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Discrete redox signaling pathways regulate photosynthetic light-harvesting and chloroplast gene transcription.

Allen JF, Santabarbara S, Allen CA, Puthiyaveetil S - PLoS ONE (2011)

Bottom Line: We asked whether CSK is also involved in regulation of absorbed light energy distribution by phosphorylation of light-harvesting complex II (LHC II).Chloroplast thylakoid membranes isolated from a CSK T-DNA insertion mutant and from wild-type Arabidopsis thaliana exhibit similar light- and redox-induced (32)P-labelling of LHC II and changes in 77 K chlorophyll fluorescence emission spectra, while room-temperature chlorophyll fluorescence emission transients from Arabidopsis leaves are perturbed by inactivation of CSK.The results indicate indirect, pleiotropic effects of reaction centre gene transcription on regulation of photosynthetic light-harvesting in vivo.

View Article: PubMed Central - PubMed

Affiliation: School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom. j.f.allen@qmul.ac.uk

ABSTRACT
In photosynthesis in chloroplasts, two related regulatory processes balance the actions of photosystems I and II. These processes are short-term, post-translational redistribution of light-harvesting capacity, and long-term adjustment of photosystem stoichiometry initiated by control of chloroplast DNA transcription. Both responses are initiated by changes in the redox state of the electron carrier, plastoquinone, which connects the two photosystems. Chloroplast Sensor Kinase (CSK) is a regulator of transcription of chloroplast genes for reaction centres of the two photosystems, and a sensor of plastoquinone redox state. We asked whether CSK is also involved in regulation of absorbed light energy distribution by phosphorylation of light-harvesting complex II (LHC II). Chloroplast thylakoid membranes isolated from a CSK T-DNA insertion mutant and from wild-type Arabidopsis thaliana exhibit similar light- and redox-induced (32)P-labelling of LHC II and changes in 77 K chlorophyll fluorescence emission spectra, while room-temperature chlorophyll fluorescence emission transients from Arabidopsis leaves are perturbed by inactivation of CSK. The results indicate indirect, pleiotropic effects of reaction centre gene transcription on regulation of photosynthetic light-harvesting in vivo. A single, direct redox signal is transmitted separately to discrete transcriptional and post-translational branches of an integrated cytoplasmic regulatory system.

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Interactions of photosynthetic electron carriers with redox-signalling components of photosystem stoichiometry adjustment and state transitions.Light reactions of photosynthesis are represented as electron transport from H2O to NADP+ via two photosystems connected by a cytochrome b6f complex which oxidizes plastiquinol (PQH2) to plastoquinone (PQ). CSK senses the redox state of the plastoquinone pool directly by becoming autophosphorylated and activated by PQ. CSK phosphorylation and dephosphorylation initiate transcription of PS II reaction centre (psbA,D) and PS I reaction centre (psaA,B) genes, respectively, selectively controlling expression of reaction centre genes in chloroplast DNA. The LHC II kinase Stn7 responds to PQH2 and initiates the state 2 transition, while the phospho-LHC II phosphatase, TAP38/PPH1, is redox-independent and predominates, inducing the state 1 transition, when PQ is oxidized. Even though they are both controlled by plastoquinone redox state, CSK exerts its transcriptional effect on photosystem stoichiometry independently of the effect of Stn7 in state transitions.
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pone-0026372-g004: Interactions of photosynthetic electron carriers with redox-signalling components of photosystem stoichiometry adjustment and state transitions.Light reactions of photosynthesis are represented as electron transport from H2O to NADP+ via two photosystems connected by a cytochrome b6f complex which oxidizes plastiquinol (PQH2) to plastoquinone (PQ). CSK senses the redox state of the plastoquinone pool directly by becoming autophosphorylated and activated by PQ. CSK phosphorylation and dephosphorylation initiate transcription of PS II reaction centre (psbA,D) and PS I reaction centre (psaA,B) genes, respectively, selectively controlling expression of reaction centre genes in chloroplast DNA. The LHC II kinase Stn7 responds to PQH2 and initiates the state 2 transition, while the phospho-LHC II phosphatase, TAP38/PPH1, is redox-independent and predominates, inducing the state 1 transition, when PQ is oxidized. Even though they are both controlled by plastoquinone redox state, CSK exerts its transcriptional effect on photosystem stoichiometry independently of the effect of Stn7 in state transitions.

Mentions: Since CSK is not involved directly in the mechanism of redox sensing in state 1- state 2 transitions (Figures 2 and 3), and a protein kinase known as Stt7/Stn7 has been implicated in state transitions by acting as the LHC II kinase, it seems necessary to assume that a bifurcated redox signalling pathway carries information from the plastoquinone pool, as depicted in Figure 4. One distal branch of the pathway, containing Stt7/Stn7, affects post-translational modification of existing proteins by phosphorylation. The second branch, consisting of CSK, controls photosystem stoichiometry by means of regulation of transcription of chloroplast genes for reaction centre apoproteins. Upstream of the point of divergence of the two branches is plastoquinone itself. It remains to be seen whether two separate plastoquinone/quinol-binding sensors initiate the two signal transduction events, or whether a single plastoquinone-binding redox sensor, as yet unidentified, controls both CSK and the LHC II kinase. The first possibility, that plastoquinone redox state is sensed by two independent redox sensors – CSK and LHC II kinase – is supported by the available evidence and consistent with a recent model for redox control of Stn7 [35].


