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Engineering a K+ channel ‘sensory antenna’ enhances stomatal kinetics, water use efficiency and photosynthesis

Abstract

Stomata of plant leaves open to enable CO2 entry for photosynthesis and close to reduce water loss via transpiration. Compared with photosynthesis, stomata respond slowly to fluctuating light, reducing assimilation and water use efficiency. Efficiency gains are possible without a cost to photosynthesis if stomatal kinetics can be accelerated. Here we show that clustering of the GORK channel, which mediates K+ efflux for stomatal closure in the model plant Arabidopsis, arises from binding between the channel voltage sensors, creating an extended ‘sensory antenna’ for channel gating. Mutants altered in clustering affect channel gating to facilitate K+ flux, accelerate stomatal movements and reduce water use without a loss in biomass. Our findings identify the mechanism coupling channel clustering with gating, and they demonstrate the potential for engineering of ion channels native to the guard cell to enhance stomatal kinetics and improve water use efficiency without a cost in carbon fixation.

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Fig. 1: GORK K+ channels interact through the cytosolic N-termini of the voltage sensor domains.
Fig. 2: Alternation of charges defines GORK–VSD interactions.
Fig. 3: Non-interacting channel mutations suppress GORK clustering when stably expressed in Arabidopsis.
Fig. 4: Non-interacting GORK channel mutations express functional K+ channels with displaced midpoint voltages.
Fig. 5: Non-interacting GORK channel mutations accelerate stomatal closure and enhance WUE.
Fig. 6: A mechanism coupling GORK clustering and gating through a binding exchange of the VSD N-terminus.

Data availability

Data generated and analysed during this study are included in the article, 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 and the model parameter sets are freely available to academic users 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/ T013508/1 to M.R.B., by a Royal Thai PhD studentship to W.H., a University of Glasgow Doctoral Training Studentship to W.C., a Lord Kelvin-Adam Smith Doctoral Fellowship to F.A.L.S.-A. and BBSRC grant BB/R019894/1 to A.A. We thank N. Donald for support in mbSUS assays and A. Ruiz-Pardo for help in plant maintenance.

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Contributions

M.R.B. conceived the work and developed the strategies for analysis with B.Z., J.C.A. and A.H.; W.H., W.C. and B.Z. carried out and analysed the mbSUS assays; W.H. carried out oocyte electrophyiology and, with J.C.A., M.K. and M.R.B., the confocal, gas exchange and growth studies; M.K. carried out the guard cell electrophysiology and analysed the results with M.R.B.; S.W. expressed and purified the channel N-termini and carried out the gel filtration studies; M.P. and A.A. undertook the hydroponic growth studies; M.R.B. carried out the modelling with A.H., J.C.A., W.H., F.A.L.S.-A. and M.K.; M.R.B. wrote the manuscript, and all authors edited and approved the manuscript.

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Correspondence to Michael R. Blatt.

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Nature Plants thanks Anna Moroni, Xin-Guang Zhu, Nobuyuki Uozumi and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Methods, Tables 1–3, Figs. 1–15 and Appendix 1.

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Numerical data and statistics for Fig. 3b.

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Numerical data for Fig. 4a–f.

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Numerical data for Fig. 5a–c,e,f.

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Horaruang, W., Klejchová, M., Carroll, W. et al. Engineering a K+ channel ‘sensory antenna’ enhances stomatal kinetics, water use efficiency and photosynthesis. Nat. Plants 8, 1262–1274 (2022). https://doi.org/10.1038/s41477-022-01255-2

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