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Composition and evolution of the vertebrate and mammalian selenoproteomes.

Mariotti M, Ridge PG, Zhang Y, Lobanov AV, Pringle TH, Guigo R, Hatfield DL, Gladyshev VN - PLoS ONE (2012)

Bottom Line: In total, we detected 45 selenoprotein subfamilies. 28 of them were found in mammals, and 41 in bony fishes.Mammalian thioredoxin reductase 1 and thioredoxin-glutathione reductase evolved from an ancestral glutaredoxin-domain containing enzyme, still present in fish.It also provides a wealth of information on these selenoproteins and their forms.

View Article: PubMed Central - PubMed

Affiliation: Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, United States of America.

ABSTRACT

Background: Selenium is an essential trace element in mammals due to its presence in proteins in the form of selenocysteine (Sec). Human genome codes for 25 Sec-containing protein genes, and mouse and rat genomes for 24.

Methodology/principal findings: We characterized the selenoproteomes of 44 sequenced vertebrates by applying gene prediction and phylogenetic reconstruction methods, supplemented with the analyses of gene structures, alternative splicing isoforms, untranslated regions, SECIS elements, and pseudogenes. In total, we detected 45 selenoprotein subfamilies. 28 of them were found in mammals, and 41 in bony fishes. We define the ancestral vertebrate (28 proteins) and mammalian (25 proteins) selenoproteomes, and describe how they evolved along lineages through gene duplication (20 events), gene loss (10 events) and replacement of Sec with cysteine (12 events). We show that an intronless selenophosphate synthetase 2 gene evolved in early mammals and replaced functionally the original multiexon gene in placental mammals, whereas both genes remain in marsupials. Mammalian thioredoxin reductase 1 and thioredoxin-glutathione reductase evolved from an ancestral glutaredoxin-domain containing enzyme, still present in fish. Selenoprotein V and GPx6 evolved specifically in placental mammals from duplications of SelW and GPx3, respectively, and GPx6 lost Sec several times independently. Bony fishes were characterized by duplications of several selenoprotein families (GPx1, GPx3, GPx4, Dio3, MsrB1, SelJ, SelO, SelT, SelU1, and SelW2). Finally, we report identification of new isoforms for several selenoproteins and describe unusually conserved selenoprotein pseudogenes.

Conclusions/significance: This analysis represents the first comprehensive survey of the vertebrate and mammal selenoproteomes, and depicts their evolution along lineages. It also provides a wealth of information on these selenoproteins and their forms.

Show MeSH
Phylogeny of SelU family in vertebrates.ML tree computed using the JTT substitution model. Sec-containing proteins are shown in red, whereas the Cys-containing homologs are shown in blue. At the bottom left, the distance scale in substitutions per position is shown. Branch support is shown along the tree in red.
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pone-0033066-g009: Phylogeny of SelU family in vertebrates.ML tree computed using the JTT substitution model. Sec-containing proteins are shown in red, whereas the Cys-containing homologs are shown in blue. At the bottom left, the distance scale in substitutions per position is shown. Branch support is shown along the tree in red.

Mentions: The ancestral vertebrate selenoproteome was uncertain, as fish had many selenoproteins resulting of genome duplication and gene duplication within bony fishes [25]. Previously, it has been suggested that the ancestral vertebrate selenoproteome consists of 31 selenoproteins: Dio1-3, GPx1-4, SelH, SelI, SelJ, SelK, SelL, SelM, SelN, SelO, SelP, SelPb, MsrB1, SelS, SelT1, SelU1-3, SelV, SelW1, SelW2a, Sep15, SPS2, TR1, TR3 and TGR [32]. In this study, we examined the occurrence of these selenoproteins in additional mammals and newly sequenced organisms which are important outgroups for understanding the evolution of different vertebrate clades (such as platypus and opossum). Particularly, we used both genomic and Trace databases for reconstruction of the selenoproteome of the phylogenetically oldest group of living jawed vertebrates, the elephant sharks. As a result, a number of new aspects were uncovered: (i) Fep15, which was previously thought to evolve in bony fish, was detected as a selenoprotein in elephant shark and as a Cys homolog in frog, and therefore should be viewed as part of the ancestral selenoproteome; (ii) TGR was found exclusively in tetrapods; (iii) SelV was found exclusively in placental mammals; (iv) phylogenetic analysis of Sec- and Cys-containing forms of the SelU family suggested that all Sec-containing SelU sequences belong to the SelU1 group (Figure 9). Mammals contain three Cys-containing SelU proteins (SelU1-3), whereas some fish (such as fugu and pufferfish) have three Sec-containing SelU proteins. It was previously thought that the three Cys-containing SelU proteins in mammals evolved from the three Sec-containing SelU sequences in fish. In this study, we could not find evidence that supports an early Sec-to-Cys conversion event for SelU2 and SelU3 proteins. Thus, the revised ancestral selenoproteome consists of the following 28 selenoproteins: GPx1-4, TR1, TR3, Dio1-3, SelH, SelI, SelJ, SelK, SelL, SelM, SelN, SelO, SelP, SelPb, MsrB1, SelS, SelT1, SelU1, SelW1, SelW2, Sep15, Fep15 and SPS2a (Figure 1).


