Regulation of chloroplast protein degradation

Chloroplasts serve as the machinery not only for photosynthesis, but also for the synthesis of metabolites, such as tetrapyrroles, isoprenoids, starch, fatty acids. Moreover, chloroplasts are important organelles for plant cells responding to environmental signals and regulating plant growth and development (Mamaeva et al., 2020; Song et al., 2021). In plant cells, chloroplasts are semi-autonomous organelles derived from an ancestor of cyanobacteria through endosymbiosis, and retained their own plastid genome (plastome) (Mechela et al., 2019). In terms of cellular structure, chloroplasts are enveloped by two concentric inner and outer envelopes, which contain the stroma and thylakoids. The outer envelope, inner envelope, and thylakoid membrane separate chloroplasts into three independent compartments, including intermembrane space, stroma, and lumen. In addition, there are special structures such as plastoglobuli and stromules formed in chloroplast with unique roles during chloroplast development and environmental responses (Kirchhoff, 2019; Song et al., 2021).

Typically, chloroplasts arise from undeveloped proplastids or etioplasts which developed in darkness. During chloroplast differentiation, thylakoids are initially formed and stacked into grana in a light-dependent manner. The thylakoids are the site of the light reactions where photosynthetic protein complex located and thus regarded as essential structures in chloroplasts. The cooperation between chloroplast genome and nuclear genome is crucial for chloroplast development and thylakoids formation (Pogson et al., 2015). For the chloroplast proteome, only about 100 proteins are encoded by plastome while nearly 3000 proteins are nuclear-encoded and synthesized in the cytosol as precursors (Llamas and Pulido, 2022; Rochaix, 2022). It is constantly challenging for numerous proteins transport, processing, targeting, and assembly especially in changeable environments. The import of nuclear-encoded preproteins into chloroplasts is regulated by translocon complex at the outer and inner chloroplast envelope (TOC-TIC complex) and a series of chaperones such as heat shock proteins. Most mutants of their encoding genes are embryo lethal (Jarvis and López-Juez, 2013), suggesting that protein import and quality control must perform precisely during chloroplast and thylakoid biogenesis. During the assembly of thylakoid, photosynthetic proteins target to thylakoids through protein translocation pathways including both the secretory (Sec) pathway and the twin-arginine translocation (Tat) pathways for lumenal proteins, and signal recognition particle (SRP)-dependent pathway for thylakoid membrane proteins (Day and Theg, 2018). The components of thylakoid also can be transported as cargos through plastid vesicles. Several Arabidopsis proteins are shown functioning in thylakoid biogenesis and vesicle transport (Mechela et al., 2019). For example, the thylakoid formation protein 1 (THF1) controls the important process of vesicle-mediated thylakoid stacks (Wang et al., 2004), and the vesicle-inducing protein in plastids 1 (VIPP1) has a critical function in constructing thylakoid membrane system (Zhang et al., 2012).

During senescence, chloroplasts initiate dismantling which involving overall degradation processes, such as cell wall collapse, chlorophyll breakdown, lipid catabolism, and proteolysis (Dominguez and Cejudo, 2021). The rate of senescence-associated protein degradation is significantly increased by the action of multiple up-regulated proteolytic enzymes (Roberts et al., 2012). Chloroplast dismantling signifies that the photosystem complexes, such as photosystem II (PSII), have to lose their repair system performed in functional chloroplasts, and be removed irreversibly. It is likely that excess oxidative damage incapacitates the repair system during senescence (Krieger-Liszkay et al., 2019). In addition, two key photosynthetic complexes, light-harvesting complex II (LHCII) and Rubisco, are most abundant in membrane protein and soluble protein, respectively, and need to be efficiently degraded during chloroplast dismantling (Kirchhoff, 2019). Despite it is unclear about the detailed mechanism of senescence-mediated LHCII degradation, Chlorophyll b degradation and three enzymes of the chlorophyll cycle are supposed to regulate the LHC complex turnover during senescence (Tanaka and Tanaka, 2011). A recent study shows that a barley cysteine protease HvPAP14 participates in the degradation of LHCII proteins LHCB1 and LHCB5 (Frank et al., 2019). Intriguingly, THF1 also regulates the dynamics of PSII-LHCII during dark-induced leaf senescence (Huang et al., 2013). Contrastingly, degradation of Rubisco, the enzyme that catalyzes initial reaction of carbon assimilation, mainly involves the autophagy-dependent pathway (Ishida et al., 2014), by which Rubisco is ultimately removed into vacuole as autophagosomes (Dominguez and Cejudo, 2021).

Chloroplasts also act as sensors to integrate various environmental stimuli and provoke corresponding response. On this account, the chloroplast stress adaptation motivates broad proteome remodeling (Watson et al., 2018). Stress conditions mediate the generation of ROS (including singlet oxygen and hydrogen peroxide) (Zhu, 2016; Watson et al., 2018; Shi et al., 2022), and induce chloroplast proteins damage, misfold, or post-translationally modification (Mamaeva et al., 2020), which disturb chloroplast proteostasis (Bouchnak and van Wijk, 2021). Particularly, high light stress impacting on chloroplast protein turnover was well-studied involving a collection of protein degradation and photosystem repair mechanisms. Under high light stress major chloroplastic proteases are up-regulated to participate in the rapid turnover of photodamaged proteins (Mamaeva et al., 2020). High light injures chloroplast and results in the whole degradation by autophagy pathway termed chlorophagy (Izumi et al., 2017; Nakamura et al., 2018). Additionally, chloroplast proteins can be ubiquitinated under oxidative stress and degraded by proteasome (Li et al., 2022). Thus, stress induced chloroplast proteostasis involves protease activity (Wang et al., 2016; Dogra et al., 2022), chlorophagy (Dominguez and Cejudo, 2021), and ubiquitin-proteasome system (Li et al., 2022).

Impaired protein abundance and quality adversely affect chloroplast development, function and even plant survival (Nishimura et al., 2017; Fu et al., 2022). Meanwhile, misfolded or damaged proteins are dysfunctional and need to be refolded or degraded to guarantee the normal function of chloroplasts. Hence, during chloroplast development and responding to stresses, the robust protein quality control systems are essential for regulation of proteostasis, which safeguards the integrity of chloroplast proteome by a range of pathways (Llamas and Pulido, 2022). Here we review the current trends in chloroplast proteostasis research and discuss updates on chloroplast protein quality control refer to multiple pathways including diverse chloroplast protease system, ubiquitin-proteasome mediated chloroplast protein degradation, and the chloroplast autophagy (chlorophagy). These mechanisms symbiotically play a vital role in chloroplast development and photosynthesis under both normal or stress conditions.

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