Chloroplast Proteostasis: Import, Sorting, Ubiquitination, and Proteolysis

Abstract

Chloroplasts are the defining plant organelles with responsibility for photosynthesis and other vital functions. To deliver these functions, they possess a complex proteome comprising thousands of largely nucleus-encoded proteins. Composition of the proteome is controlled by diverse processes affecting protein translocation and degradation—our focus here. Most chloroplast proteins are imported from the cytosol via multiprotein translocons in the outer and inner envelope membranes (the TOC and TIC complexes, respectively), or via one of several noncanonical pathways, and then sorted by different systems to organellar subcompartments. Chloroplast proteolysis is equally complex, involving the concerted action of internal proteases of prokaryotic origin and the nucleocytosolic ubiquitin–proteasome system (UPS). The UPS degrades unimported proteins in the cytosol and chloroplast-resident proteins via chloroplast-associated protein degradation (CHLORAD). The latter targets the TOC apparatus to regulate protein import, as well as numerous internal proteins directly, to reconfigure chloroplast functions in response to developmental and environmental signals. Expected final online publication date for the Annual Review of Plant Biology, Volume 74 is May 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Chloroplast protein translocation pathways and ubiquitin-dependent regulation at a glance

“…Then, the imported protein can assume its final folded conformation, or be delivered to one of several suborganellar destinations. Pathways that target proteins to the thylakoids and IEM are described briefly below (for more details, refer to Cline and Dabney-Smith, 2008 ; Sun and Jarvis, 2023 ; Ziehe et al, 2018 ).…”

“…This involves the stromal Get3B ATPase and unknown membrane insertase(s) (possibly Alb3 or Alb4). Finally, some membrane proteins are integrated spontaneously without the assistance of known factors ( Sun and Jarvis, 2023 ).…”

“…Sophisticated targeting mechanisms mediate the directional flow of new chloroplast proteins from cytosolic ribosomes to different chloroplast subcompartments ( Jarvis and López-Juez, 2013 ). These mechanisms involve: (1) cytosolic factors that act as molecular chaperones to target newly synthesized proteins to the chloroplast surface; (2) protein translocation complexes in the chloroplast envelope membranes that import proteins into the organelle [the translocons at the outer chloroplast membrane (TOC) and translocons at the inner chloroplast membrane (TIC); collectively TOC-TIC]; and (3) internal sorting systems that distribute new proteins from the translocons to various internal compartments (see poster) ( Li and Chiu, 2010 ; Paila et al, 2015 ; Shi and Theg, 2013a ; Sun and Jarvis, 2023 ; Thomson et al, 2020 ).…”

A unifying mechanism for protein transport through the core bacterial Sec machinery

“…In the subsequent years, numerous protein transport machineries have been identified as residents of most biological membranes; both general purpose and highly specific [4][5][6][7]. The most prevalent of these is the universal Sec systemthe protein translocation channel first postulated by Blobel.…”

Chloroplast import motor subunits FtsHi1 and FtsHi2 are located on opposite sides of the inner envelope membrane

“…For example, Toc75 is the protein-translocating channel across the outer membrane, whereas Tic20 is the major component of the inner-membrane channel. Tic110, an integral inner membrane protein with a large soluble domain located in the stroma, functions as a stroma-side receptor for transit peptides and a scaffold for other stromally located translocon components ( 1 ).…”