Coexpressed subunits of dual genetic origin define a conserved supercomplex mediating essential protein import into chloroplasts.

TitleCoexpressed subunits of dual genetic origin define a conserved supercomplex mediating essential protein import into chloroplasts.
Publication TypeJournal Article
Year of Publication2020
AuthorsRamundo, S, Asakura, Y, Salomé, PA, Strenkert, D, Boone, M, Mackinder, LCM, Takafuji, K, Dinc, E, Rahire, M, Crèvecoeur, M, Magneschi, L, Schaad, O, Hippler, M, Jonikas, MC, Merchant, S, Nakai, M, Rochaix, J-D, Walter, P
JournalProc Natl Acad Sci U S A
Volume117
Issue51
Pagination32739-32749
Date Published2020 12 22
ISSN1091-6490
KeywordsCell Compartmentation, Chlamydomonas reinhardtii, Chloroplasts, Evolution, Molecular, Gene Expression Regulation, Plant, Multiprotein Complexes, Plant Proteins, Protein Transport, Sequence Homology, Amino Acid
Abstract

<p>In photosynthetic eukaryotes, thousands of proteins are translated in the cytosol and imported into the chloroplast through the concerted action of two translocons-termed TOC and TIC-located in the outer and inner membranes of the chloroplast envelope, respectively. The degree to which the molecular composition of the TOC and TIC complexes is conserved over phylogenetic distances has remained controversial. Here, we combine transcriptomic, biochemical, and genetic tools in the green alga Chlamydomonas () to demonstrate that, despite a lack of evident sequence conservation for some of its components, the algal TIC complex mirrors the molecular composition of a TIC complex from The Chlamydomonas TIC complex contains three nuclear-encoded subunits, Tic20, Tic56, and Tic100, and one chloroplast-encoded subunit, Tic214, and interacts with the TOC complex, as well as with several uncharacterized proteins to form a stable supercomplex (TIC-TOC), indicating that protein import across both envelope membranes is mechanistically coupled. Expression of the nuclear and chloroplast genes encoding both known and uncharacterized TIC-TOC components is highly coordinated, suggesting that a mechanism for regulating its biogenesis across compartmental boundaries must exist. Conditional repression of Tic214, the only chloroplast-encoded subunit in the TIC-TOC complex, impairs the import of chloroplast proteins with essential roles in chloroplast ribosome biogenesis and protein folding and induces a pleiotropic stress response, including several proteins involved in the chloroplast unfolded protein response. These findings underscore the functional importance of the TIC-TOC supercomplex in maintaining chloroplast proteostasis.</p>

DOI10.1073/pnas.2014294117
Alternate JournalProc Natl Acad Sci U S A
PubMed ID33273113
PubMed Central IDPMC7768757
Grant ListHHMI826735-0012 / HHMI / Howard Hughes Medical Institute / United States
R01 GM032384 / GM / NIGMS NIH HHS / United States