Quality Control of PSII: Behavior of PSII in the Highly Crowded Grana Thylakoids Under Excessive Light

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

doi:10.1093/pcp/pcu043

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.

Highlights

Plants respond to long-term change in light conditions, such as seasonal or locational variation in light intensity, by acclimation, whereas short-term, ever-changing light conditions may sometimes cause excessive irradiation of plants and result in short-term light stress
We provide an overview of the processes by which PSII avoids and tolerates light stress, and discuss the role of membrane fluidity in regulation of the movement of PSII/light-harvesting Chl a/b–protein complex of PSII (LHCII), which is responsible for photoprotective processes
If singlet oxygen (1O2) is generated in leaves or cells under weak illumination in vivo, it may indicate that irreversible protein aggregation that takes place in a wide range of light intensities may damage the qE process of non-photochemical quenching of Chl fluorescence (NPQ), in which aggregation of LHCII becomes irreversible through oxidation of LHCII by 1O2 (Fig. 4)

Summary

Introduction

Plants respond to long-term change in light conditions, such as seasonal or locational variation in light intensity, by acclimation, whereas short-term, ever-changing light conditions may sometimes cause excessive irradiation of plants and result in short-term light stress. Excessive illumination of the thylakoids induces reversible aggregation of LHCII (Horton et al 1991, Duffy et al 2013) and irreversible aggregation of PSII core subunits (Yamamoto 2001, Yamamoto et al 2008). Reversible aggregation of LHCII is observed in thylakoids when excessive light energy is dissipated as heat, where the singlet excited state lifetime of Chl a decreases through qE of NPQ (Muller et al 2001, Holt et al 2004, Johnson et al 2011).

Results

Conclusion