Fig. 3.

Regulation of the plastid general import machinery by the ubiquitin–proteasome system (UPS) during developmental transitions. Distinct TOC complexes mediate the import of specific classes (Groups 1 and 2) of nuclear-encoded preproteins into plastids. The specificity of the import complexes is determined by the Toc34–Toc159 family of transit peptide receptors. The relative abundance of distinct TOCs is regulated by the UPS and is required to balance the capacity of distinct import pathways with the changes in gene expression that accompany proteome remodeling during plastid-type transitions. (a) During the transition from non-green plastids to chloroplasts, the abundance of TOC complexes containing Toc132/Toc33 receptors (orange) relative to Toc159/Toc33 receptors (green) is altered to accommodate the import of proteins required for photosynthesis and the transition from chemoautotrophic to photoautotrophic metabolism. UPS-mediated turnover of TOC complexes involves a RING-type E3 ubiquitin ligase (SP1) that polyubiquitinates TOC components. The ubiquitinated TOC components appear to be extracted from the outer membrane and delivered to the 26S proteasome for degradation by the combined activities of the SP2 β-barrel channel protein and the cytosolic Cdc48 AAA+ ATPase. (b) Gibberellic acid (GA) plays an important part in preventing the premature biogenesis of chloroplasts during seed germination. The DELLA transcriptional regulators accumulate in the absence of GA and suppress the transcription of genes associated with germination, including genes required for chloroplast biogenesis. DELLAs also bind to the cytosolic form of the Toc159 protein import receptor, thereby promoting receptor degradation by the UPS and preventing the formation of TOC complexes required for the import and assembly of the photosynthetic machinery. A GA-regulated quality control system also targets cytosolic chloroplast preproteins for UPS degradation to prevent the accumulation of toxic preproteins in the cytosol. During germination, increased GA promotes UPS-mediated degradation of DELLAs via the GA–Gibberellin insensitive dwarf1 (GID) complex, the F-box protein SLY1, and the SCF E3 ligase, thereby inducing the expression of genes required for assembly of the photosynthetic machinery, while simultaneously allowing Toc159 to assemble with other TOC components to form complexes required for chloroplast biogenesis.