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Review
, 15 (1), 118

The Integration of Chloroplast Protein Targeting With Plant Developmental and Stress Responses

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Review

The Integration of Chloroplast Protein Targeting With Plant Developmental and Stress Responses

Lynn G L Richardson et al. BMC Biol.

Abstract

The plastids, including chloroplasts, are a group of interrelated organelles that confer photoautotrophic growth and the unique metabolic capabilities that are characteristic of plant systems. Plastid biogenesis relies on the expression, import, and assembly of thousands of nuclear encoded preproteins. Plastid proteomes undergo rapid remodeling in response to developmental and environmental signals to generate functionally distinct plastid types in specific cells and tissues. In this review, we will highlight the central role of the plastid protein import system in regulating and coordinating the import of functionally related sets of preproteins that are required for plastid-type transitions and maintenance.

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Competing interests

The authors declare that they have no competing interests.

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Figures

Fig. 1.
Fig. 1.
Plastid protein import and control of the import machinery by the ubiquitin-proteasome system. a The majority of plastid proteins are encoded in the nucleus and translated on cytosolic ribosomes. Plastid preproteins contain an N-terminal transit peptide that is necessary and sufficient to target proteins to the organelle. The transit peptide is recognized at the surface of the plastid by two GTPase receptors of the TOC complex (brown), Toc159 (159) and Toc33 (33), at the outer envelope membrane (OM). The receptors initiate membrane transport via a GTP-dependent switch, and the preprotein translocates through an associated β-barrel channel, Toc75 (75) of the TOC complex. Import occurs simultaneously across TOC and TIC (blue) and is driven by an ATP-dependent import-associated chaperone network, which constitutes the import motor (orange). The transit peptide is removed by the stromal processing peptidase upon import, and the chaperone network assists in folding and assembly of the newly imported proteins. Proteins destined for the inner envelope or thylakoid membranes are subsequently recognized by conserved sub-organellar targeting machineries. b Distinct TOC complexes (brown and green), defined by the presence of specific TOC GTPase receptors (e.g., Toc159/33 vs. Toc132/34) mediate import of specific classes of preproteins, thereby preventing competition for import between proteins from different functional or developmental-specific groups (e.g., Groups I and II) and providing a mechanism of selectively regulating their import. The turnover of TOC complexes plays a key role in plastid-type transitions, including the conversion from chemoautotrophic to photoautotrophic metabolism in seedlings. TOC complex turnover is controlled by the ubiquitin proteasome system (UPS) via an outer envelope-associated RING-type E3 ubiquitin ligase, SP1. This functions to balance the levels of specific TOC pathways with changes in the expression of specific classes of preproteins to maintain organelle homeostasis
Fig. 2.
Fig. 2.
Targeting of preproteins to the TOC complex is monitored by the ubiquitin proteasome system in the cytosol. Preproteins are targeted to the TOC complex post-translationally as unfolded polypeptides, and cells must monitor protein import to avoid the toxic accumulation of mis-sorted or misfolded preproteins in the cytosol. This is particularly critical during plastid developmental transitions when TOC complexes are turned over, or under stress conditions when import is inhibited. Cytosolic Hsp70 (blue) and Hsp90 (green) chaperones have been implicated as components of targeting complexes to assist preprotein transit through the cytoplasm en route to their interaction with the TOC receptors (black arrows). When import of preproteins is inhibited (red X), an Hsp70 isoform, Hsc70-4, functions in conjunction with the cytosolic E3 ubiquitin ligase, CHIP (orange), to target misfolded or mis-sorted preproteins for degradation by the cytosolic ubiquitin-proteasome system (UPS; red arrow). N-terminal acetylation is prevalent under conditions that result in the accumulation of preproteins in the cytosol, suggesting that this might serve as a marker for UPS-mediated degradation
Fig. 3.
Fig. 3.
Chaperone systems in the intermembrane space and stroma assist cooperation between TOC and TIC and provide the driving force for import. a Import across the outer and inner envelope membranes (OM and IM) through TOC and TIC is coupled to provide direct targeting from the cytosol to the plastid stroma. Toc75 (75), the major membrane channel of the TOC complex (green), contains three polypeptide transport associated domains (POTRAs) that bind to preproteins in the intermembrane space as they emerge across the outer envelope. The POTRAs and Tic22 (light green), an intermembrane space chaperone, work together to ensure that preproteins do not misfold in the intermembrane space and assist in hand-off to the TIC machinery. In some species, preprotein targeting to the TIC system is facilitated by a 1 MDa complex at the inner membrane (gray) that includes Tic56 (56), Tic100 (100) and Tic214 (214). Tic20 (20), Tic110 (110), and Tic40 (40) are major components of the translocation machinery at the inner membrane. b Membrane translocation is driven by an import-associated chaperone network, containing cpHsp70 (70), cpHsp90 (90), and Hsp93/ClpC (93), which assemble at the site of import by the coordinate actions of Tic110 (110) and Tic40 (40). This chaperone network functions as an ATP-dependent import motor and may assist in folding and assembly of newly imported proteins. Recent evidence also suggests that Hsp93/ClpC is associated with the ClpP/R protease (ClpP/R), leading to the hypothesis that the Clp complex functions as a quality control system to degrade newly imported proteins that are orphaned or misfolded
Fig. 4.
Fig. 4.
The TIC complex interacts with factors that facilitate the targeting of proteins to the inner envelope and thylakoid membranes to avoid potential mis-sorting of hydrophobic membrane proteins to the stroma. a At least five mechanisms conserved from the original bacterial endosymbiont exist for targeting proteins to the internal thylakoids of chloroplasts. The cpSRP system mediates the targeting of abundant thylakoid membrane proteins, including the light harvesting complex proteins. Genetic and biochemical evidence has identified a novel factor, LHCP translocation defect (LTD) protein, that docks at the inner membrane via an interaction with TIC components, Tic40 and Tic110, and also binds to cpSRP. LTD is proposed to facilitate the passage of LHCP proteins from the import apparatus to the cpSRP4 for delivery to the thylakoid Sec translocase (cpSec1). In a related pathway, Albino4 (ALB4), a homologue of ALB3, and STIC2, a homologue of bacterial YbaB, function by linking TIC and cpSRP to facilitate the targeting of a subset of proteins other than LHCPs to the thylakoid membrane. b Inner envelope membrane proteins are integrated into the membrane by a stop-transfer mechanism directly via the TIC channel or following import via a cpSec2 system (post-import/conservative mechanism) that catalyzes membrane protein integration from the stroma. For proteins using the post-import/conservative mechanism, the TIC complex and the cpSec2 system cooperate to allow protein import and membrane integration to proceed simultaneously to facilitate targeting to the inner membrane

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