Diversity of strategies for escaping reactive oxygen species production within photosystem I among land plants: P700 oxidation system is prerequisite for alleviating photoinhibition in photosystem I

Abstract

In land plants, photosystem I (PSI) photoinhibition limits carbon fixation and causes growth defects. In addition, recovery from PSI photoinhibition takes much longer than PSII photoinhibition when the PSI core-complex is degraded by oxidative damage. Accordingly, PSI photoinhibition should be avoided in land plants, and land plants should have evolved mechanisms to prevent PSI photoinhibition. However, such protection mechanisms have not yet been identified, and it remains unclear whether all land plants suffer from PSI photoinhibition in the same way. In the present study, we focused on the susceptibility of PSI to photoinhibition and investigated whether mechanisms of preventing PSI photoinhibition varied among land plant species. To assess the susceptibility of PSI to photoinhibition, we used repetitive short-pulse (rSP) illumination, which specifically induces PSI photoinhibition. Subsequently, we found that land plants possess a wide variety of tolerance mechanisms against PSI photoinhibition. In particular, gymnosperms, ferns and mosses/liverworts exhibited higher tolerance to rSP illumination-induced PSI photoinhibition than angiosperms, and detailed analyses indicated that the tolerance of these groups could be partly attributed to flavodiiron proteins, which protected PSI from photoinhibition by oxidizing the PSI reaction center chlorophyll (P700) as an electron acceptor. Furthermore, we demonstrate, for the first time, that gymnosperms, ferns and mosses/liverworts possess a protection mechanism against photoinhibition of PSI that differs from that of angiosperms.

PROTON GRADIENT REGULATION 5 supports linear electron flow to oxidize photosystem I

“…Furthermore, we also found that inducing Y(ND) under illumination is a major mechanism to lower the risk of PSI photoinhibition in photosynthetic organisms (Shimakawa et al , , Takagi et al ). We named this new mechanism, for avoiding ROS production under illumination, the ‘P700 oxidation system’ (Shimakawa et al , , Takagi et al ).…”

“…That is, maintaining Y(ND) lowers the quantum yield of ROS production in PSI during photosynthesis. In a subsequent study, we found that photosynthetic organisms from cyanobacteria higher plants possess and develop various mechanisms to induce P700 + during photosynthesis (Shaku et al , Shimakawa et al , Takagi et al ). Furthermore, we also found that inducing Y(ND) under illumination is a major mechanism to lower the risk of PSI photoinhibition in photosynthetic organisms (Shimakawa et al , , Takagi et al ).…”

“…In a subsequent study, we found that photosynthetic organisms from cyanobacteria higher plants possess and develop various mechanisms to induce P700 + during photosynthesis (Shaku et al , Shimakawa et al , Takagi et al ). Furthermore, we also found that inducing Y(ND) under illumination is a major mechanism to lower the risk of PSI photoinhibition in photosynthetic organisms (Shimakawa et al , , Takagi et al ). We named this new mechanism, for avoiding ROS production under illumination, the ‘P700 oxidation system’ (Shimakawa et al , , Takagi et al ).…”

“…PSI is a major site of reactive oxygen species (ROS) production during photosynthesis. To avoid ROS production, photosynthetic organisms have developed various mechanisms to stimulate P700 oxidation, which we named the P700 oxidation system (Shimakawa et al , Takagi et al ). At the donor side of PSI, lumenal acidification retards the oxidation of PQH 2 at Cyt b 6 f (Tikhonov ), and P700 oxidation is achieved by limiting electron flow from PSII to PSI.…”

From light capture to metabolic needs, oxygenic photosynthesis is an ever‐expanding field of study in plants, algae and cyanobacteria

“…In photosynthetic electron transport, PSII is the main source of singlet oxygen ( 1 O 2 ) while superoxide (O 2 •− ) is mainly generated at PSI. However, PSI may also generate 1 O 2 when illuminated with repetitive short light pulses of high intensity (Takagi et al ). The molecular mechanism of 1 O 2 generation in PSI is unknown but it has been demonstrated that 1 O 2 in PSII is generated by charge recombination reactions of the primary radical pair, yielding the triplet state of chlorophyll.…”