-ready crops.",

author = "Xiangyu Xu and Hongyan Liu and Myrthe Praat and Pizzio, \{Gaston A\} and Zhang Jiang and Driever, \{Steven Michiel\} and Ren Wang and \{Van De Cotte\}, Brigitte and Villers, \{Selwyn L Y\} and Kris Gevaert and Nathalie Leonhardt and Hilde Nelissen and Toshinori Kinoshita and Steffen Vanneste and Rodriguez, \{Pedro L\} and \{van Zanten\}, Martijn and Vu, \{Lam Dai\} and \{De Smet\}, Ive",

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Xu, X, Liu, H, Praat, M, Pizzio, GA, Jiang, Z, Driever, SM, Wang, R, Van De Cotte, B, Villers, SLY, Gevaert, K, Leonhardt, N, Nelissen, H, Kinoshita, T, Vanneste, S, Rodriguez, PL, van Zanten, M, Vu, LD & De Smet, I 2025, 'Stomatal opening under high temperatures is controlled by the OST1-regulated TOT3-AHA1 module', Nature Plants, vol. 11, no. 1, 10485, pp. 105-117. https://doi.org/10.1038/s41477-024-01859-w

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AU - Xu, Xiangyu

AU - Liu, Hongyan

AU - Praat, Myrthe

AU - Pizzio, Gaston A

AU - Jiang, Zhang

AU - Driever, Steven Michiel

AU - Wang, Ren

AU - Van De Cotte, Brigitte

AU - Villers, Selwyn L Y

AU - Gevaert, Kris

AU - Leonhardt, Nathalie

AU - Nelissen, Hilde

AU - Kinoshita, Toshinori

AU - Vanneste, Steffen

AU - Rodriguez, Pedro L

AU - van Zanten, Martijn

AU - Vu, Lam Dai

AU - De Smet, Ive

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N2 - Plants continuously respond to changing environmental conditions to prevent damage and maintain optimal performance. To regulate gas exchange with the environment and to control abiotic stress relief, plants have pores in their leaf epidermis, called stomata. Multiple environmental signals affect the opening and closing of these stomata. High temperatures promote stomatal opening (to cool down), and drought induces stomatal closing (to prevent water loss). Coinciding stress conditions may evoke conflicting stomatal responses, but the cellular mechanisms to resolve these conflicts are unknown. Here we demonstrate that the high-temperature-associated kinase TARGET OF TEMPERATURE 3 directly controls the activity of plasma membrane H+-ATPases to induce stomatal opening. OPEN STOMATA 1, which regulates stomatal closure to prevent water loss during drought stress, directly inactivates TARGET OF TEMPERATURE 3 through phosphorylation. Taken together, this signalling axis harmonizes stomatal opening and closing under high temperatures and/or drought. In the context of global climate change, understanding how different stress signals converge on stomatal regulation allows the development of climate-change-ready crops.

AB - Plants continuously respond to changing environmental conditions to prevent damage and maintain optimal performance. To regulate gas exchange with the environment and to control abiotic stress relief, plants have pores in their leaf epidermis, called stomata. Multiple environmental signals affect the opening and closing of these stomata. High temperatures promote stomatal opening (to cool down), and drought induces stomatal closing (to prevent water loss). Coinciding stress conditions may evoke conflicting stomatal responses, but the cellular mechanisms to resolve these conflicts are unknown. Here we demonstrate that the high-temperature-associated kinase TARGET OF TEMPERATURE 3 directly controls the activity of plasma membrane H+-ATPases to induce stomatal opening. OPEN STOMATA 1, which regulates stomatal closure to prevent water loss during drought stress, directly inactivates TARGET OF TEMPERATURE 3 through phosphorylation. Taken together, this signalling axis harmonizes stomatal opening and closing under high temperatures and/or drought. In the context of global climate change, understanding how different stress signals converge on stomatal regulation allows the development of climate-change-ready crops.

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ER -

Stomatal opening under high temperatures is controlled by the OST1-regulated TOT3-AHA1 module

Abstract

Bibliographical note

Funding

UN SDGs

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