Higher order photoprotection mutants reveal the importance of \u0394pH-dependent photosynthesis-control in preventing light induced damage to both photosystem II and photosystem I

Roberto Barbato,Alessandro Alboresi,Tomas Morosinotto,Virpi Paakkarinen,Carlotta Peracchio,Luca Tadini,Marjaana Suorsa,Azfar Ali Bajwa,Eva-Mari Aro,Paolo Pesaresi,Nicolaj Jeran,Romina Cannata

doi:10.1038/s41598-020-62717-1

Abstract

Although light is essential for photosynthesis, when in excess, it may damage the photosynthetic apparatus, leading to a phenomenon known as photoinhibition. Photoinhibition was thought as a light-induced damage to photosystem II; however, it is now clear that even photosystem I may become very vulnerable to light. One main characteristic of light induced damage to photosystem II (PSII) is the increased turnover of the reaction center protein, D1: when rate of degradation exceeds the rate of synthesis, loss of PSII activity is observed. With respect to photosystem I (PSI), an excess of electrons, instead of an excess of light, may be very dangerous. Plants possess a number of mechanisms able to prevent, or limit, such damages by safe thermal dissipation of light energy (non-photochemical quenching, NPQ), slowing-down of electron transfer through the intersystem transport chain (photosynthesis-control, PSC) in co-operation with the Proton Gradient Regulation (PGR) proteins, PGR5 and PGRL1, collectively called as short-term photoprotection mechanisms, and the redistribution of light between photosystems, called state transitions (responsible of fluorescence quenching at PSII, qT), is superimposed to these short term photoprotective mechanisms. In this manuscript we have generated a number of higher order mutants by crossing genotypes carrying defects in each of the short-term photoprotection mechanisms, with the final aim to obtain a direct comparison of their role and efficiency in photoprotection. We found that mutants carrying a defect in the ΔpH-dependent photosynthesis-control are characterized by photoinhibition of both photosystems, irrespectively of whether PSBS-dependent NPQ or state transitions defects were present or not in the same individual, demonstrating the primary role of PSC in photoprotection. Moreover, mutants with a limited capability to develop a strong PSBS-dependent NPQ, were characterized by a high turnover of the D1 protein and high values of Y(NO), which might reflect energy quenching processes occurring within the PSII reaction center.

Highlights

Photoinhibition of photosynthesis is a long-known phenomenon[1]
Stn[7] stn[8] and ΔSTeM growth rates appear comparable to Col-0 until 14 days after sowing (DAS), whereas they diverge at 18 DAS resulting in rosettes with a decreased size at 24 DAS (Fig. 1A,C)
To confirm the main role of PGR5-PGRL1 protein complex in the formation of the proton motive force, Col-0, npq[], pgr[5], npq[] pgr[5], stn[7] stn[8] and ΔSTeM plant lines were subjected to the kinetic analysis of the electrochromic pigment absorbance shift (ECS) (Fig. 2)

Summary

Introduction

Photoinhibition of photosynthesis is a long-known phenomenon[1]. Due to the discovery of the high turnover D1-protein[2] and its subsequent recognition as a main component of PSII reaction center harboring most of PSII redox cofactors[3,4], photoinhibition was thought as the increase of degradation rate for the D1 over its synthesis or, more in general, as an unbalance between damage and repair of PSII5,6. Electrons from PSI could generate superoxide radicals which, once reduced to hydrogen peroxide, could react with iron-sulfur centers on the acceptor side of the PSI, producing irreversible damages[10] Mutations such as pgr[5], in which the ability to develop a full ΔpH trans-thylakoidal gradient is impaired, make PSI very sensitive to light, both in growth chamber[11,12] and field conditions[12], because of over-reduction of electron acceptors[13]. Owing to the absence of high turnover rates for PSI subunits, damages to this photosystem is very dangerous for plants In this kind of mutants, PSII was found to be highly vulnerable to light[14], to the extent that PSII damage/repair cycle has been proposed as a photoprotection mechanism for PSI15. Even less clear is the relative importance of the different described mechanisms in protecting PSII from photoinhibition, through the high-turnover of the D1 protein

Methods

Results

Conclusion