New Insights into the Chloroplast Outer Membrane Proteome and Associated Targeting Pathways

Abstract

Plastids are a dynamic class of organelle in plant cells that arose from an ancient cyanobacterial endosymbiont. Over the course of evolution, most genes encoding plastid proteins were transferred to the nuclear genome. In parallel, eukaryotic cells evolved a series of targeting pathways and complex proteinaceous machinery at the plastid surface to direct these proteins back to their target organelle. Chloroplasts are the most well-characterized plastids, responsible for photosynthesis and other important metabolic functions. The biogenesis and function of chloroplasts rely heavily on the fidelity of intracellular protein trafficking pathways. Therefore, understanding these pathways and their regulation is essential. Furthermore, the chloroplast outer membrane proteome remains relatively uncharted territory in our understanding of protein targeting. Many key players in the cytosol, receptors at the organelle surface, and insertases that facilitate insertion into the chloroplast outer membrane remain elusive for this group of proteins. In this review, we summarize recent advances in the understanding of well-characterized chloroplast outer membrane protein targeting pathways as well as provide new insights into novel targeting signals and pathways more recently identified using a bioinformatic approach. As a result of our analyses, we expand the known number of chloroplast outer membrane proteins from 117 to 138.

“Omics” insights into plastid behavior toward improved carotenoid accumulation

“…Plastids are organelles with their own prokaryotic genomes, genetic structure, and gene expression ( Fish et al., 2022 ). For the past two decades, numerous plastid genomes (plastome) have been sequenced, conferring substantial information of their organization and evolution ( Tonti-Filippini et al., 2017 ).…”

“…In addition, protein targeting mechanisms have been advanced ( Zhu et al., 2022 ). Typically, chloroplast-localized proteins are synthesized as precursors with an N-terminal sign al known as a transit peptide (TP) and delivered to the chloroplast surface by cytosolic chaperones ( Fish et al., 2022 ). Most of these proteins are imported through translocons of the inner and outer membrane of the chloroplast, termed TIC andTOC, respectively ( Hoermann et al., 2007 ).…”

“…For plants such as Arabidopsis, pea, and tomato, the TOC machinery exists in multiple bv forms and plays a key role in precursor protein recognition ( Figure 2 ) ( Ganesan and Theg, 2019 ). This may help to accommodate different proteomes in diverse plastid types, as the majority of proteins in plastids are imported from the cytosol ( Fish et al., 2022 ). It was discovered that this RING-type E3 ligase suppresses the ppi1 locus 1 (SP1) ( Ling et al., 2019 ), which is a TOC33 knock-out mutant with pale yellow phenotypes in Arabidopsis thaliana ( Thomson et al., 2020 ).…”

“…It plays a role in protein input by physically interacting with many components in the TIC machine, including TIC40 and TIC110 ( Yuan et al., 2021 ). OR also interferes with the interaction between TIC40 and TIC110 by reducing the turnover of TIC40 ( Fish et al., 2022 ), and reducing the binding of pre-protein and TIC110, thereby carrying out protein translocation and processing ( Yuan et al., 2021 ). The OR of a “golden SNP” (OR His ) in melon fruit prevents the conversion of β-carotene to downstream products ( Chayut et al., 2017 ; Giuliano, 2017 ).…”

“…The plastids in plant cells are responsible for carotenoid biosynthesis and storage ( Fish et al., 2022 ). Apart from proplastids which are undifferentiated plastids, all other types of plastids are capable of producing carotenoids ( Sadali et al., 2019 ).…”