TY - JOUR
T1 - Coexpressed subunits of dual genetic origin define a conserved supercomplex mediating essential protein import into chloroplasts
AU - Ramundo, Silvia
AU - Asakura, Yukari
AU - Salomé, Patrice A.
AU - Strenkert, Daniela
AU - Boone, Morgane
AU - Mackinder, Luke C.M.
AU - Takafuji, Kazuaki
AU - Dinc, Emine
AU - Rahire, Michèle
AU - Crèvecoeur, Michèle
AU - Magneschi, Leonardo
AU - Schaad, Olivier
AU - Hippler, Michael
AU - Jonikas, Martin C.
AU - Merchant, Sabeeha
AU - Nakai, Masato
AU - Rochaix, Jean David
AU - Walter, Peter
N1 - Publisher Copyright:
© 2020 National Academy of Sciences. All rights reserved.
PY - 2020/12/22
Y1 - 2020/12/22
N2 - 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.
AB - 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.
KW - Chlamydomonas reinhardtii
KW - Chloroplast gene targeting
KW - Chloroplast protein import
KW - Gene coexpression
UR - http://www.scopus.com/inward/record.url?scp=85098183899&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85098183899&partnerID=8YFLogxK
U2 - 10.1073/pnas.2014294117
DO - 10.1073/pnas.2014294117
M3 - Article
C2 - 33273113
AN - SCOPUS:85098183899
SN - 0027-8424
VL - 117
SP - 32739
EP - 32749
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 51
ER -