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Evolutionary and genetic analyses of mitochondrial translation initiation factors identify the missing mitochondrial IF3 in S. cerevisiae

Atkinson, Gemma C. LU ; Kuzmenko, Anton ; Kamenski, Piotr ; Vysokikh, Mikhail Y. ; Lakunina, Valentina ; Tankov, Stoyan ; Smirnova, Ekaterina ; Soosaar, Aksel ; Tenson, Tanel and Hauryliuk, Vasili LU orcid (2012) In Nucleic Acids Research 40(13). p.6122-6134
Abstract

Mitochondrial translation is essentially bacteria-like, reflecting the bacterial endosymbiotic ancestry of the eukaryotic organelle. However, unlike the translation system of its bacterial ancestors, mitochondrial translation is limited to just a few mRNAs, mainly coding for components of the respiratory complex. The classical bacterial initiation factors (IFs) IF1, IF2 and IF3 are universal in bacteria, but only IF2 is universal in mitochondria (mIF2). We analyse the distribution of mitochondrial translation initiation factors and their sequence features, given two well-propagated claims: first, a sequence insertion in mitochondrial IF2 (mIF2) compensates for the universal lack of IF1 in mitochondria, and secondly, no homologue of... (More)

Mitochondrial translation is essentially bacteria-like, reflecting the bacterial endosymbiotic ancestry of the eukaryotic organelle. However, unlike the translation system of its bacterial ancestors, mitochondrial translation is limited to just a few mRNAs, mainly coding for components of the respiratory complex. The classical bacterial initiation factors (IFs) IF1, IF2 and IF3 are universal in bacteria, but only IF2 is universal in mitochondria (mIF2). We analyse the distribution of mitochondrial translation initiation factors and their sequence features, given two well-propagated claims: first, a sequence insertion in mitochondrial IF2 (mIF2) compensates for the universal lack of IF1 in mitochondria, and secondly, no homologue of mitochondrial IF3 (mIF3) is identifiable in Saccharomyces cerevisiae. Our comparative sequence analysis shows that, in fact, the mIF2 insertion is highly variable and restricted in length and primary sequence conservation to vertebrates, while phylogenetic and in vivo complementation analyses reveal that an uncharacterized S. cerevisiae mitochondrial protein currently named Aim23p is a bona fide evolutionary and functional orthologue of mIF3. Our results highlight the lineage-specific nature of mitochondrial translation and emphasise that comparative analyses among diverse taxa are essential for understanding whether generalizations from model organisms can be made across eukaryotes.

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author
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publishing date
type
Contribution to journal
publication status
published
in
Nucleic Acids Research
volume
40
issue
13
pages
13 pages
publisher
Oxford University Press
external identifiers
  • scopus:84864447598
  • pmid:22457064
ISSN
0305-1048
DOI
10.1093/nar/gks272
language
English
LU publication?
no
additional info
Funding Information: The European Social Fund (MJD99, Mobilitas grant to G.C.A.); Estonian Science Foundation (ETF7616 and ETF9012 to V.H., ETF9020 to G.C.A.); the European Regional Development Fund through the Center of Excellence in Chemical Biology (code RLOTITIPP to V.H. and T.T.); Russian Foundation for Basic Research, Ministry of Education and Science of Russia, the President of Russian Federation Grant for Young Researchers and funds from International Associated Laboratory ‘RNA-mitocure’ (to P.K., A.K., V.L. and E.S.); SA Archimedes foundation, European Social Fund and DoRa program (to A.K. and S.T.); U.M.N.I.K. program (E.S. and A.K.); ANR (Agence Nationale de la Recherche to M.V.). Funding for open access charge: Estonian Science Foundation grant of G.C.A. and the Center of Excellence in Chemical Biology. Copyright: Copyright 2013 Elsevier B.V., All rights reserved.
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f431a381-35fe-4388-8bf1-9baac33a19e3
date added to LUP
2021-09-24 20:46:11
date last changed
2024-01-05 16:12:13
@article{f431a381-35fe-4388-8bf1-9baac33a19e3,
  abstract     = {{<p>Mitochondrial translation is essentially bacteria-like, reflecting the bacterial endosymbiotic ancestry of the eukaryotic organelle. However, unlike the translation system of its bacterial ancestors, mitochondrial translation is limited to just a few mRNAs, mainly coding for components of the respiratory complex. The classical bacterial initiation factors (IFs) IF1, IF2 and IF3 are universal in bacteria, but only IF2 is universal in mitochondria (mIF2). We analyse the distribution of mitochondrial translation initiation factors and their sequence features, given two well-propagated claims: first, a sequence insertion in mitochondrial IF2 (mIF2) compensates for the universal lack of IF1 in mitochondria, and secondly, no homologue of mitochondrial IF3 (mIF3) is identifiable in Saccharomyces cerevisiae. Our comparative sequence analysis shows that, in fact, the mIF2 insertion is highly variable and restricted in length and primary sequence conservation to vertebrates, while phylogenetic and in vivo complementation analyses reveal that an uncharacterized S. cerevisiae mitochondrial protein currently named Aim23p is a bona fide evolutionary and functional orthologue of mIF3. Our results highlight the lineage-specific nature of mitochondrial translation and emphasise that comparative analyses among diverse taxa are essential for understanding whether generalizations from model organisms can be made across eukaryotes.</p>}},
  author       = {{Atkinson, Gemma C. and Kuzmenko, Anton and Kamenski, Piotr and Vysokikh, Mikhail Y. and Lakunina, Valentina and Tankov, Stoyan and Smirnova, Ekaterina and Soosaar, Aksel and Tenson, Tanel and Hauryliuk, Vasili}},
  issn         = {{0305-1048}},
  language     = {{eng}},
  number       = {{13}},
  pages        = {{6122--6134}},
  publisher    = {{Oxford University Press}},
  series       = {{Nucleic Acids Research}},
  title        = {{Evolutionary and genetic analyses of mitochondrial translation initiation factors identify the missing mitochondrial IF3 in S. cerevisiae}},
  url          = {{http://dx.doi.org/10.1093/nar/gks272}},
  doi          = {{10.1093/nar/gks272}},
  volume       = {{40}},
  year         = {{2012}},
}