Redox signalling and photosynthetic control of chloroplast gene expression

John F. Allen
School of Biological and Chemical Sciences
Queen Mary, University of London
Mile End Road

E1 4NS

The light reactions of photosynthesis consist of two photosystems, termed I and II, which drive electron transport from water to NADP+, thereby establishing a proton motive force for ATP synthesis. Since photosystem I and photosystem II are connected, electrochemically, in series, their rates of electron transport must be equal for linear electron flow. For maximal efficiency, defined as quantum yield, the ratio of the rates of electron transport through the two photosytems must be equal to the ratio of their rates of absorption of light energy, otherwise a fraction of absorbed light energy will be unconverted and will be lost as heat or fluorescence. A purely post-translational means of redistributing light-harvesting capacity between photosystem I and photosystem II appears to maintain quantum yield at low light intensity by eliminating a signal of imbalance in energy distribution [1]. This signal is an excess of either the reduced or oxidised form of plastoquinone, an electron carrier which connects each photosystem with the other. Recent results [2] show that the same signal of imbalance, the redox state of plastoquinone, controls transcription of chloroplast genes encoding the central subunits of each photosynthetic reaction centre. Oxidised plastoquinone is a signal that photosystem II is rate-limiting: it increases transcription of photosystem II reaction centre genes, and decreases transcription of photosystem I reaction centre genes. Reduced plastoquinone, a signal that photosystem I is rate-limiting, has precisely the opposite effect in each case. The changes in transcriptional rate, particularly for photosystem I genes, are remarkably rapid, and can be detected even before the post-translational events of light-harvesting protein phosphorylation are complete [3]. The changes in rate of reaction centre gene transcription are followed by corresponding changes in mRNA quantity, and, in vivo, by corresponding changes in photosystem stoichiometry. It is proposed that the redox regulatory system controlling chloroplast transcription has been conserved, in evolution, from the prokaryotic ancestor of the chloroplast [4]. This redox control of transcription exemplifies a proposed function for the extra-nuclear, cytoplasmic genetic systems of chloroplasts and mitochondria [5].

1. Nilsson, A., Stys, D., Drakenberg, T., Spangfort, M. D., Forsén, S. and Allen, J. F. (1997) J. Biol. Chem. 272, 18350-18357

2. Pfannschmidt, T., Nilsson, A. and Allen, J. F. (1999) Nature 397, 625-628

3. Allen, J. F. and Pfannschmidt, T. (2000) Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 355, 1351-1357

4. Puthiyaveetil S, Kavanagh TA, Cain P, Sullivan JA, Newell CA, Gray JC, Robinson C, van der Giezen M, Rogers MB, Allen JF (2008) The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proceedings of the National Academy of Sciences of the United States of America 105: 10061-10066

5. Allen, J. F. (1993) J. Theor. Biol. 165, 609-631

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