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Reversible heat-inactivation of the calvin cycle: A possible mechanism of the temperature regulation of photosynthesis

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Abstract

Photosynthetic CO2 fixation rates in leaves and intact chloroplasts of spinach measured at 18°–20° C are substantially decreased by pretreatment at temperatures exceeding 20° C. Mild heating which causes 80% inhibition of CO2 fixation does not affect phosphoglyceroacid reduction and causes increases in the ATP/ADP ratio and the light-induced transthylakoid proton gradient. The inactivation of the CO2 fixation is completely reversible with half-times of recovery in the order of 15–20 min. Comparison of steady-state patterns of 14C labeled Calvin cycle intermediates of heat-treated and control samples reveals a large increase in the ribulose-1,5-bisphosphate/phosphoglyceroacid ratio and a large decrease in the phosphoglyceroacid/triosephosphate ratio. It is concluded that inactivation of CO2 fixation occurring at elevated temperatures is caused by inhibition of the ribulose-1,5-bisphosphate carboxylase (EC 4.1.1.39). Measurements of light-induced light scattering changes of thylakoids and of the light-induced electrochromic absorption shift show that these signals are affected by mild heating in a way which is strictly correlated with the inactivation of the CO2 fixation. It is proposed that the function of the ribulose-1,5-bisphosphate carboxylase in vivo requires a form of activation that involves properties of the thylakoid membrane which are affected by the heat treatment. The fact that these changes in thylakoid membrane properties and of ribulose-1,5-bisphosphate carboxylase activity are already affected at elevated temperatures which can still be considered physiological, and the reversible nature of these changes, suggest that they may play a role in temperature regulation of the overall photosynthetic process.

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Abbreviations

9-AA:

9-aminoacridine

DMO:

5,5-dimethyloxazolidine-2,4-dione

FBP:

fructose-1,6-bisphosphate

HEPES:

N-2-hydroxyethylpiperazine N-2-ethane sulfonic acid

HMP:

hexose monophosphates

PGA:

3-phosphoglycerate

PMP:

pentose monophosphates

RuBP:

ribulose-1,5-bisphosphate

SBP:

seduheptulose-1,7-bisphosphate

TP:

triose monophosphates

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  1. Botanisches Institut der Universität, Universitätsstraße 1, Gebäude 26.13, D-4000, Düsseldorf, Germany

    Engelbert Weis

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  1. Engelbert Weis
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Weis, E. Reversible heat-inactivation of the calvin cycle: A possible mechanism of the temperature regulation of photosynthesis. Planta 151, 33–39 (1981). https://doi.org/10.1007/BF00384234

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  • DOI: https://doi.org/10.1007/BF00384234

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