Rapid regulation of photosynthetic light harvesting in the absence of minor antenna and reaction centre complexes.

Francesco Saccon,Mahendra K Shukla,Vasco Giovagnetti,Alexander V Ruban,Tracy Lawson

doi:10.1093/jxb/eraa126

Abstract

Plants are subject to dramatic fluctuations in the intensity of sunlight throughout the day. When the photosynthetic machinery is exposed to high light, photons are absorbed in excess, potentially leading to oxidative damage of its delicate membrane components. A photoprotective molecular process called non-photochemical quenching (NPQ) is the fastest response carried out in the thylakoid membranes to harmlessly dissipate excess light energy. Despite having been intensely studied, the site and mechanism of this essential regulatory process are still debated. Here, we show that the main NPQ component called energy-dependent quenching (qE) is present in plants with photosynthetic membranes largely enriched in the major trimeric light-harvesting complex (LHC) II, while being deprived of all minor LHCs and most photosystem core proteins. This fast and reversible quenching depends upon thylakoid lumen acidification (ΔpH). Enhancing ΔpH amplifies the extent of the quenching and restores qE in the membranes lacking PSII subunit S protein (PsbS), whereas the carotenoid zeaxanthin modulates the kinetics and amplitude of the quenching. These findings highlight the self-regulatory properties of the photosynthetic light-harvesting membranes in vivo, where the ability to switch reversibly between the harvesting and dissipative states is an intrinsic property of the major LHCII.

Highlights

The ability to regulate the energetic fluxes in the thylakoid membranes is a crucial requisite in plants to cope with changes of environmental variables such as water and nutrient availability, cold, soil salinity, and light irradiance (Anderson et al, 1988; Kramer et al, 2004; Demmig-Adams et al, 2012)
Numerous studies reported that the quencher in plants is formed in the trimeric light-harvesting complexes (LHC) II (Ruban et al, 2012, qE in the major LHCII | 3627 and references therein), which represent the main fraction of pigment-binding antenna proteins serving PSII
The separation of lincomycin-treated thylakoid membranes by sucrose density gradient ultracentrifugation revealed the presence of only one pigmented band of antenna complexes, corresponding to the major LHCII trimers (Dall’Osto et al, 2014) (Fig. 1A)

Summary

Introduction

The ability to regulate the energetic fluxes in the thylakoid membranes is a crucial requisite in plants to cope with changes of environmental variables such as water and nutrient availability, cold, soil salinity, and light irradiance (Anderson et al, 1988; Kramer et al, 2004; Demmig-Adams et al, 2012). Numerous studies reported that the quencher in plants is formed in the trimeric light-harvesting complexes (LHC) II (encoded by the Lhcb1–Lhcb genes) (Ruban et al, 2012, qE in the major LHCII | 3627 and references therein), which represent the main fraction of pigment-binding antenna proteins serving PSII. In this context, a ‘LHCII aggregation’ model has been postulated, suggesting that qE originates from conformational changes in the LHCII that result in protein–protein interactions and consequent stabilization of the dissipative conformation (Horton et al, 1991; Ruban, 2018). An additional qE site has been identified within the PSII, accounting for only a minor fraction of the process (Finazzi et al, 2004; Dall’Osto et al, 2017; Nicol et al, 2019)

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Conclusion