Chloroplast proteostasis: A story of birth, life, and death

Gao, Lei; Hong, Zheng-Hui; Wang, Yinsong; Wu, Guo-Zhang

doi:10.1016/j.xplc.2022.100424

Cited by 23 publications

(10 citation statements)

References 300 publications

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“…To demonstrate the application of our OM proximity proteome in a biological discovery context, we focused on protein transport to organelles, which is functionally linked to organellar and cytosolic proteostasis, as well as organellar biogenesis (Gao et al., 2023; Topf et al., 2016; Wrobel et al., 2015). Mitochondria, peroxisomes, and chloroplasts contain several hundred proteins that are critical for their functions, most of which are encoded in the nucleus, synthesized in the cytoplasm, and imported post‐translationally into each organelle through organellar import complexes present in their envelopes.…”

Section: Discussionmentioning

confidence: 99%

Mapping of cytosol‐facing organelle outer membrane proximity proteome by proximity‐dependent biotinylation in living Arabidopsis cells

Bao,

Jia,

Zhang

et al. 2024

The Plant Journal

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SUMMARYThe cytosol‐facing outer membrane (OM) of organelles communicates with other cellular compartments to exchange proteins, metabolites, and signaling molecules. Cellular surveillance systems also target OM‐resident proteins to control organellar homeostasis and ensure cell survival under stress. However, the OM proximity proteomes have never been mapped in plant cells since using traditional approaches to discover OM proteins and identify their dynamically interacting partners remains challenging. In this study, we developed an OM proximity labeling (OMPL) system using biotin ligase‐mediated proximity biotinylation to identify the proximity proteins of the OMs of mitochondria, chloroplasts, and peroxisomes in living Arabidopsis (Arabidopsis thaliana) cells. Using this approach, we mapped the OM proximity proteome of these three organelles under normal conditions and examined the effects of the ultraviolet‐B (UV‐B) or high light (HL) stress on the abundances of OM proximity proteins. We demonstrate the power of this system with the discovery of cytosolic factors and OM receptor candidates potentially involved in local protein translation and translocation. The candidate proteins that are involved in mitochondrion–peroxisome, mitochondrion–chloroplast, or peroxisome–chloroplast contacts, and in the organellar quality control system are also proposed based on OMPL analysis. OMPL‐generated OM proximity proteomes are valuable sources of candidates for functional validation and suggest directions for further investigation of important questions in cell biology.

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Section: Discussionmentioning

confidence: 99%

Mapping of cytosol‐facing organelle outer membrane proximity proteome by proximity‐dependent biotinylation in living Arabidopsis cells

Bao,

Jia,

Zhang

et al. 2024

The Plant Journal

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show abstract

“…To demonstrate the application of our OM proximity proteomes in a biological discovery context, we focused on protein transport to organelles, which is functionally linked to organellar and cytosolic protostasis, as well as organellar biogenesis (Gao et al, 2023; Topf et al, 2016; Wrobel et al, 2015). Mitochondria, peroxisomes and chloroplasts contain several hundred proteins that are critical for their functions, most of which are encoded in the nucleus, synthesized in the cytoplasm, and imported post-translationally into each organelle through organellar import complexes present in their envelopes.…”

Section: Discussionmentioning

confidence: 99%

A proximity-dependent biotinylation map of cytosol-facing organelle outer membrane proteome in living Arabidopsis cells

Bao

Jia

Zhang

et al. 2023

Preprint

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The cytosol-facing outer membrane (OM) of organelles communicates with other cellular compartments to exchange proteins, metabolites and signaling molecules. Cellular surveillance systems also target OM-resident proteins to control organellar homeostasis and ensure cell survival under stress. Using traditional approaches to discover OM proteins and identify their dynamically interacting partners remains challenging. In this study, we developed an OM proximity labeling (OMPL) system using biotin ligase-mediated proximity biotinylation to map the proximity proteome of the OMs of mitochondria, chloroplasts, and peroxisomes in living Arabidopsis (Arabidopsis thaliana) cells. We demonstrate the power of this system with the discovery of cytosolic factors and OM receptor candidates involved in local protein translation and translocation, membrane contact sites, and organelle quality control. This system also performed admirably for the rapid isolation of intact mitochondria and peroxisomes. Our data support the notion that TOM20-3 is a candidate for both a mitochondrial and a chloroplast receptor, and that PEX11D is a candidate for a peroxisome receptor for the coupling of protein translation and import. OMPL-generated OM proximity proteomes are valuable sources of candidates for functional validation and suggest directions for further investigation of important questions in cell biology.

