Stomatal responses to carbon dioxide and light require abscisic acid catabolism in Arabidopsis

Mahsa Movahedi; Nicholas Zoulias; Stuart A. Casson; Peng Sun; Yun Kuan Liang; Alistair M. Hetherington; Julie E. Gray; Caspar C.C. Chater

doi:10.1098/rsfs.2020.0036

Stomatal responses to carbon dioxide and light require abscisic acid catabolism in Arabidopsis

Mahsa Movahedi, Nicholas Zoulias, Stuart A. Casson, Peng Sun, Yun Kuan Liang, Alistair M. Hetherington, Julie E. Gray, Caspar C.C. Chater^*

^*Corresponding author for this work

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

6 Citations (Scopus)

Abstract

In plants, stomata control water loss and CO 2 uptake. The aperture and density of stomatal pores, and hence the exchange of gases between the plant and the atmosphere, are controlled by internal factors such as the plant hormone abscisic acid (ABA) and external signals including light and CO 2. In this study, we examine the importance of ABA catabolism in the stomatal responses to CO 2 and light. By using the ABA 8′-hydroxylase-deficient Arabidopsis thaliana double mutant cyp707a1 cyp707a3, which is unable to break down and instead accumulates high levels of ABA, we reveal the importance of the control of ABA concentration in mediating stomatal responses to CO 2 and light. Intriguingly, our experiments suggest that endogenously produced ABA is unable to close stomata in the absence of CO 2. Furthermore, we show that when plants are grown in short day conditions ABA breakdown is required for the modulation of both elevated [CO 2 ]-induced stomatal closure and elevated [CO 2 ]-induced reductions in leaf stomatal density. ABA catabolism is also required for the stomatal density response to light intensity, and for the full range of light-induced stomatal opening, suggesting that ABA catabolism is critical for the integration of stomatal responses to a range of environmental stimuli.

Original language	English
Article number	20200036
Journal	Interface Focus
Volume	11
Issue number	2
DOIs	https://doi.org/10.1098/rsfs.2020.0036
Publication status	Published - 6 Apr 2021

Bibliographical note

Funding Information:
uploaded as part of the electronic supplementary material. Authors’ contributions. M.M. and C.C.C.C. contributed equally to this work by designing and performing experiments and analysing data. N.Z. and S.A.C. performed reciprocal light and qRT-PCR experiments. P.S. and Y.-K.L. performed CaCl2 bioassays. M.M., C.C.C.C., J.E.G., N.Z., S.A.C. and A.M.H. wrote the manuscript and interpreted data. C.C.C.C., J.E.G. and A.M.H. conceived the project. All authors reviewed the manuscript. Competing interests. The authors declare no competing financial interests. Funding. A.M.H. and J.E.G. acknowledge the Biotechnology and Biological Sciences Research Council (BBSRC) and the Leverhulme Trust for supporting the work described in this paper. C.C.C.C. would like to acknowledge funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement no. 700867. Acknowledgements. The authors gratefully thank Dr Eiji Nambara (University of Toronto) for the gift of the ABA catabolism mutants and Dr Annie Marion-Poll (INRA) for the gift of the ABA biosynthesis mutants.

Publisher Copyright:
© 2021 The Author(s).

Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.

Keywords

abscisic acid
carbon dioxide
CO 2
guard cells
light
stomata

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@article{81ddbfc9a14344ec98757ebceb2b3b0f,

title = "Stomatal responses to carbon dioxide and light require abscisic acid catabolism in Arabidopsis",

abstract = "In plants, stomata control water loss and CO 2 uptake. The aperture and density of stomatal pores, and hence the exchange of gases between the plant and the atmosphere, are controlled by internal factors such as the plant hormone abscisic acid (ABA) and external signals including light and CO 2. In this study, we examine the importance of ABA catabolism in the stomatal responses to CO 2 and light. By using the ABA 8′-hydroxylase-deficient Arabidopsis thaliana double mutant cyp707a1 cyp707a3, which is unable to break down and instead accumulates high levels of ABA, we reveal the importance of the control of ABA concentration in mediating stomatal responses to CO 2 and light. Intriguingly, our experiments suggest that endogenously produced ABA is unable to close stomata in the absence of CO 2. Furthermore, we show that when plants are grown in short day conditions ABA breakdown is required for the modulation of both elevated [CO 2 ]-induced stomatal closure and elevated [CO 2 ]-induced reductions in leaf stomatal density. ABA catabolism is also required for the stomatal density response to light intensity, and for the full range of light-induced stomatal opening, suggesting that ABA catabolism is critical for the integration of stomatal responses to a range of environmental stimuli. ",

keywords = "abscisic acid, carbon dioxide, CO 2, guard cells, light, stomata",

author = "Mahsa Movahedi and Nicholas Zoulias and Casson, {Stuart A.} and Peng Sun and Liang, {Yun Kuan} and Hetherington, {Alistair M.} and Gray, {Julie E.} and Chater, {Caspar C.C.}",

