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Guard cell endomembrane Ca2+-ATPases underpin a ‘carbon memory’ of photosynthetic assimilation that impacts on water-use efficiency

Nature Plants volume 7, pages 1301–1313 (2021)Cite this article

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Abstract

Stomata of most plants close to preserve water when the demand for CO2 by photosynthesis is reduced. Stomatal responses are slow compared with photosynthesis, and this kinetic difference erodes assimilation and water-use efficiency under fluctuating light. Despite a deep knowledge of guard cells that regulate the stoma, efforts to enhance stomatal kinetics are limited by our understanding of its control by foliar CO2. Guided by mechanistic modelling that incorporates foliar CO2 diffusion and mesophyll photosynthesis, here we uncover a central role for endomembrane Ca2+ stores in guard cell responsiveness to fluctuating light and CO2. Modelling predicted and experiments demonstrated a delay in Ca2+ cycling that was enhanced by endomembrane Ca2+-ATPase mutants, altering stomatal conductance and reducing assimilation and water-use efficiency. Our findings illustrate the power of modelling to bridge the gap from the guard cell to whole-plant photosynthesis, and they demonstrate an unforeseen latency, or ‘carbon memory’, of guard cells that affects stomatal dynamics, photosynthesis and water-use efficiency.

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Fig. 1: Schematic of CO2 diffusion from the atmosphere, through the stomatal pore and point p near the inner mouth of the pore, to the CO2 sink of photosynthesis in the mesophyll of the leaf.
Fig. 2: OnGuard3 reproduces gs and its dependence on \(pCO_{2}\) and light for photosynthesis in Arabidopsis.
Fig. 3: OnGuard3 predicts an elevation in [Ca2+]i on steps to 1,000 μbar CO2 and an undershoot in [Ca2+]i on its return.
Fig. 4: \(pCO_{2}\) elevation and its recovery identify a hysteresis in [Ca2+]i and K+ channel activities predicted with OnGuard3.
Fig. 5: Repeated \(pCO_{2}\) challenge uncovers a latency in stomatal kinetics that depends on guard cell endomembrane Ca2+ stores.
Fig. 6: Latency in stomatal kinetics affects long-term WUE and plant growth.
Fig. 7: A latent carbon memory in stomatal responsiveness depends on guard cell endomembrane Ca2+ stores.

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Data availability

All data generated and analysed during this study are included in this published article and its supplementary information files and are also available on reasonable request to the corresponding author. Source data are provided with this paper.

Code availability

The OnGuard3 platform (v. 3.3.1.6) and the model parameter sets for wild-type and aca mutant Arabidopsis as binary code described herein are freely available and may be downloaded from www.psrg.org.uk.

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Acknowledgements

This work was supported by BBSRC grants BB/L001276/1, BB/L019205/1, BB/M001601/1 and BB/N01832X/1 to M.R.B. and by National Science Foundation grant IOS 1656774 to J.F.H. Y.W. was supported by the National Science Foundation of China grant 31871537 and the Central Universities Fundamental Research Fund 2020XZZX002-21. F.A.L.S.-A. was supported by a Lord Kelvin and Adam Smith PhD studentship. We thank A. Ruiz-Pardo for help in plant maintenance.

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  1. These authors contributed equally: Marieke Jezek, Fernanda A. L. Silva-Alvim, Adrian Hills.

  2. These authors jointly supervised this work: Yizhou Wang, Virgilio L. Lew, Michael R. Blatt.

Authors and Affiliations

  1. Laboratory of Plant Physiology and Biophysics, University of Glasgow, Glasgow, UK

    Mareike Jezek, Fernanda A. L. Silva-Alvim, Adrian Hills, Naomi Donald, Jessica Shadbolt & Michael R. Blatt

  2. Department of Biochemistry and Molecular Biology, University of Nevada, Reno, NV, USA

    Maryam Rahmati Ishka & Jeffrey F. Harper

  3. Institute of Crop Science, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China

    Bingqing He, Yizhou Wang & Michael R. Blatt

  4. School of Life Sciences, University of Essex, Colchester, UK

    Tracy Lawson

  5. Physiological Laboratory, University of Cambridge, Cambridge, UK

    Virgilio L. Lew

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Contributions

M.R.B., A.H. and V.L.L. conceived the work and developed the model platform; A.H. encoded the platform; M.R.B., M.J., B.H. and Y.H. resolved the models; M.J., J.S. and Y.H. carried out gas exchange and aperture measurements; F.A.L.S.-A., N.D. and M.R.B. carried out growth studies, biochemical and Ca2+ analyses; Y.W. and F.A.L.S.-A. carried out voltage clamp experiments and M.J., Y.W. and F.A.L.S.-A. analysed the results with M.R.B.; M.R.B. wrote the manuscript with M.J., A.H., F.A.L.S.-A. and V.L.L.; all authors edited and approved the manuscript.

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Correspondence to Michael R. Blatt.

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Jezek, M., Silva-Alvim, F.A.L., Hills, A. et al. Guard cell endomembrane Ca2+-ATPases underpin a ‘carbon memory’ of photosynthetic assimilation that impacts on water-use efficiency. Nat. Plants 7, 1301–1313 (2021). https://doi.org/10.1038/s41477-021-00966-2

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