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Photosynthetic control of chloroplast gene expression

Abstract

Redox chemistry—the transfer of electrons or hydrogen atoms—is central to energy conversion in respiration and photosynthesis. In photosynthesis in chloroplasts, two separate, light-driven reactions, termed photosystem I and photosystem II, are connected in series by a chain of electron carriers1,2,3. The redox state of one connecting electron carrier, plastoquinone, governs the distribution of absorbed light energy between photosystems I and II by controlling the phosphorylation of a mobile, light-harvesting, pigment–protein complex4,5. Here we show that the redox state of plastoquinone also controls the rate of transcription of genes encoding reaction-centre apoproteins of photosystem I and photosystem II. As a result of this control, the stoichiometry between the two photosystems changes in a way that counteracts the inefficiency produced when either photosystem limits the rate of the other. In eukaryotes, these reaction-centre proteins are encoded universally within the chloroplast. Photosynthetic control of chloroplast gene expression indicates an evolutionary explanation for this rule: the redox signal-transduction pathway can be short, the response rapid, and the control direct.

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Figure 1: Reaction-centre stoichiometry and transcription.
Figure 2: Complementary changes in transcription.
Figure 3: Transcription of reaction-centre genes psaAB (photosystem I) and psbA (photosystem II) in chloroplasts isolated from 7-day-old light 2 → 1 and light 1 → 2 plants.
Figure 4: A working hypothesis for photosynthetic control of chloroplast gene expression by redox regulation of transcription.

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Acknowledgements

We thank G. Link for discussions and for providing mustard seeds and DNA probes, and A. Tullberg for assistance with the experiments on isolated chloroplasts. This work was supported by the Swedish Natural Sciences Research Council and the Swedish Council for Co-ordination and Planning of Research. T.P. was the recipient of a postdoctoral fellowship of the Deutsche Forschungsgemeinschaft.

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Correspondence to John F. Allen.

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Pfannschmidt, T., Nilsson, A. & Allen, J. Photosynthetic control of chloroplast gene expression. Nature 397, 625–628 (1999). https://doi.org/10.1038/17624

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