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

Silvia Ramundo, Yukari Asakura, Patrice A. Salomé, Daniela Strenkert, Morgane Boone, Luke C.M. Mackinder, Kazuaki Takafuji, Emine Dinc, Michèle Rahire, Michèle Crèvecoeur, Leonardo Magneschi, Olivier Schaad, Michael Hippler, Martin C. Jonikas, Sabeeha Merchant, Masato Nakai, Jean David Rochaix, Peter Walter

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

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 (Chlamydomonas reinhardtii) 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 Arabidopsis thaliana. 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 TICTOC supercomplex in maintaining chloroplast proteostasis.

Original languageEnglish (US)
Pages (from-to)32739-32749
Number of pages11
JournalProceedings of the National Academy of Sciences of the United States of America
Volume117
Issue number51
DOIs
StatePublished - Dec 22 2020

All Science Journal Classification (ASJC) codes

  • General

Keywords

  • Chlamydomonas reinhardtii
  • Chloroplast gene targeting
  • Chloroplast protein import
  • Gene coexpression

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