TY - JOUR

T1 - Balancing the two photosystems

T2 - photosynthetic electron transfer governs transcription of reaction centre genes in chloroplasts

AU - Allen, J F

AU - Pfannschmidt, T

PY - 2000/10/29

Y1 - 2000/10/29

N2 - Chloroplasts are cytoplasmic organelles whose primary function is photosynthesis, but which also contain small, specialized and quasi-autonomous genetic systems. In photosynthesis, two energy converting photosystems are connected, electrochemically, in series. The connecting electron carriers are oxidized by photosystem I (PS I) and reduced by photosystem II (PS II). It has recently been shown that the oxidation reduction state of one connecting electron carrier, plastoquinone, controls transcription of chloroplast genes for reaction centre proteins of the two photosystems. The control counteracts the imbalance in electron transport that causes it: oxidized plastoquinone induces PS II and represses PS I; reduced plastoquinone induces PS I and represses PS II. This complementarity is observed both in vivo, using light favouring one or other photosystem, and in vitro, when site-specific electron transport inhibitors are added to transcriptionally and photosynthetically active chloroplasts. There is thus a transcriptional level of control that has a regulatory function similar to that of purely post-translational 'state transitions' in which the redistribution of absorbed excitation energy between photosystems is mediated by thylakoid membrane protein phosphorylation. The changes in rates of transcription that are induced by spectral changes in vivo can be detected even before the corresponding state transitions are complete, suggesting the operation of a branched pathway of redox signal transduction. These findings suggest a mechanism for adjustment of photosystem stoichiometry in which initial events involve a sensor of the redox state of plastoquinone, and may thus be the same as the initial events of state transitions. Redox control of chloroplast transcription is also consistent with the proposal that a direct regulatory coupling between electron transport and gene expression determines the function and composition of the chloroplast's extra-nuclear genetic system.

AB - Chloroplasts are cytoplasmic organelles whose primary function is photosynthesis, but which also contain small, specialized and quasi-autonomous genetic systems. In photosynthesis, two energy converting photosystems are connected, electrochemically, in series. The connecting electron carriers are oxidized by photosystem I (PS I) and reduced by photosystem II (PS II). It has recently been shown that the oxidation reduction state of one connecting electron carrier, plastoquinone, controls transcription of chloroplast genes for reaction centre proteins of the two photosystems. The control counteracts the imbalance in electron transport that causes it: oxidized plastoquinone induces PS II and represses PS I; reduced plastoquinone induces PS I and represses PS II. This complementarity is observed both in vivo, using light favouring one or other photosystem, and in vitro, when site-specific electron transport inhibitors are added to transcriptionally and photosynthetically active chloroplasts. There is thus a transcriptional level of control that has a regulatory function similar to that of purely post-translational 'state transitions' in which the redistribution of absorbed excitation energy between photosystems is mediated by thylakoid membrane protein phosphorylation. The changes in rates of transcription that are induced by spectral changes in vivo can be detected even before the corresponding state transitions are complete, suggesting the operation of a branched pathway of redox signal transduction. These findings suggest a mechanism for adjustment of photosystem stoichiometry in which initial events involve a sensor of the redox state of plastoquinone, and may thus be the same as the initial events of state transitions. Redox control of chloroplast transcription is also consistent with the proposal that a direct regulatory coupling between electron transport and gene expression determines the function and composition of the chloroplast's extra-nuclear genetic system.

KW - Animals

KW - Chloroplasts/metabolism

KW - Electron Transport

KW - Gene Expression Regulation, Plant

KW - Genes, Plant

KW - Genome, Plant

KW - Oxidation-Reduction

KW - Photosynthesis/physiology

KW - Photosynthetic Reaction Center Complex Proteins/genetics

KW - Photosystem I Protein Complex

KW - Photosystem II Protein Complex

KW - Plastoquinone/metabolism

KW - Transcription, Genetic

U2 - 10.1098/rstb.2000.0697

DO - 10.1098/rstb.2000.0697

M3 - Review article

C2 - 11127990

VL - 355

SP - 1351

EP - 1359

JO - Philosophical Transactions of the Royal Society B: Biological Sciences

JF - Philosophical Transactions of the Royal Society B: Biological Sciences

SN - 0962-8436

IS - 1402

ER -