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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
Evolution of the vertebrate selenoproteome.The ancestral vertebrate selenoproteome is indicated in red, and its changes across the investigated vertebrates are depicted along their phylogenetic tree. The ancestral selenoproteins found uniquely in vertebrates are underlined. The creation of a new selenoprotein (here always by duplication of an existing one) is indicated by its name in green. Loss is indicated in grey. Replacement of Sec with Cys is indicated in blue (apart from SelW2c in pufferfish, which is with arginine). Events of conversion of Cys to Sec were not found. On the right, the number of selenoproteins predicted in each species is shown.
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pone-0033066-g001: Evolution of the vertebrate selenoproteome.The ancestral vertebrate selenoproteome is indicated in red, and its changes across the investigated vertebrates are depicted along their phylogenetic tree. The ancestral selenoproteins found uniquely in vertebrates are underlined. The creation of a new selenoprotein (here always by duplication of an existing one) is indicated by its name in green. Loss is indicated in grey. Replacement of Sec with Cys is indicated in blue (apart from SelW2c in pufferfish, which is with arginine). Events of conversion of Cys to Sec were not found. On the right, the number of selenoproteins predicted in each species is shown.

Mentions: We characterized vertebrate selenoproteomes by searching for all known selenoproteins in Trace Archive, non-redundant, expressed sequence tag (EST), and genomic databases of 44 vertebrates (including 34 mammals) (Figure 1 and Supplementary Table S1). The search was supplemented with the analysis of SECIS elements via SECISearch [9], and with the subsequent phylogenetic analysis of proteins belonging to the same superfamily. Overall, the searches yielded 45 selenoproteins (selenoprotein subfamilies) in sequenced vertebrates, 28 of which were found in mammals (Table 1). However, none of the mammals analyzed contained all these proteins: at most, 25 selenoproteins were detected. The largest selenoproteomes were found in bony fishes, with a maximum of 38 selenoproteins in zebrafish. The smallest selenoproteome (24 selenoprotein genes) was predicted in frog and in some mammals (Figure 1). 21 selenoproteins were found in all vertebrates: GPx1-4, TR1, TR3, Dio1, Dio2, Dio3, SelH, SelI, SelK, SelM, SelN, SelO, SelP, MsrB1 (methionine-R-sulfoxide reductase 1), SelS, SelT1, SelW1, Sep15. The other selenoproteins were found only in certain lineages, highlighting a dynamic process by which new selenoprotein genes were generated by duplication, while others were lost or replaced their Sec with cysteine (Cys). The predicted ancestral vertebrate selenoproteome is indicated in Figure 1, along with the details of its transformations across vertebrates. We found 28 proteins in the ancestral vertebrate selenoproteome and 25 in the ancestral mammalian selenoproteome.


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)

Evolution of the vertebrate selenoproteome.The ancestral vertebrate selenoproteome is indicated in red, and its changes across the investigated vertebrates are depicted along their phylogenetic tree. The ancestral selenoproteins found uniquely in vertebrates are underlined. The creation of a new selenoprotein (here always by duplication of an existing one) is indicated by its name in green. Loss is indicated in grey. Replacement of Sec with Cys is indicated in blue (apart from SelW2c in pufferfish, which is with arginine). Events of conversion of Cys to Sec were not found. On the right, the number of selenoproteins predicted in each species is shown.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0033066-g001: Evolution of the vertebrate selenoproteome.The ancestral vertebrate selenoproteome is indicated in red, and its changes across the investigated vertebrates are depicted along their phylogenetic tree. The ancestral selenoproteins found uniquely in vertebrates are underlined. The creation of a new selenoprotein (here always by duplication of an existing one) is indicated by its name in green. Loss is indicated in grey. Replacement of Sec with Cys is indicated in blue (apart from SelW2c in pufferfish, which is with arginine). Events of conversion of Cys to Sec were not found. On the right, the number of selenoproteins predicted in each species is shown.
Mentions: We characterized vertebrate selenoproteomes by searching for all known selenoproteins in Trace Archive, non-redundant, expressed sequence tag (EST), and genomic databases of 44 vertebrates (including 34 mammals) (Figure 1 and Supplementary Table S1). The search was supplemented with the analysis of SECIS elements via SECISearch [9], and with the subsequent phylogenetic analysis of proteins belonging to the same superfamily. Overall, the searches yielded 45 selenoproteins (selenoprotein subfamilies) in sequenced vertebrates, 28 of which were found in mammals (Table 1). However, none of the mammals analyzed contained all these proteins: at most, 25 selenoproteins were detected. The largest selenoproteomes were found in bony fishes, with a maximum of 38 selenoproteins in zebrafish. The smallest selenoproteome (24 selenoprotein genes) was predicted in frog and in some mammals (Figure 1). 21 selenoproteins were found in all vertebrates: GPx1-4, TR1, TR3, Dio1, Dio2, Dio3, SelH, SelI, SelK, SelM, SelN, SelO, SelP, MsrB1 (methionine-R-sulfoxide reductase 1), SelS, SelT1, SelW1, Sep15. The other selenoproteins were found only in certain lineages, highlighting a dynamic process by which new selenoprotein genes were generated by duplication, while others were lost or replaced their Sec with cysteine (Cys). The predicted ancestral vertebrate selenoproteome is indicated in Figure 1, along with the details of its transformations across vertebrates. We found 28 proteins in the ancestral vertebrate selenoproteome and 25 in the ancestral mammalian selenoproteome.

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