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Evolution of selenophosphate synthetases: emergence and relocation of function through independent duplications and recurrent subfunctionalization

Selenoproteins are proteins that incorporate selenocysteine (Sec), a nonstandard amino acid encoded by UGA, normally a stop codon. Sec synthesis requires the enzyme Selenophosphate synthetase (SPS or SelD), conserved in all prokaryotic and eukaryotic genomes encoding selenoproteins. Here, we study t...

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Autores principales: Mariotti, Marco, Santesmasses, Didac, Capella-Gutierrez, Salvador, Mateo, Andrea, Arnan, Carme, Johnson, Rory, D'Aniello, Salvatore, Yim, Sun Hee, Gladyshev, Vadim N., Serras, Florenci, Corominas, Montserrat, Gabaldón, Toni, Guigó, Roderic
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4561486/
https://www.ncbi.nlm.nih.gov/pubmed/26194102
http://dx.doi.org/10.1101/gr.190538.115
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author Mariotti, Marco
Santesmasses, Didac
Capella-Gutierrez, Salvador
Mateo, Andrea
Arnan, Carme
Johnson, Rory
D'Aniello, Salvatore
Yim, Sun Hee
Gladyshev, Vadim N.
Serras, Florenci
Corominas, Montserrat
Gabaldón, Toni
Guigó, Roderic
author_facet Mariotti, Marco
Santesmasses, Didac
Capella-Gutierrez, Salvador
Mateo, Andrea
Arnan, Carme
Johnson, Rory
D'Aniello, Salvatore
Yim, Sun Hee
Gladyshev, Vadim N.
Serras, Florenci
Corominas, Montserrat
Gabaldón, Toni
Guigó, Roderic
author_sort Mariotti, Marco
collection PubMed
description Selenoproteins are proteins that incorporate selenocysteine (Sec), a nonstandard amino acid encoded by UGA, normally a stop codon. Sec synthesis requires the enzyme Selenophosphate synthetase (SPS or SelD), conserved in all prokaryotic and eukaryotic genomes encoding selenoproteins. Here, we study the evolutionary history of SPS genes, providing a map of selenoprotein function spanning the whole tree of life. SPS is itself a selenoprotein in many species, although functionally equivalent homologs that replace the Sec site with cysteine (Cys) are common. Many metazoans, however, possess SPS genes with substitutions other than Sec or Cys (collectively referred to as SPS1). Using complementation assays in fly mutants, we show that these genes share a common function, which appears to be distinct from the synthesis of selenophosphate carried out by the Sec- and Cys- SPS genes (termed SPS2), and unrelated to Sec synthesis. We show here that SPS1 genes originated through a number of independent gene duplications from an ancestral metazoan selenoprotein SPS2 gene that most likely already carried the SPS1 function. Thus, in SPS genes, parallel duplications and subsequent convergent subfunctionalization have resulted in the segregation to different loci of functions initially carried by a single gene. This evolutionary history constitutes a remarkable example of emergence and evolution of gene function, which we have been able to trace thanks to the singular features of SPS genes, wherein the amino acid at a single site determines unequivocally protein function and is intertwined to the evolutionary fate of the entire selenoproteome.
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spelling pubmed-45614862015-09-11 Evolution of selenophosphate synthetases: emergence and relocation of function through independent duplications and recurrent subfunctionalization Mariotti, Marco Santesmasses, Didac Capella-Gutierrez, Salvador Mateo, Andrea Arnan, Carme Johnson, Rory D'Aniello, Salvatore Yim, Sun Hee Gladyshev, Vadim N. Serras, Florenci Corominas, Montserrat Gabaldón, Toni Guigó, Roderic Genome Res Research Selenoproteins are proteins that incorporate selenocysteine (Sec), a nonstandard amino acid encoded by UGA, normally a stop codon. Sec synthesis requires the enzyme Selenophosphate synthetase (SPS or SelD), conserved in all prokaryotic and eukaryotic genomes encoding selenoproteins. Here, we study the evolutionary history of SPS genes, providing a map of selenoprotein function spanning the whole tree of life. SPS is itself a selenoprotein in many species, although functionally equivalent homologs that replace the Sec site with cysteine (Cys) are common. Many metazoans, however, possess SPS genes with substitutions other than Sec or Cys (collectively referred to as SPS1). Using complementation assays in fly mutants, we show that these genes share a common function, which appears to be distinct from the synthesis of selenophosphate carried out by the Sec- and Cys- SPS genes (termed SPS2), and unrelated to Sec synthesis. We show here that SPS1 genes originated through a number of independent gene duplications from an ancestral metazoan selenoprotein SPS2 gene that most likely already carried the SPS1 function. Thus, in SPS genes, parallel duplications and subsequent convergent subfunctionalization have resulted in the segregation to different loci of functions initially carried by a single gene. This evolutionary history constitutes a remarkable example of emergence and evolution of gene function, which we have been able to trace thanks to the singular features of SPS genes, wherein the amino acid at a single site determines unequivocally protein function and is intertwined to the evolutionary fate of the entire selenoproteome. Cold Spring Harbor Laboratory Press 2015-09 /pmc/articles/PMC4561486/ /pubmed/26194102 http://dx.doi.org/10.1101/gr.190538.115 Text en © 2015 Mariotti et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by/4.0/ This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.
spellingShingle Research
Mariotti, Marco
Santesmasses, Didac
Capella-Gutierrez, Salvador
Mateo, Andrea
Arnan, Carme
Johnson, Rory
D'Aniello, Salvatore
Yim, Sun Hee
Gladyshev, Vadim N.
Serras, Florenci
Corominas, Montserrat
Gabaldón, Toni
Guigó, Roderic
Evolution of selenophosphate synthetases: emergence and relocation of function through independent duplications and recurrent subfunctionalization
title Evolution of selenophosphate synthetases: emergence and relocation of function through independent duplications and recurrent subfunctionalization
title_full Evolution of selenophosphate synthetases: emergence and relocation of function through independent duplications and recurrent subfunctionalization
title_fullStr Evolution of selenophosphate synthetases: emergence and relocation of function through independent duplications and recurrent subfunctionalization
title_full_unstemmed Evolution of selenophosphate synthetases: emergence and relocation of function through independent duplications and recurrent subfunctionalization
title_short Evolution of selenophosphate synthetases: emergence and relocation of function through independent duplications and recurrent subfunctionalization
title_sort evolution of selenophosphate synthetases: emergence and relocation of function through independent duplications and recurrent subfunctionalization
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4561486/
https://www.ncbi.nlm.nih.gov/pubmed/26194102
http://dx.doi.org/10.1101/gr.190538.115
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