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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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Fluorescence emission spectra of isolated thylakoids at 77 K.77 K fluorescence emission spectra from wild type and CSK  mutant thylakoids as measured by the Perkin-Elmer LS 55 luminescence spectrometer. Figure 2a and 2c shows fluorescence emission spectra of thylakoids isolated from light 1 adapted plants. Figure 2b and 2d show fluorescence emission spectra of thylakoids isolated from white light grown plants. The excitation wavelength was 435 nm (5 nm slit width) and emission was detected from 650 to 800 nm (2.5 nm slit width). All spectra were normalized at 685 nm.
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pone-0026372-g002: Fluorescence emission spectra of isolated thylakoids at 77 K.77 K fluorescence emission spectra from wild type and CSK mutant thylakoids as measured by the Perkin-Elmer LS 55 luminescence spectrometer. Figure 2a and 2c shows fluorescence emission spectra of thylakoids isolated from light 1 adapted plants. Figure 2b and 2d show fluorescence emission spectra of thylakoids isolated from white light grown plants. The excitation wavelength was 435 nm (5 nm slit width) and emission was detected from 650 to 800 nm (2.5 nm slit width). All spectra were normalized at 685 nm.

Mentions: As a complete interpretation of the steady-state fluorescence emission in presence of actinic background is complicated by the presence of many different physiological processes, we investigated the effect of CSK in the control of state-transitions by fluorescence emission spectroscopy at 77 K of isolated thylakoids. Spectra are shown in Figure 2. In all cases, two principal fluorescence emission maxima are seen, one centred at 685 nm, also associated with a shoulder at ∼700 nm, and arising principally from photosystem II emission and the other, centred at 735 nm, which originates from photosystem I. The intensity of the 685 nm and 735 nm peaks observed at 77 K can be used to estimate the relative absorption cross-section of the two photosystems, and hence on state transitions. The state 2 transition was induced in vitro by illumination of thylakoids in the presence of ATP, and state 1 was produced from thylakoids incubated in the dark with ATP. As a control, thylakoids were incubated in the dark without ATP, and this treatment also induces state 1 (results not shown). It is seen in all cases that the emission ratio F735/F685 is greater in state 2 than in state 1, most noticeably in thylakoids from white light-grown plants (Figure 2b and 2d). However, the effect of the ATP and illumination on excitation energy distribution between photosystems I and II is much the same in the CSK mutant (Figure 2c, 2d) as in the wild-type (Figures 2a, 2b). Thus, neither the Fm values from white light grown plants at room temperature (Figure 1b) nor 77 K fluorescence emission spectra (Figure 2) indicate any effect of the CSK mutation on redistribution of excitation energy in light-state transitions.


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

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

Fluorescence emission spectra of isolated thylakoids at 77 K.77 K fluorescence emission spectra from wild type and CSK  mutant thylakoids as measured by the Perkin-Elmer LS 55 luminescence spectrometer. Figure 2a and 2c shows fluorescence emission spectra of thylakoids isolated from light 1 adapted plants. Figure 2b and 2d show fluorescence emission spectra of thylakoids isolated from white light grown plants. The excitation wavelength was 435 nm (5 nm slit width) and emission was detected from 650 to 800 nm (2.5 nm slit width). All spectra were normalized at 685 nm.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0026372-g002: Fluorescence emission spectra of isolated thylakoids at 77 K.77 K fluorescence emission spectra from wild type and CSK mutant thylakoids as measured by the Perkin-Elmer LS 55 luminescence spectrometer. Figure 2a and 2c shows fluorescence emission spectra of thylakoids isolated from light 1 adapted plants. Figure 2b and 2d show fluorescence emission spectra of thylakoids isolated from white light grown plants. The excitation wavelength was 435 nm (5 nm slit width) and emission was detected from 650 to 800 nm (2.5 nm slit width). All spectra were normalized at 685 nm.
Mentions: As a complete interpretation of the steady-state fluorescence emission in presence of actinic background is complicated by the presence of many different physiological processes, we investigated the effect of CSK in the control of state-transitions by fluorescence emission spectroscopy at 77 K of isolated thylakoids. Spectra are shown in Figure 2. In all cases, two principal fluorescence emission maxima are seen, one centred at 685 nm, also associated with a shoulder at ∼700 nm, and arising principally from photosystem II emission and the other, centred at 735 nm, which originates from photosystem I. The intensity of the 685 nm and 735 nm peaks observed at 77 K can be used to estimate the relative absorption cross-section of the two photosystems, and hence on state transitions. The state 2 transition was induced in vitro by illumination of thylakoids in the presence of ATP, and state 1 was produced from thylakoids incubated in the dark with ATP. As a control, thylakoids were incubated in the dark without ATP, and this treatment also induces state 1 (results not shown). It is seen in all cases that the emission ratio F735/F685 is greater in state 2 than in state 1, most noticeably in thylakoids from white light-grown plants (Figure 2b and 2d). However, the effect of the ATP and illumination on excitation energy distribution between photosystems I and II is much the same in the CSK mutant (Figure 2c, 2d) as in the wild-type (Figures 2a, 2b). Thus, neither the Fm values from white light grown plants at room temperature (Figure 1b) nor 77 K fluorescence emission spectra (Figure 2) indicate any effect of the CSK mutation on redistribution of excitation energy in light-state transitions.

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