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Review
. 2014 Jul;55(7):1206-15.
doi: 10.1093/pcp/pcu043. Epub 2014 Mar 7.

Quality control of PSII: behavior of PSII in the highly crowded grana thylakoids under excessive light

Yasusi Yamamoto  1 , Suguru Kai  2 , Atsuki Ohnishi  2 , Nodoka Tsumura  2 , Tomomi Ishikawa  2 , Haruka Hori  2 , Noriko Morita  2 , Yasuo Ishikawa  2
Affiliations
Review

Quality control of PSII: behavior of PSII in the highly crowded grana thylakoids under excessive light

Yasusi Yamamoto et al. Plant Cell Physiol. 2014 Jul.

Abstract

The grana thylakoids of higher plant chloroplasts are crowded with PSII and the associated light-harvesting complexes (LHCIIs). They constitute supercomplexes, and often form semi-crystalline arrays in the grana. The crowded condition of the grana may be necessary for efficient trapping of excitation energy by LHCII under weak light, but it might hinder proper movement of LHCII necessary for reversible aggregation of LHCII in the energy-dependent quenching of Chl fluorescence under moderate high light. When the thylakoids are illuminated with extreme high light, the reaction center-binding D1 protein of PSII is photodamaged, and the damaged protein migrates to the grana margins for degradation and subsequent repair. In both moderate and extreme high-light conditions, fluidity of the thylakoid membrane is crucial. In this review, we first provide an overview of photoprotective processes, then discuss changes in membrane fluidity and mobility of the protein complexes in the grana under excessive light, which are closely associated with photoprotection of PSII. We hypothesize that reversible aggregation of LHCII, which is necessary to avoid light stress under moderate high light, and swift turnover of the photodamaged D1 protein under extreme high light are threatened by irreversible protein aggregation induced by reactive oxygen species in photochemical reactions.

Keywords: Light stress; Membrane crowdedness; Non-photochemical quenching; Photoinhibition; Photosystem II; Protein aggregation.