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“…CLP, CGEP, SPP, PREP1,2, OOP, various aminopeptidases) as well as the inner envelope membrane ( e.g. FTSH7,8,9,11,12 and rhomboids) (Gao et al ., 2023; Llamas and Pulido, 2022; Majsec et al ., 2017; Nishimura et al ., 2016). Intra-chloroplast proteolysis is complemented by chlorophagy and other extra-chloroplast proteolytic pathways in which chloroplast proteins are degraded in the cytosol or vacuole (Fu et al, 2022; Izumi and Nakamura, 2018; Woodson, 2022).…”

Section: Introductionmentioning

confidence: 99%

“…INTRODUCTION Intra-chloroplast proteolysis is a key part of chloroplast proteostasis and plays a crucial role in the development and function of chloroplasts (Gao et al, 2023;Llamas and Pulido, 2022;Majsec et al, 2017;Nishimura et al, 2016). Chloroplasts contain several dozen different proteases organized as either homomeric proteins or organized into heteromeric complexes.…”

mentioning

confidence: 99%

Stromal DUF760-1 and DUF760-2 proteins are degraded by the chloroplast Clp protease system but have very different half-lives

Yuan,

van Wijk

2024

Preprint

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The chloroplast AAA+ chaperone CLPC1 aids to select, unfold and deliver hundreds of proteins to the stromal CLP protease core complex for degradation. Through in vivo CLPC1 trapping we previously identified dozens of trapped proteins that are substrate adaptors (e.g. CLPS1 and CLPF), other chaperones (CLPC2 and CLPD) or (potential) substrates (e.g. RH3) for the CLP chaperone-protease system. Here we show that two of these highly trapped proteins, DUF760-1 and DUF760-2, are substrates for the chloroplast CLP protease system. In planta BiFC and yeast-2-hybrid analyses show that both DUF760 proteins can directly interact with the N-domain of CLPC1. Immunoblotting and confocal microscopy analysis demonstrates that both DUF760 proteins are highly enriched in clpc1-1 and clpr2-1 loss-of function mutants. In vivo cycloheximide chase assays in different genetic backgrounds show that DUF760-1 and 2 are both degraded by the chloroplast CLP protease. The half-life of DUF760-1 is 4-6 hours, whereas DUF760-2 is so unstable that it is very hard to detect unless degradation is inhibited in CLP loss-of-function alleles. Null mutants for DUF760-1 and DUF760-2 show weak but differential pigment phenotypes and differential sensitivity of protein translation inhibitors. The functions of these DUF760 proteins are unknown; the lack of shared mRNA co-expressors and the large difference in half-life and protein abundance, suggest that they play different roles within the chloroplast. Taken together, our results demonstrate that DUF760-1 and 2 are newly discovered substrates of CLP chaperone-protease system.

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Chloroplast proteostasis: A story of birth, life, and death

Cited by 23 publications

References 300 publications

Mapping of cytosol‐facing organelle outer membrane proximity proteome by proximity‐dependent biotinylation in living Arabidopsis cells

Mapping of cytosol‐facing organelle outer membrane proximity proteome by proximity‐dependent biotinylation in living Arabidopsis cells

A proximity-dependent biotinylation map of cytosol-facing organelle outer membrane proteome in living Arabidopsis cells

Stromal DUF760-1 and DUF760-2 proteins are degraded by the chloroplast Clp protease system but have very different half-lives

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