Discrete redox signaling pathways regulate photosynthetic light-harvesting and chloroplast gene transcription.

Allen JF, Santabarbara S, Allen CA, Puthiyaveetil S - PLoS ONE (2011)

Interactions of photosynthetic electron carriers with redox-signalling components of photosystem stoichiometry adjustment and state transitions.Light reactions of photosynthesis are represented as electron transport from H2O to NADP+ via two photosystems connected by a cytochrome b6f complex which oxidizes plastiquinol (PQH2) to plastoquinone (PQ). CSK senses the redox state of the plastoquinone pool directly by becoming autophosphorylated and activated by PQ. CSK phosphorylation and dephosphorylation initiate transcription of PS II reaction centre (psbA,D) and PS I reaction centre (psaA,B) genes, respectively, selectively controlling expression of reaction centre genes in chloroplast DNA. The LHC II kinase Stn7 responds to PQH2 and initiates the state 2 transition, while the phospho-LHC II phosphatase, TAP38/PPH1, is redox-independent and predominates, inducing the state 1 transition, when PQ is oxidized. Even though they are both controlled by plastoquinone redox state, CSK exerts its transcriptional effect on photosystem stoichiometry independently of the effect of Stn7 in state transitions.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3198397&req=5

pone-0026372-g004: Interactions of photosynthetic electron carriers with redox-signalling components of photosystem stoichiometry adjustment and state transitions.Light reactions of photosynthesis are represented as electron transport from H2O to NADP+ via two photosystems connected by a cytochrome b6f complex which oxidizes plastiquinol (PQH2) to plastoquinone (PQ). CSK senses the redox state of the plastoquinone pool directly by becoming autophosphorylated and activated by PQ. CSK phosphorylation and dephosphorylation initiate transcription of PS II reaction centre (psbA,D) and PS I reaction centre (psaA,B) genes, respectively, selectively controlling expression of reaction centre genes in chloroplast DNA. The LHC II kinase Stn7 responds to PQH2 and initiates the state 2 transition, while the phospho-LHC II phosphatase, TAP38/PPH1, is redox-independent and predominates, inducing the state 1 transition, when PQ is oxidized. Even though they are both controlled by plastoquinone redox state, CSK exerts its transcriptional effect on photosystem stoichiometry independently of the effect of Stn7 in state transitions.
Mentions: Since CSK is not involved directly in the mechanism of redox sensing in state 1- state 2 transitions (Figures 2 and 3), and a protein kinase known as Stt7/Stn7 has been implicated in state transitions by acting as the LHC II kinase, it seems necessary to assume that a bifurcated redox signalling pathway carries information from the plastoquinone pool, as depicted in Figure 4. One distal branch of the pathway, containing Stt7/Stn7, affects post-translational modification of existing proteins by phosphorylation. The second branch, consisting of CSK, controls photosystem stoichiometry by means of regulation of transcription of chloroplast genes for reaction centre apoproteins. Upstream of the point of divergence of the two branches is plastoquinone itself. It remains to be seen whether two separate plastoquinone/quinol-binding sensors initiate the two signal transduction events, or whether a single plastoquinone-binding redox sensor, as yet unidentified, controls both CSK and the LHC II kinase. The first possibility, that plastoquinone redox state is sensed by two independent redox sensors – CSK and LHC II kinase – is supported by the available evidence and consistent with a recent model for redox control of Stn7 [35].

Bottom Line: We asked whether CSK is also involved in regulation of absorbed light energy distribution by phosphorylation of light-harvesting complex II (LHC II).Chloroplast thylakoid membranes isolated from a CSK T-DNA insertion mutant and from wild-type Arabidopsis thaliana exhibit similar light- and redox-induced (32)P-labelling of LHC II and changes in 77 K chlorophyll fluorescence emission spectra, while room-temperature chlorophyll fluorescence emission transients from Arabidopsis leaves are perturbed by inactivation of CSK.The results indicate indirect, pleiotropic effects of reaction centre gene transcription on regulation of photosynthetic light-harvesting in vivo.

View Article: PubMed Central - PubMed

Affiliation: School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom. j.f.allen@qmul.ac.uk

ABSTRACT
In photosynthesis in chloroplasts, two related regulatory processes balance the actions of photosystems I and II. These processes are short-term, post-translational redistribution of light-harvesting capacity, and long-term adjustment of photosystem stoichiometry initiated by control of chloroplast DNA transcription. Both responses are initiated by changes in the redox state of the electron carrier, plastoquinone, which connects the two photosystems. Chloroplast Sensor Kinase (CSK) is a regulator of transcription of chloroplast genes for reaction centres of the two photosystems, and a sensor of plastoquinone redox state. We asked whether CSK is also involved in regulation of absorbed light energy distribution by phosphorylation of light-harvesting complex II (LHC II). Chloroplast thylakoid membranes isolated from a CSK T-DNA insertion mutant and from wild-type Arabidopsis thaliana exhibit similar light- and redox-induced (32)P-labelling of LHC II and changes in 77 K chlorophyll fluorescence emission spectra, while room-temperature chlorophyll fluorescence emission transients from Arabidopsis leaves are perturbed by inactivation of CSK. The results indicate indirect, pleiotropic effects of reaction centre gene transcription on regulation of photosynthetic light-harvesting in vivo. A single, direct redox signal is transmitted separately to discrete transcriptional and post-translational branches of an integrated cytoplasmic regulatory system.

Show MeSH
Related in: MedlinePlus