Composition and evolution of the vertebrate and mammalian selenoproteomes.

Mariotti M, Ridge PG, Zhang Y, Lobanov AV, Pringle TH, Guigo R, Hatfield DL, Gladyshev VN - PLoS ONE (2012)

Phylogeny of SelU family in vertebrates.ML tree computed using the JTT substitution model. Sec-containing proteins are shown in red, whereas the Cys-containing homologs are shown in blue. At the bottom left, the distance scale in substitutions per position is shown. Branch support is shown along the tree in red.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3316567&req=5

pone-0033066-g009: Phylogeny of SelU family in vertebrates.ML tree computed using the JTT substitution model. Sec-containing proteins are shown in red, whereas the Cys-containing homologs are shown in blue. At the bottom left, the distance scale in substitutions per position is shown. Branch support is shown along the tree in red.
Mentions: The ancestral vertebrate selenoproteome was uncertain, as fish had many selenoproteins resulting of genome duplication and gene duplication within bony fishes [25]. Previously, it has been suggested that the ancestral vertebrate selenoproteome consists of 31 selenoproteins: Dio1-3, GPx1-4, SelH, SelI, SelJ, SelK, SelL, SelM, SelN, SelO, SelP, SelPb, MsrB1, SelS, SelT1, SelU1-3, SelV, SelW1, SelW2a, Sep15, SPS2, TR1, TR3 and TGR [32]. In this study, we examined the occurrence of these selenoproteins in additional mammals and newly sequenced organisms which are important outgroups for understanding the evolution of different vertebrate clades (such as platypus and opossum). Particularly, we used both genomic and Trace databases for reconstruction of the selenoproteome of the phylogenetically oldest group of living jawed vertebrates, the elephant sharks. As a result, a number of new aspects were uncovered: (i) Fep15, which was previously thought to evolve in bony fish, was detected as a selenoprotein in elephant shark and as a Cys homolog in frog, and therefore should be viewed as part of the ancestral selenoproteome; (ii) TGR was found exclusively in tetrapods; (iii) SelV was found exclusively in placental mammals; (iv) phylogenetic analysis of Sec- and Cys-containing forms of the SelU family suggested that all Sec-containing SelU sequences belong to the SelU1 group (Figure 9). Mammals contain three Cys-containing SelU proteins (SelU1-3), whereas some fish (such as fugu and pufferfish) have three Sec-containing SelU proteins. It was previously thought that the three Cys-containing SelU proteins in mammals evolved from the three Sec-containing SelU sequences in fish. In this study, we could not find evidence that supports an early Sec-to-Cys conversion event for SelU2 and SelU3 proteins. Thus, the revised ancestral selenoproteome consists of the following 28 selenoproteins: GPx1-4, TR1, TR3, Dio1-3, SelH, SelI, SelJ, SelK, SelL, SelM, SelN, SelO, SelP, SelPb, MsrB1, SelS, SelT1, SelU1, SelW1, SelW2, Sep15, Fep15 and SPS2a (Figure 1).

Bottom Line: In total, we detected 45 selenoprotein subfamilies. 28 of them were found in mammals, and 41 in bony fishes.Mammalian thioredoxin reductase 1 and thioredoxin-glutathione reductase evolved from an ancestral glutaredoxin-domain containing enzyme, still present in fish.It also provides a wealth of information on these selenoproteins and their forms.

View Article: PubMed Central - PubMed

Affiliation: Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, United States of America.

ABSTRACT

Background: Selenium is an essential trace element in mammals due to its presence in proteins in the form of selenocysteine (Sec). Human genome codes for 25 Sec-containing protein genes, and mouse and rat genomes for 24.

Methodology/principal findings: We characterized the selenoproteomes of 44 sequenced vertebrates by applying gene prediction and phylogenetic reconstruction methods, supplemented with the analyses of gene structures, alternative splicing isoforms, untranslated regions, SECIS elements, and pseudogenes. In total, we detected 45 selenoprotein subfamilies. 28 of them were found in mammals, and 41 in bony fishes. We define the ancestral vertebrate (28 proteins) and mammalian (25 proteins) selenoproteomes, and describe how they evolved along lineages through gene duplication (20 events), gene loss (10 events) and replacement of Sec with cysteine (12 events). We show that an intronless selenophosphate synthetase 2 gene evolved in early mammals and replaced functionally the original multiexon gene in placental mammals, whereas both genes remain in marsupials. Mammalian thioredoxin reductase 1 and thioredoxin-glutathione reductase evolved from an ancestral glutaredoxin-domain containing enzyme, still present in fish. Selenoprotein V and GPx6 evolved specifically in placental mammals from duplications of SelW and GPx3, respectively, and GPx6 lost Sec several times independently. Bony fishes were characterized by duplications of several selenoprotein families (GPx1, GPx3, GPx4, Dio3, MsrB1, SelJ, SelO, SelT, SelU1, and SelW2). Finally, we report identification of new isoforms for several selenoproteins and describe unusually conserved selenoprotein pseudogenes.

Conclusions/significance: This analysis represents the first comprehensive survey of the vertebrate and mammal selenoproteomes, and depicts their evolution along lineages. It also provides a wealth of information on these selenoproteins and their forms.

Show MeSH