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Relaxation of selective constraints causes independent selenoprotein extinction in insect genomes.

Chapple CE, Guigó R - PLoS ONE (2008)

Bottom Line: We have found that five insect species have completely lost the ability to encode selenoproteins and that selenoprotein loss in these species, although so far confined to the Endopterygota infraclass, cannot be attributed to a single evolutionary event, but rather to multiple, independent events.We have also found that, while many selenoprotein factors are concomitantly lost with the selenoproteins, others are present and conserved in all investigated genomes, irrespective of whether they code for selenoproteins or not, suggesting that they are involved in additional, non-selenoprotein related functions.The dispensability of selenoproteins in insects may be related to the fundamental differences in antioxidant defense between these animals and other metazoans.

View Article: PubMed Central - PubMed

Affiliation: Center for Genomic Regulation, Universitat Pompeu Fabra and Institut Municipal d'Investigació Mèdica, Barcelona, Catalonia, Spain.

ABSTRACT

Background: Selenoproteins are a diverse family of proteins notable for the presence of the 21st amino acid, selenocysteine. Until very recently, all metazoan genomes investigated encoded selenoproteins, and these proteins had therefore been believed to be essential for animal life. Challenging this assumption, recent comparative analyses of insect genomes have revealed that some insect genomes appear to have lost selenoprotein genes.

Methodology/principal findings: In this paper we investigate in detail the fate of selenoproteins, and that of selenoprotein factors, in all available arthropod genomes. We use a variety of in silico comparative genomics approaches to look for known selenoprotein genes and factors involved in selenoprotein biosynthesis. We have found that five insect species have completely lost the ability to encode selenoproteins and that selenoprotein loss in these species, although so far confined to the Endopterygota infraclass, cannot be attributed to a single evolutionary event, but rather to multiple, independent events. Loss of selenoproteins and selenoprotein factors is usually coupled to the deletion of the entire no-longer functional genomic region, rather than to sequence degradation and consequent pseudogenisation. Such dynamics of gene extinction are consistent with the high rate of genome rearrangements observed in Drosophila. We have also found that, while many selenoprotein factors are concomitantly lost with the selenoproteins, others are present and conserved in all investigated genomes, irrespective of whether they code for selenoproteins or not, suggesting that they are involved in additional, non-selenoprotein related functions.

Conclusions/significance: Selenoproteins have been independently lost in several insect species, possibly as a consequence of the relaxation in insects of the selective constraints acting across metazoans to maintain selenoproteins. The dispensability of selenoproteins in insects may be related to the fundamental differences in antioxidant defense between these animals and other metazoans.

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Selenoprotein extinction in arthropoda.Species whose genomes do not code for selenoprotein genes are shown in red. Sec-encoding species are shown in green with the number of selenoproteins found in each genome in parentheses next to its name. Species for which the available data was inconclusive are shown in white. The phylogenetic relationships have been taken from the ncbi's Taxonomy database (http://www.ncbi.nlm.nih.gov/Taxonomy/) and the Tree of Life project (http://www.tolweb.org/tree/). The Drosphilidae tree was taken from the Drosophila Sequencing Consortium wiki (http://rana.lbl.gov/drosophila/caf1.html).
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pone-0002968-g008: Selenoprotein extinction in arthropoda.Species whose genomes do not code for selenoprotein genes are shown in red. Sec-encoding species are shown in green with the number of selenoproteins found in each genome in parentheses next to its name. Species for which the available data was inconclusive are shown in white. The phylogenetic relationships have been taken from the ncbi's Taxonomy database (http://www.ncbi.nlm.nih.gov/Taxonomy/) and the Tree of Life project (http://www.tolweb.org/tree/). The Drosphilidae tree was taken from the Drosophila Sequencing Consortium wiki (http://rana.lbl.gov/drosophila/caf1.html).

Mentions: We have extended our analysis by searching genomic, EST, cDNA and peptide sequences available for other arthropod species (including the Arachnids Ixodes scapularis and Amblyomma americanum, and the Crustacean Daphnia pulex ). Results are summarized in Figure 8. Since none of these genomes (except D. pulex) is complete, lack of evidence for selenoproteins cannot be taken to indicate total loss of selenoproteins in a given species. Results are interesting, notwithstanding. We have found no evidence of selenoprotein loss in the genomes of any species outside the Endopterygota. Within this infraclass, species of the Hymenoptera, Lepidoptera and Coleoptera orders whose genomes have been completely sequenced do not code for selenoprotein genes, and no evidence of selenoproteins can be found in the partially sequenced species from these orders. In contrast, within Diptera, we found both selenoprotein coding and non-coding species. In summary, existing data do not support selenoprotein loss outside the Endopterygota, but within this infraclass, the loss appears to be generalized across the orders investigated, with the exception of the Diptera.


