FtsH Is Involved in the Early Stages of Repair of Photosystem II inSynechocystissp PCC 6803 [W]

Abstract

When plants, algae, and cyanobacteria are exposed to excessive light, especially in combination with other environmental stress conditions such as extreme temperatures, their photosynthetic performance declines. A major cause of this photoinhibition is the light-induced irreversible photodamage to the photosystem II (PSII) complex responsible for photosynthetic oxygen evolution. A repair cycle operates to selectively replace a damaged D1 subunit within PSII with a newly synthesized copy followed by the light-driven reactivation of the complex. Net loss of PSII activity occurs (photoinhibition) when the rate of damage exceeds the rate of repair. The identities of the chaperones and proteases involved in the replacement of D1 in vivo remain uncertain. Here, we show that one of the four members of the FtsH family of proteases (cyanobase designation slr0228) found in the cyanobacterium Synechocystis sp PCC 6803 is important for the repair of PSII and is vital for preventing chronic photoinhibition. Therefore, the ftsH gene family is not functionally redundant with respect to the repair of PSII in this organism. Our data also indicate that FtsH binds directly to PSII, is involved in the early steps of D1 degradation, and is not restricted to the removal of D1 fragments. These results, together with the recent analysis of ftsH mutants of Arabidopsis, highlight the critical role played by FtsH proteases in the removal of damaged D1 from the membrane and the maintenance of PSII activity in vivo.

Thylakoid Development from Biogenesis to Senescence, and Ruminations on Regulation

“…However, they showed that the fug1 mutation led to a decrease in D1 synthesis, and Bailey et al (2002) previously found that FtsH2 degrades D1 in a light-dependent manner. Silva et al (2003) and Yoshioka et al (2006) provided additional evidence that FtsH proteins are involved in the primary cleavage of photodamaged D1. Miura et al speculate that a balance of synthesis and degradation of D1 protein could be a critical feature of var mutants: the accumulation of photodamaged D1 due to loss of FtsH proteins in var mutants might be a key element in the development of variegated sectors, whereas fug1 might prevent variegation by limiting the accumulation of photodamaged D1.…”

Expression in Multigene Families. Analysis of Chloroplast and Mitochondrial Proteases

“…Clp protease appears to be involved in degradation of unassembled proteins in the stroma (Halperin and Adam, 1996;Halperin et al, 2001a), in degradation of thylakoid membrane proteins in response to nutrient limitation (Majeran et al, 2000), and in shoot development (Kuroda and Maliga, 2003). FtsH is involved in the degradation of unassembled proteins in the thylakoid membrane (Ostersetzer and Adam, 1997), degradation of the oxidatively damaged D1 protein of PSII (Lindahl et al, 2000;Bailey et al, 2002;Sakamoto et al, 2002;Silva et al, 2003), and chloroplast development (Chen et al, 2000;Takechi et al, 2000;Sakamoto et al, 2002). The only reported activity of chloroplast DegP is the initial cleavage of the D1 protein of PSII during repair from photoinhibition .…”

Quality control of Photosystem II: The molecular basis for the action of FtsH protease and the dynamics of the thylakoid membranes

“…Through this and other related works, the D1 protein was suggested to be degraded first by Deg proteases [31], then further degraded by FtsH proteases [36,37]. The FtsH proteases were then suggested as the proteases responsible for the primary cleavage of the D1 protein [35,45]. More recently, the role of Deg proteases was reevaluated in the study of Arabidopsis Deg/FtsH double mutants, and a reversed order of the action of FtsH and lumenal Deg was suggested [32,75].…”

“…PCC6803, where four genes slr1390, slr0228, slr1604 and sll1463 were found to be homologous to the bacterial FtsH (FtsH1, 2, 3 and 4) [45,69,72]. Of the four homologs, FtsH1 and 3 are required for cell viability while FtsH2 and 4 are not essential for the survival of the cyanobacterium [68,69].…”

“…Further studies, however, showed that a mutant lacking the FtsH2 is sensitive to light stress compared with the wild-type protein, and the photodamaged D1 protein was found to accumulate in the mutant thylakoids. A series of works using slr0228 cells demonstrated that FtsH2 is involved in the primary cleavage of the photodamaged D1 protein [35,45,73]. It has been reported that FtsH2 (slr0228) proteases is also involved in the repair of damaged PSII by UV-B radiation [74].…”