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Expression and Evolution of the Non-Canonically Translated Yeast Mitochondrial Acetyl-CoA Carboxylase Hfa1p

The Saccharomyces cerevisiae genome encodes two sequence related acetyl-CoA carboxylases, the cytosolic Acc1p and the mitochondrial Hfa1p, required for respiratory function. Several aspects of expression of the HFA1 gene and its evolutionary origin have remained unclear. Here, we determined the HFA1...

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Autores principales: Suomi, Fumi, Menger, Katja E., Monteuuis, Geoffray, Naumann, Uta, Kursu, V. A. Samuli, Shvetsova, Antonina, Kastaniotis, Alexander J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4263661/
https://www.ncbi.nlm.nih.gov/pubmed/25503745
http://dx.doi.org/10.1371/journal.pone.0114738
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author Suomi, Fumi
Menger, Katja E.
Monteuuis, Geoffray
Naumann, Uta
Kursu, V. A. Samuli
Shvetsova, Antonina
Kastaniotis, Alexander J.
author_facet Suomi, Fumi
Menger, Katja E.
Monteuuis, Geoffray
Naumann, Uta
Kursu, V. A. Samuli
Shvetsova, Antonina
Kastaniotis, Alexander J.
author_sort Suomi, Fumi
collection PubMed
description The Saccharomyces cerevisiae genome encodes two sequence related acetyl-CoA carboxylases, the cytosolic Acc1p and the mitochondrial Hfa1p, required for respiratory function. Several aspects of expression of the HFA1 gene and its evolutionary origin have remained unclear. Here, we determined the HFA1 transcription initiation sites by 5′ RACE analysis. Using a novel “Stop codon scanning” approach, we mapped the location of the HFA1 translation initiation site to an upstream AUU codon at position −372 relative to the annotated start codon. This upstream initiation leads to production of a mitochondrial targeting sequence preceding the ACC domains of the protein. In silico analyses of fungal ACC genes revealed conserved “cryptic” upstream mitochondrial targeting sequences in yeast species that have not undergone a whole genome duplication. Our Δhfa1 baker's yeast mutant phenotype rescue studies using the protoploid Kluyveromyces lactis ACC confirmed functionality of the cryptic upstream mitochondrial targeting signal. These results lend strong experimental support to the hypothesis that the mitochondrial and cytosolic acetyl-CoA carboxylases in S. cerevisiae have evolved from a single gene encoding both the mitochondrial and cytosolic isoforms. Leaning on a cursory survey of a group of genes of our interest, we propose that cryptic 5′ upstream mitochondrial targeting sequences may be more abundant in eukaryotes than anticipated thus far.
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spelling pubmed-42636612014-12-19 Expression and Evolution of the Non-Canonically Translated Yeast Mitochondrial Acetyl-CoA Carboxylase Hfa1p Suomi, Fumi Menger, Katja E. Monteuuis, Geoffray Naumann, Uta Kursu, V. A. Samuli Shvetsova, Antonina Kastaniotis, Alexander J. PLoS One Research Article The Saccharomyces cerevisiae genome encodes two sequence related acetyl-CoA carboxylases, the cytosolic Acc1p and the mitochondrial Hfa1p, required for respiratory function. Several aspects of expression of the HFA1 gene and its evolutionary origin have remained unclear. Here, we determined the HFA1 transcription initiation sites by 5′ RACE analysis. Using a novel “Stop codon scanning” approach, we mapped the location of the HFA1 translation initiation site to an upstream AUU codon at position −372 relative to the annotated start codon. This upstream initiation leads to production of a mitochondrial targeting sequence preceding the ACC domains of the protein. In silico analyses of fungal ACC genes revealed conserved “cryptic” upstream mitochondrial targeting sequences in yeast species that have not undergone a whole genome duplication. Our Δhfa1 baker's yeast mutant phenotype rescue studies using the protoploid Kluyveromyces lactis ACC confirmed functionality of the cryptic upstream mitochondrial targeting signal. These results lend strong experimental support to the hypothesis that the mitochondrial and cytosolic acetyl-CoA carboxylases in S. cerevisiae have evolved from a single gene encoding both the mitochondrial and cytosolic isoforms. Leaning on a cursory survey of a group of genes of our interest, we propose that cryptic 5′ upstream mitochondrial targeting sequences may be more abundant in eukaryotes than anticipated thus far. Public Library of Science 2014-12-11 /pmc/articles/PMC4263661/ /pubmed/25503745 http://dx.doi.org/10.1371/journal.pone.0114738 Text en © 2014 Suomi et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Suomi, Fumi
Menger, Katja E.
Monteuuis, Geoffray
Naumann, Uta
Kursu, V. A. Samuli
Shvetsova, Antonina
Kastaniotis, Alexander J.
Expression and Evolution of the Non-Canonically Translated Yeast Mitochondrial Acetyl-CoA Carboxylase Hfa1p
title Expression and Evolution of the Non-Canonically Translated Yeast Mitochondrial Acetyl-CoA Carboxylase Hfa1p
title_full Expression and Evolution of the Non-Canonically Translated Yeast Mitochondrial Acetyl-CoA Carboxylase Hfa1p
title_fullStr Expression and Evolution of the Non-Canonically Translated Yeast Mitochondrial Acetyl-CoA Carboxylase Hfa1p
title_full_unstemmed Expression and Evolution of the Non-Canonically Translated Yeast Mitochondrial Acetyl-CoA Carboxylase Hfa1p
title_short Expression and Evolution of the Non-Canonically Translated Yeast Mitochondrial Acetyl-CoA Carboxylase Hfa1p
title_sort expression and evolution of the non-canonically translated yeast mitochondrial acetyl-coa carboxylase hfa1p
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4263661/
https://www.ncbi.nlm.nih.gov/pubmed/25503745
http://dx.doi.org/10.1371/journal.pone.0114738
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