Relaxation of selective constraints causes independent selenoprotein extinction in insect genomes.

Chapple CE, Guigó R - PLoS ONE (2008)

Selenoprotein extinction in arthropoda.Species whose genomes do not code for selenoprotein genes are shown in red. Sec-encoding species are shown in green with the number of selenoproteins found in each genome in parentheses next to its name. Species for which the available data was inconclusive are shown in white. The phylogenetic relationships have been taken from the ncbi's Taxonomy database (http://www.ncbi.nlm.nih.gov/Taxonomy/) and the Tree of Life project (http://www.tolweb.org/tree/). The Drosphilidae tree was taken from the Drosophila Sequencing Consortium wiki (http://rana.lbl.gov/drosophila/caf1.html).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2500217&req=5

pone-0002968-g008: Selenoprotein extinction in arthropoda.Species whose genomes do not code for selenoprotein genes are shown in red. Sec-encoding species are shown in green with the number of selenoproteins found in each genome in parentheses next to its name. Species for which the available data was inconclusive are shown in white. The phylogenetic relationships have been taken from the ncbi's Taxonomy database (http://www.ncbi.nlm.nih.gov/Taxonomy/) and the Tree of Life project (http://www.tolweb.org/tree/). The Drosphilidae tree was taken from the Drosophila Sequencing Consortium wiki (http://rana.lbl.gov/drosophila/caf1.html).
Mentions: We have extended our analysis by searching genomic, EST, cDNA and peptide sequences available for other arthropod species (including the Arachnids Ixodes scapularis and Amblyomma americanum, and the Crustacean Daphnia pulex ). Results are summarized in Figure 8. Since none of these genomes (except D. pulex) is complete, lack of evidence for selenoproteins cannot be taken to indicate total loss of selenoproteins in a given species. Results are interesting, notwithstanding. We have found no evidence of selenoprotein loss in the genomes of any species outside the Endopterygota. Within this infraclass, species of the Hymenoptera, Lepidoptera and Coleoptera orders whose genomes have been completely sequenced do not code for selenoprotein genes, and no evidence of selenoproteins can be found in the partially sequenced species from these orders. In contrast, within Diptera, we found both selenoprotein coding and non-coding species. In summary, existing data do not support selenoprotein loss outside the Endopterygota, but within this infraclass, the loss appears to be generalized across the orders investigated, with the exception of the Diptera.

Bottom Line: We have found that five insect species have completely lost the ability to encode selenoproteins and that selenoprotein loss in these species, although so far confined to the Endopterygota infraclass, cannot be attributed to a single evolutionary event, but rather to multiple, independent events.We have also found that, while many selenoprotein factors are concomitantly lost with the selenoproteins, others are present and conserved in all investigated genomes, irrespective of whether they code for selenoproteins or not, suggesting that they are involved in additional, non-selenoprotein related functions.The dispensability of selenoproteins in insects may be related to the fundamental differences in antioxidant defense between these animals and other metazoans.

View Article: PubMed Central - PubMed

Affiliation: Center for Genomic Regulation, Universitat Pompeu Fabra and Institut Municipal d'Investigació Mèdica, Barcelona, Catalonia, Spain.

ABSTRACT

Background: Selenoproteins are a diverse family of proteins notable for the presence of the 21st amino acid, selenocysteine. Until very recently, all metazoan genomes investigated encoded selenoproteins, and these proteins had therefore been believed to be essential for animal life. Challenging this assumption, recent comparative analyses of insect genomes have revealed that some insect genomes appear to have lost selenoprotein genes.

Methodology/principal findings: In this paper we investigate in detail the fate of selenoproteins, and that of selenoprotein factors, in all available arthropod genomes. We use a variety of in silico comparative genomics approaches to look for known selenoprotein genes and factors involved in selenoprotein biosynthesis. We have found that five insect species have completely lost the ability to encode selenoproteins and that selenoprotein loss in these species, although so far confined to the Endopterygota infraclass, cannot be attributed to a single evolutionary event, but rather to multiple, independent events. Loss of selenoproteins and selenoprotein factors is usually coupled to the deletion of the entire no-longer functional genomic region, rather than to sequence degradation and consequent pseudogenisation. Such dynamics of gene extinction are consistent with the high rate of genome rearrangements observed in Drosophila. We have also found that, while many selenoprotein factors are concomitantly lost with the selenoproteins, others are present and conserved in all investigated genomes, irrespective of whether they code for selenoproteins or not, suggesting that they are involved in additional, non-selenoprotein related functions.

Conclusions/significance: Selenoproteins have been independently lost in several insect species, possibly as a consequence of the relaxation in insects of the selective constraints acting across metazoans to maintain selenoproteins. The dispensability of selenoproteins in insects may be related to the fundamental differences in antioxidant defense between these animals and other metazoans.

Show MeSH