Impaired PSII Proteostasis Promotes Retrograde Signaling via Salicylic Acid

Abstract

Photodamage of the PSII reaction center (RC) is an inevitable process in an oxygen-rich environment. The damaged PSII RC proteins (Dam-PSII) undergo degradation via the thylakoid membrane-bound FtsH metalloprotease, followed by posttranslational assembly of PSII. While the effect of Dam-PSII on gene regulation is described for cyanobacteria, its role in land plants is largely unknown. In this study, we reveal an intriguing retrograde signaling pathway by using the Arabidopsis (Arabidopsis thaliana) yellow variegated2-9 mutant, which expresses a mutated FtsH2 (FtsH2 G267D) metalloprotease, specifically impairing its substrate-unfolding activity. This lesion leads to the perturbation of PSII protein homeostasis (proteostasis) and the accumulation of Dam-PSII. Subsequently, this results in an up-regulation of salicylic acid (SA)-responsive genes, which is abrogated by inactivation of either an SA transporter in the chloroplast envelope membrane or extraplastidic SA signaling components as well as by removal of SA. These results suggest that the stress hormone SA, which is mainly synthesized via the chloroplast isochorismate pathway in response to the impaired PSII proteostasis, mediates the retrograde signaling. These findings reinforce the emerging view of chloroplast function toward plant stress responses and suggest SA as a potential plastid factor mediating retrograde signaling. Chloroplast-generated reactive oxygen species (ROS) damage primarily the photosynthetic apparatus, thereby deleteriously affecting plant development. Among ROS, singlet oxygen (1 O 2), mainly generated by PSII, has been considered as a prime cause of PSII damage because of its proximity to PSII (Triantaphylidès et al., 2008; Kato and Sakamoto, 2009). Since 1 O 2 is a known by-product of photosynthesis, PSII reaction center (PSII RC) proteins undergo constant damage in a light-dependent manner (Ohad et al., 1984; Mishra et al., 1994). The damaged PSII (Dam-PSII) becomes repaired via a series of steps: (1) D1 oxidation and subsequent phosphorylation; (2) migration of the Dam-PSII from the grana core (appressed membranes) to the grana margin (nonappressed membranes); (3) dephosphorylation of D1; (4) degradation of the damaged D1 protein by the membrane-bound FtsH metalloprotease; (5) de novo synthesis of D1; and (6) reassembly and subsequent remigration to the grana core (Yamamoto et al., 2013; Yoshioka-Nishimura and Yamamoto, 2014). Accordingly, the impaired PSII repair in Arabidopsis (Arabidopsis thaliana) mutants lacking the membrane-bound FtsH protease leads to the failure of acclimation to a sublethal intensity of

Singlet Oxygen Metabolism: From Genesis to Signaling

“…Besides D1, the D2 protein of the PSII RC also exhibits a decline upon a 1 O 2 burst, indicating probable photodamage of D2 by 1 O 2 (Koivuniemi et al, 1995;Jansen et al, 1999;Edelman and Mattoo, 2008). In accordance, recent studies have demonstrated that the oxidative modification is not limited to D1, but rather all PSII RC proteins including D2, CP43, and CP47 get oxidized by 1 O 2 (Dreaden Kasson et al, 2012;Dogra et al, 2019a;Dogra et al, 2019b;Duan et al, 2019). Though these oxidative modifications might be linked with the turnover, the precise relevance of these modifications in PSII proteins needs to be investigated.…”

ROS-Driven Oxidative Modification: Its Impact on Chloroplasts-Nucleus Communication

“…Among them, FtsH2 and FtsH5 are pivotal for establishing a functional FtsH protease, as evident in the emergence of leaf variegation in the cognate mutant plants (Yu et al, 2005). Besides, the loss of FtsH2 results in the accumulation of damaged PSII proteins relative to wild-type plants and in the failure of survival under very mild light stress conditions wherein wild-type plants can rapidly acclimate (Duan et al, 2019). Not only PSII proteins but also other chloroplast proteins appear to accumulate in the chloroplasts of var2 mutant lacking FtsH2.…”

“…Intriguingly, one var2 allele, var2-9, was found to upregulate not only a suite of genes involved in PQC but also salicylic acidresponsive genes (SRGs) (Duan et al, 2019). var2-9 mutant plants express dysfunctional FtsH2, which specifically impairs the substrate unfolding activity.…”

Chloroplast protein homeostasis is coupled with retrograde signaling

“…24,25 Thus, 1 O 2 generation and PSII damage are considered as default processes during photosynthesis, which tend to increase under photo-oxidative stress conditions. 21,22,26 The damaged PSII continually undergoes a repair process at the non-appressed regions of the thylakoids. The degradation of the damaged PSII RC proteins such as D1 by the FtsH protease is required to promote PSII reassembly.…”

“…21 Moreover, the reinforced PSII proteostasis and the accumulation of damaged proteins appear to promote SA synthesis via the chloroplast-established isochorismate (ICS) pathway. 22 This finding suggests a potential interconnection between the impaired proteostasis (or its related problem such as altered redox status) and the stimulation of the ICS pathway.…”