note = "Funding Information: uploaded as part of the electronic supplementary material. Authors{\textquoteright} contributions. M.M. and C.C.C.C. contributed equally to this work by designing and performing experiments and analysing data. N.Z. and S.A.C. performed reciprocal light and qRT-PCR experiments. P.S. and Y.-K.L. performed CaCl2 bioassays. M.M., C.C.C.C., J.E.G., N.Z., S.A.C. and A.M.H. wrote the manuscript and interpreted data. C.C.C.C., J.E.G. and A.M.H. conceived the project. All authors reviewed the manuscript. Competing interests. The authors declare no competing financial interests. Funding. A.M.H. and J.E.G. acknowledge the Biotechnology and Biological Sciences Research Council (BBSRC) and the Leverhulme Trust for supporting the work described in this paper. C.C.C.C. would like to acknowledge funding from the European Union{\textquoteright}s Horizon 2020 research and innovation programme under the Marie Sk{\l}odowska-Curie grant agreement no. 700867. Acknowledgements. The authors gratefully thank Dr Eiji Nambara (University of Toronto) for the gift of the ABA catabolism mutants and Dr Annie Marion-Poll (INRA) for the gift of the ABA biosynthesis mutants. Publisher Copyright: {\textcopyright} 2021 The Author(s). Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

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doi = "10.1098/rsfs.2020.0036",

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AU - Movahedi, Mahsa

AU - Zoulias, Nicholas

AU - Casson, Stuart A.

AU - Sun, Peng

AU - Liang, Yun Kuan

AU - Hetherington, Alistair M.

AU - Gray, Julie E.

AU - Chater, Caspar C.C.

N1 - Funding Information: uploaded as part of the electronic supplementary material. Authors’ contributions. M.M. and C.C.C.C. contributed equally to this work by designing and performing experiments and analysing data. N.Z. and S.A.C. performed reciprocal light and qRT-PCR experiments. P.S. and Y.-K.L. performed CaCl2 bioassays. M.M., C.C.C.C., J.E.G., N.Z., S.A.C. and A.M.H. wrote the manuscript and interpreted data. C.C.C.C., J.E.G. and A.M.H. conceived the project. All authors reviewed the manuscript. Competing interests. The authors declare no competing financial interests. Funding. A.M.H. and J.E.G. acknowledge the Biotechnology and Biological Sciences Research Council (BBSRC) and the Leverhulme Trust for supporting the work described in this paper. C.C.C.C. would like to acknowledge funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement no. 700867. Acknowledgements. The authors gratefully thank Dr Eiji Nambara (University of Toronto) for the gift of the ABA catabolism mutants and Dr Annie Marion-Poll (INRA) for the gift of the ABA biosynthesis mutants. Publisher Copyright: © 2021 The Author(s). Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

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N2 - In plants, stomata control water loss and CO 2 uptake. The aperture and density of stomatal pores, and hence the exchange of gases between the plant and the atmosphere, are controlled by internal factors such as the plant hormone abscisic acid (ABA) and external signals including light and CO 2. In this study, we examine the importance of ABA catabolism in the stomatal responses to CO 2 and light. By using the ABA 8′-hydroxylase-deficient Arabidopsis thaliana double mutant cyp707a1 cyp707a3, which is unable to break down and instead accumulates high levels of ABA, we reveal the importance of the control of ABA concentration in mediating stomatal responses to CO 2 and light. Intriguingly, our experiments suggest that endogenously produced ABA is unable to close stomata in the absence of CO 2. Furthermore, we show that when plants are grown in short day conditions ABA breakdown is required for the modulation of both elevated [CO 2 ]-induced stomatal closure and elevated [CO 2 ]-induced reductions in leaf stomatal density. ABA catabolism is also required for the stomatal density response to light intensity, and for the full range of light-induced stomatal opening, suggesting that ABA catabolism is critical for the integration of stomatal responses to a range of environmental stimuli.

AB - In plants, stomata control water loss and CO 2 uptake. The aperture and density of stomatal pores, and hence the exchange of gases between the plant and the atmosphere, are controlled by internal factors such as the plant hormone abscisic acid (ABA) and external signals including light and CO 2. In this study, we examine the importance of ABA catabolism in the stomatal responses to CO 2 and light. By using the ABA 8′-hydroxylase-deficient Arabidopsis thaliana double mutant cyp707a1 cyp707a3, which is unable to break down and instead accumulates high levels of ABA, we reveal the importance of the control of ABA concentration in mediating stomatal responses to CO 2 and light. Intriguingly, our experiments suggest that endogenously produced ABA is unable to close stomata in the absence of CO 2. Furthermore, we show that when plants are grown in short day conditions ABA breakdown is required for the modulation of both elevated [CO 2 ]-induced stomatal closure and elevated [CO 2 ]-induced reductions in leaf stomatal density. ABA catabolism is also required for the stomatal density response to light intensity, and for the full range of light-induced stomatal opening, suggesting that ABA catabolism is critical for the integration of stomatal responses to a range of environmental stimuli.

KW - abscisic acid

KW - carbon dioxide

KW - CO 2

KW - guard cells

KW - light

KW - stomata

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U2 - 10.1098/rsfs.2020.0036

DO - 10.1098/rsfs.2020.0036

M3 - Article (Academic Journal)

C2 - 33633834

AN - SCOPUS:85101370881

VL - 11

JO - Interface Focus

JF - Interface Focus

SN - 2042-8898

IS - 2

M1 - 20200036

ER -

Stomatal responses to carbon dioxide and light require abscisic acid catabolism in Arabidopsis

Abstract

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Keywords

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