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Figures

Fig. 1
Fig. 1
Light response curve for PSII activity. The solid line shows PSII activity at various light intensities, while the broken line represents the input energy, or PSII activity in the absence of any rate-limiting factors. (A) Energy usage in PSII. The gray shaded area represents excessive light energy. The area below the solid line corresponds to the energy used for photosynthesis. (B) Relationship between qE of NPQ and photoinhibition of PSII in the light–response curve. Under low light, PSII activity increases in proportion to the light intensity. No light stress is likely under this condition (indicated by the blue arrow). With increasing light intensity, PSII activity gradually decreases and reaches a plateau. Under these conditions, chloroplasts avoid light stress using the qE mechanism of NPQ (indicated by the orange arrow). The qE takes place through aggregation of LHCII activated by acidification of the thylakoid lumen and zeaxanthin formation by the xanthophyll cycle, and it acts to dissipate excessive light energy as heat. Under high-intensity light, photoinhibition prevails. PSII tolerates the severe light stress by stimulating damage and repair of the reaction center-binding D1 protein (indicated by the red arrow).
Fig. 2
Fig. 2
Chl fluorescence emission spectra of spinach thylakoids at 77K. The excitation wavelength was 435 nm and the band width was 20 nm. The emission wavelength was 650–750 nm and the band width was 2.5 nm. The typical fluorescence emission spectra (green curves) are shown with Gaussian decompositions. The curve with little noise is the original fluorescence emission spectrum, while the smooth curve corresponds to the sum of the six Gaussian curves showing the validity of the decomposition results. Six main components were identified in accordance with Stoitchkova et al. (2006) and are referred to as F680 (red curves: peak, 681 nm; half band width, 10.1 nm), F685 (green-yellow curves: peak, 685 nm; half band width, 9.3 nm), F695 (blue-purple curves: peak, 693 nm; half band width, 9.2 nm), F700 (orange curves: peak, 700 nm; half band width, 15.8 nm), F720 (blue curves: peak 720 nm; half band width, 21.9 nm) and F735 (red-purple curves: peak 735 nm; half band width 23.4 nm), respectively. The curves correspond to the fluorescence maxima of the trimeric and monomeric forms of LHCII (F680), the PSII reaction center complex (F685), the core antenna complex of PSII (F695), the aggregated trimers of LHCII (F700), the core complex of PSI (F720) and LHCI (F735). Low emission of PSI fluorescence at the long wavelength is the consequence of a decrease in the quantum efficiency of the photomultiplier used in the fluorescence spectrophotometer. (A) Fluorescence from thylakoids incubated in the dark. (B) Fluorescence from thylakoids illuminated with high light (light intensity: 1,000 µmol photons m−2 s−1). An increase in the ratio of F700:F680 at high light indicates conversion of free LHCIIs to aggregated LHCIIs.
Fig. 3
Fig. 3
Schematic diagram of the events occurring in the grana and stroma thylakoids under excessive illumination. A horizontal view of the stacked thylakoids is shown. PSII/LHCII supercomplexes (light red) are abundant in the grana regions (LHCII complexes are omitted in this figure). Upon excessive illumination, a portion of the PSII proteins including the reaction center-binding D1 protein is phosphorylated (shown as ‘P’), which protects the proteins from photodamage. However, once PSII complexes, which are present as dimers, are damaged by excessive light (shown by ‘X’), they move to the grana margins, are disintegrated into monomers, and the damaged D1 proteins are dephosphorylated by phosphatases (orange) located in the grana margins. The D1 proteins are then degraded by proteases including FtsH (purple) that are also located in the grana margins. A portion of the photodamaged PSII complexes in the grana (dar red) are immobilized by irreversible protein aggregation. To facilitate degradation of the photodamaged D1 protein in the grana margins, partial unstacking of the thylakoids may be necessary, because it may increase the area of the grana margins and also stimulate mobilization of PSII complexes and the proteases responsible for proteolysis.
Fig. 4
Fig. 4
Schematic diagram of events taking place in the grana and stroma thylakoids under excessive illumination. This diagram shows a top view of a thylakoid (light blue), which has a rounded shape and is stacked with other thylakoids to form the grana. Here, two grana-forming thylakoid domains are depicted (left, dark control; right, illuminated with high light), which are interconnected by a stroma thylakoid. PSII core complexes (blue) are surrounded by LHCII complexes (green). When the thylakoids are illuminated with high light, the PSII/LHCII complexes are mobilized, probably by phosphorylation, and LHCII complexes form reversible aggregates to dissipate the excess light energy as heat. Simultaneously, free spaces are generated in the grana and the damaged PSII complexes move to the grana margin regions to react with proteases such as FtsH (orange) using these free spaces. However, when the light intensity is extremely high, 1O2 molecules are produced in PSII/LHCII complexes through photochemical reaction or in the lipid matrix through lipid peroxidation, and the reactive oxygen species damage the proteins and lipids to form irreversible aggregates. MDA may also participate in this process. These protein and lipid aggregates hinder the movement of PSII/LHCII complexes on the membranes, and the function of the thylakoids may finally deteriorate.
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References

    1. Albertsson P. A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci. 2001;6:349–358. - PubMed
    1. Allen JF. Protein phosphorylation in regulation of photosynthesis. Biochim. Biophys. Acta. 1992;1098:275–335. - PubMed
    1. Allen JF, Forsberg J. Molecular recognition in thylakoid structure and function. Trends Plant Sci. 2001;6:317–326. - PubMed
    1. Anderson JM. Insights into the consequences of grana stacking of thylakoid membranes in vascular plants: a personal perspective. Aust. J. Plant Physiol. 1999;26:625–639.
    1. Armbruster U, Labs M, Pribil M, Viola S, Xu W, Scharfenberg M, et al. Arabidopsis CURVATURE THYLAKOID1 proteins modify thylakoid architecture by inducing membrane curvature. Plant Cell. 2013;25:2661–2678. - PMC - PubMed

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