Functions of autophagy in chloroplast protein degradation and homeostasis

Abstract

Chloroplasts are defining organelles in plant and algae, which carried out various critical metabolic processes, including photosynthesis. Roles of chloroplast protein homeostasis in plant development and stress adaptation were clearly demonstrated in previous studies, and its maintenance requires internal proteases originated from the prokaryotic ancestor. Recently, increasing evidence revealed that eukaryotic proteolytic pathways, ubiquitin-proteasome system (UPS) and autophagy, are also involved in the turnover of chloroplast proteins, in response to developmental and environmental cues. Notably, chloroplasts can be regulated via the selective degradation of chloroplast materials in a process called chlorophagy. Yet, understandings of the mechanism of chlorophagy are still rudimentary, particularly regarding its initiation and operation. Here we provide an updated overview of autophagy pathways for chloroplast protein degradation and discuss their importance for plant physiology. In addition, recent advance in analogous mitophagy in yeast and mammals will also be discussed, which provides clues for further elucidating the mechanism of chlorophagy.

Autophagy regulates plastid reorganization during spermatogenesis in the liverwort Marchantia polymorpha

“…Plastid degradation through autophagy has been intensively analyzed in Arabidopsis thaliana ; it is divided into two types: a piecemeal type in which a portion of the plastid is degraded by autophagy ( Ishida et al., 2008 ; Wang et al., 2013 ; Michaeli et al., 2014 ), and autophagic degradation of entire plastids ( Wada et al., 2009 ; Izumi et al., 2017 ; Nakamura et al., 2018 ). These types of plastid degradation are both dependent on ATG5 activity ( Ishida et al., 2008 ; Wang et al., 2013 ; Michaeli et al., 2014 ; Izumi et al., 2017 ; Nakamura et al., 2018 ) and responsible for normal stress responses ( Izumi and Nakamura, 2018 ; Zhuang and Jiang, 2019 ; Wan and Ling, 2022 ); however, it remains unclear whether autophagy of plastids is involved in cellular differentiation. In this study, we showed that in M. polymorpha , ATG5-dependent autophagic degradation of a portion of the plastid occurs during differentiation from the spermatid to the spermatozoid.…”

“…During spermiogenesis in M. polymorpha , the loss of function of Mp ATG5 did not substantially affect the number of plastids ( Figure 2A ), suggesting that piecemeal plastid degradation occurs in spermatids undergoing spermiogenesis. Although several cargoes for the piecemeal-type autophagic degradation of plastids have been reported ( Izumi and Nakamura, 2018 ; Zhuang and Jiang, 2019 ; Wan and Ling, 2022 ), it remains unknown which components of the plastid are degraded by autophagy during spermiogenesis in M. polymorpha . Although plastid DNA is eliminated during spermiogenesis in M. polymorpha , autophagy is unnecessary for this process, indicating that plastid DNA is not a direct target of autophagy ( Figure 5 ).…”

“…In addition to bulk degradation for metabolic recycling, a wide range of cytoplasmic material is selectively degraded by autophagy in the vacuole/lysosome. The plastid (chloroplast) is a well-known target of selective autophagy in plant cells, which is important for responses to nutrition-limited conditions, senescence, and chloroplast damage ( Izumi and Nakamura, 2018 ; Zhuang and Jiang, 2019 ; Wan and Ling, 2022 ). However, the role of autophagic degradation of plastids in cellular differentiation during plant development remains unknown.…”

Picky eaters: selective autophagy in plant cells

“…The transportation of SSGL bodies is dependent on ATG proteins and was demonstrated with experiments in atg mutants under dark conditions, where starch content was increased, proving the importance of autophagy in degradation of SSGL bodies (Malinova et al., 2018; Wang et al., 2013). The recognition of SSGL bodies share similarities with RCBs, where starch molecules are released through stromules (Wan & Ling, 2022). Importantly, the presence of the marker granule‐bound starch synthase I (GBSSI) distinguished SSGL bodies and its interaction with ATG8 is observed in the autophagosomal membrane (Wang et al., 2013).…”

Selective autophagy regulates chloroplast protein import and promotes plant stress tolerance

“…Two main types of chloroplast autophagy (or called chlorophagy) have been revealed: bulk degradation of Rubisco‐containing bodies during dark‐induced senescence (Ishida et al , 2008; Wada et al , 2009), and degradation of whole photodamaged chloroplasts (Izumi et al , 2017; Nakamura et al , 2018). However, little is known about the roles of selective autophagy in regulating chloroplast proteins (Otegui, 2018), and selective chlorophagy receptors or adaptors have not been identified (Kirkin & Rogov, 2019; Wan & Ling, 2022), with the exception of ATI1, a potential receptor for chloroplast degradation (Avin‐Wittenberg et al , 2012; Michaeli et al , 2014). Moreover, the role of chloroplast autophagy in various abiotic stress, such as heat and UVB, is poorly understood.…”