Phosphorylation of photosystem II core proteins prevents undesirable cleavage of D1 and contributes to the fine‐tuned repair of photosystem II

Abstract

SUMMARYPhotosystem II (PSII) is a primary target for light-induced damage in photosynthetic protein complexes. To avoid photoinhibition, chloroplasts have evolved a repair cycle with efficient degradation of the PSII reaction center protein, D1, by the proteases FtsH and Deg. Earlier reports have described that phosphorylated D1 is a poor substrate for proteolysis, suggesting a mechanistic role for protein phosphorylation in PSII quality control, but its precise role remains elusive. STN8, a protein kinase, plays a central role in this phosphorylation process. To elucidate the relationship between phosphorylation of D1 and the protease function we assessed in this study the involvement of STN8, using Arabidopsis thaliana mutants lacking FtsH2 [yellow variegated2 (var2)] and Deg5/Deg8 (deg5 deg8). In support of our presumption we found that phosphorylation of D1 increased more in var2. Furthermore, the coexistence of var2 and stn8 was shown to recover the delay in degradation of D1, resulting in mitigation of the high vulnerability to photoinhibition of var2. Partial D1 cleavage fragments that depended on Deg proteases tended to increase, with concomitant accumulation of reactive oxygen species in the mutants lacking STN8. We inferred that the accelerated degradation of D1 in var2 stn8 presents a tradeoff in that it improved the repair of PSII but simultaneously enhanced oxidative stress. Together, these results suggest that PSII core phosphorylation prevents undesirable cleavage of D1 by Deg proteases, which causes cytotoxicity, thereby balancing efficient linear electron flow and photo-oxidative damage. We propose that PSII core phosphorylation contributes to fine-tuned degradation of D1.

A megacomplex composed of both photosystem reaction centres in higher plants

“…4a, G), which reflects reformation of PSI-PSII complexes. It has been suggested that phosphorylation of LHC and PSII core components is involved in the migration of photosystems between grana stack and stroma thylakoid regions 18 . To investigate the role of phosphorylation of these proteins, we examined the delayed fluorescence of mutants defective in the phosphorylation of individual proteins.…”

Down-regulation of specific plastid ribosomal proteins suppresses thf1 leaf variegation, implying a role of THF1 in plastid gene expression

“…It has been demonstrated that the FtsH protease is composed of type A (FtsH1 and FtsH5) and type B (FtsH2 and FtsH8) proteins, and the subunits in the same type are functional redundancy, while those in the different type are not interchangeable (Sakamoto 2003;Yu et al 2004;Zaltsman et al 2005). The well-known function of the FtsH protease is to degrade D1 protein during PSII repair (Yu et al 2004;Kato et al 2009Kato et al , 2012Kato and Sakamoto 2014). However, available evidence suggests that the role of FtsH2/ VAR2 in chloroplast development is independent of its protease activity on D1 degradation (Zaltsman et al 2005;Zhang et al 2009;Kato et al 2009Kato et al , 2012Kato and Sakamoto 2014).…”

Chloroplast Proteases: Updates on Proteolysis within and across Suborganellar Compartments

“…These observations have led to the idea that PSII phosphorylation prevents excessive D1 degradation to avoid the accumulation of cytotoxic cleavage intermediates. Furthermore, given that phosphorylation of PSII core proteins can promote PSII migration and disassembly through structural remodeling of the thylakoid membrane to facilitate D1 access to the proteases (Kirchhoff, 2013), it is plausible that PSII phosphorylation fine-tunes the repair cycle by balancing D1 presentation and degradation (Kato and Sakamoto, 2014). How PSII phosphorylation modulates D1 proteolysis requires further investigation.…”

“…The phosphorylation and dephosphorylation of these proteins require the thylakoid-associated Ser/Thr kinase STATE TRANSITION8 (STN8; Bonardi et al, 2005) and the stroma/thylakoid-localized PROTEIN PHOSPHATASE 2C-TYPE PSII CORE PHOSPHA-TASE (PBCP; Samol et al, 2012). Lack of STN8 results in enhanced Deg-dependent D1 fragmentation under high-light conditions (Kato and Sakamoto, 2014), whereas PBCP defects cause delayed D1 degradation in high light (Samol et al, 2012). Levels of smaller, intermediary D1 fragments are correlated with ROS accumulation, suggestive of their cytotoxicity.…”