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. 2013 Oct 29:4:433.
doi: 10.3389/fpls.2013.00433. eCollection 2013.

Quality control of Photosystem II: reversible and irreversible protein aggregation decides the fate of Photosystem II under excessive illumination

Yasusi Yamamoto  1 , Haruka Hori, Suguru Kai, Tomomi Ishikawa, Atsuki Ohnishi, Nodoka Tsumura, Noriko Morita
Affiliations

Quality control of Photosystem II: reversible and irreversible protein aggregation decides the fate of Photosystem II under excessive illumination

Yasusi Yamamoto et al. Front Plant Sci. .

Abstract

In response to excessive light, the thylakoid membranes of higher plant chloroplasts show dynamic changes including the degradation and reassembly of proteins, a change in the distribution of proteins, and large-scale structural changes such as unstacking of the grana. Here, we examined the aggregation of light-harvesting chlorophyll-protein complexes and Photosystem II core subunits of spinach thylakoid membranes under light stress with 77K chlorophyll fluorescence; aggregation of these proteins was found to proceed with increasing light intensity. Measurement of changes in the fluidity of thylakoid membranes with fluorescence polarization of diphenylhexatriene showed that membrane fluidity increased at a light intensity of 500-1,000 μmol photons m(-) (2) s(-) (1), and decreased at very high light intensity (1,500 μmol photons m(-) (2) s(-) (1)). The aggregation of light-harvesting complexes at moderately high light intensity is known to be reversible, while that of Photosystem II core subunits at extremely high light intensity is irreversible. It is likely that the reversibility of protein aggregation is closely related to membrane fluidity: increases in fluidity should stimulate reversible protein aggregation, whereas irreversible protein aggregation might decrease membrane fluidity. When spinach leaves were pre-illuminated with moderately high light intensity, the qE component of non-photochemical quenching and the optimum quantum yield of Photosystem II increased, indicating that Photosystem II/light-harvesting complexes rearranged in the thylakoid membranes to optimize Photosystem II activity. Transmission electron microscopy revealed that the thylakoids underwent partial unstacking under these light stress conditions. Thus, protein aggregation is involved in thylakoid dynamics and regulates photochemical reactions, thereby deciding the fate of Photosystem II.

Keywords: Photosystem II; lipid peroxidation; membrane dynamics; non-photochemical quenching; photoinhibition; protein aggregation; quality control mechanism; thylakoid unstacking.

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Figures

FIGURE 1
FIGURE 1
Chlorophyll fluorescence emission spectra of spinach thylakoids at 77K. (A) A typical fluorescence emission spectrum with Gaussian decompositions from thylakoids kept in the dark. The six main components were identified as F680 (peak, 681 nm), F685 (peak, 685 nm), F695 (peak, 693 nm), F700 (peak, 700 nm), F720 (peak 720 nm), and F735 (peak 735 nm). They correspond to the fluorescence maxima of the trimeric and monomeric forms of LHCII, the PSII reaction center complex, the core antenna complex of PSII, the aggregated trimers of LHCII, the core complex of PSI, and LHCI, respectively. (B) The ratio of F700:F680 at various light intensities. The increase in the ratio under excessive light indicates the conversion of free LHCIIs to aggregated ones. The data are the means of three independent measurements ± S.D. (C) The ratios of F680:F720 (blue), F685:F720 (red), F695:F720 (green), and F700:F720 (purple) at various light intensities. The light-induced decrease in F680:F720 and increase in F700:F720 indicate LHCII aggregation, while decrease in F685:F720 and F695:F720 suggests aggregation between the D1 protein and CP43. We assumed that the level of F720 is constant at various light intensities. The data are the means of three independent measurements ± S.D.
FIGURE 2
FIGURE 2
Assay of the membrane fluidity of spinach thylakoids with fluorescence polarization of diphenylhexatriene (DPH). (A) The chemical structure of DPH. (B) The p-values of DPH fluorescence polarization in thylakoids incubated at different temperatures from 5 to 40°C. Three different colors indicate three independent measurements. The increase and decrease in the p-value indicate a decrease and increase in membrane fluidity, respectively. (C) The p-values of DPH fluorescence polarization in thylakoids illuminated with white light of different intensities at 20°C. The data are the means of three independent measurements ± S.D.
FIGURE 3
FIGURE 3
Effects of pre-illumination of spinach leaves on chlorophyll fluorescence parameters Fv/Fm, NPQ, and qE. These parameters were measured with a Mini-PAM chlorophyll fluorometer (Walz, Germany). (A) A typical time course of fluorescence measurement for NPQ and qE. The light intensity of the continuous illumination was 600 μmol photons m-2 s-1, and during the illumination several saturating flashes were given to estimate the formation of qE. After continuous illumination, another series of saturating flashes was given to the sample and the fluorescence intensity induced by the flash at the 4 min point in the dark period was used to calculate qE. (B) The effects of pre-illumination of spinach leaves at various temperatures on Fv/Fm. The data are the means of three independent measurements ± S.D. (C) The effects of pre-illumination of spinach leaves at 20 °C on NPQ and qE. The data are the means of three independent measurements ± S.D.
FIGURE 4
FIGURE 4
Changes in thylakoid stacking in the chloroplasts after strong illumination of spinach leaves. (A) A diagram showing possible structural changes in the grana after illumination. Models A, B and C correspond to light-induced unstacking of the grana, shrinkage of the grana and bending of the stromal thylakoids outward. (B) Electron micrographs obtained by TEM. Model C in (A), which shows partial thylakoid unstacking, fits best with the present results.
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