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Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP

Abstract

Water stress substantially alters plant metabolism, decreasing plant growth and photosynthesis1,2,3,4 and profoundly affecting ecosystems and agriculture, and thus human societies5. There is controversy over the mechanisms by which stress decreases photosynthetic assimilation of CO2. Two principal effects are invoked2,4: restricted diffusion of CO2 into the leaf, caused by stomatal closure6,7,8, and inhibition of CO2 metabolism9,10,11. Here we show, in leaves of sunflower (Helianthus annuus L.), that stress decreases CO2 assimilation more than it slows O2 evolution, and that the effects are not reversed by high concentrations of CO212,13. Stress decreases the amounts of ATP9,11 and ribulose bisphosphate found in the leaves, correlating with reduced CO2 assimilation11, but the amount and activity of ribulose bisphosphate carboxylase-oxygenase (Rubisco) do not correlate. We show that ATP-synthase (coupling factor) decreases with stress and conclude that photosynthetic assimilation of CO2 by stressed leaves is not limited by CO2 diffusion but by inhibition of ribulose biphosphate synthesis, related to lower ATP content resulting from loss of ATP synthase.

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Figure 1: Rate of photosynthetic CO2 assimilation (A) in sunflower (H. annuus L.) as a function of the calculated CO2 concentration inside the leaf mesophyll (ci) for leaves of different water potential (ψ, shown against each curve) measured at 800 µmol m-2 s-1 PAR and 25 °C.
Figure 2: Photosynthetic processes of sunflower (H. annuus L.) leaves as a function of leaf water potential (ψ).
Figure 3: Biochemical composition of sunflower (H. annuus L.) leaves as a function of water potential (ψ).

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Acknowledgements

We acknowledge help in measurement of metabolites and Rubisco from A. J. Keys, M. A. Parry and M. J. Paul and of ATP-synthase by J. C. Theobald; discussions with R. A. C. Mitchell; and manuscript preparation by K. Lawlor. J. C. Gray supplied the ATP synthase antibody. Financial support to W.T. was from CONICYT, Venezuela and Rothamsted International. IACR-Rothamsted receives grant aid from the BBSRC, UK.

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Correspondence to D. W. Lawlor.

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Tezara, W., Mitchell, V., Driscoll, S. et al. Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401, 914–917 (1999). https://doi.org/10.1038/44842

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