The evolution of pepsinogen C genes in vertebrates: duplication, loss and functional diversification.
<h4>Background</h4>Aspartic proteases comprise a large group of enzymes involved in peptide proteolysis. This collection includes prominent enzymes globally categorized as pepsins, which are derived from pepsinogen precursors. Pepsins are involved in gastric digestion, a hallmark of vert...
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oai:doaj.org-article:236f0682c5b743899ed5a0088b9a3d552021-11-18T07:25:38ZThe evolution of pepsinogen C genes in vertebrates: duplication, loss and functional diversification.1932-620310.1371/journal.pone.0032852https://doaj.org/article/236f0682c5b743899ed5a0088b9a3d552012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22427897/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>Aspartic proteases comprise a large group of enzymes involved in peptide proteolysis. This collection includes prominent enzymes globally categorized as pepsins, which are derived from pepsinogen precursors. Pepsins are involved in gastric digestion, a hallmark of vertebrate physiology. An important member among the pepsinogens is pepsinogen C (Pgc). A particular aspect of Pgc is its apparent single copy status, which contrasts with the numerous gene copies found for example in pepsinogen A (Pga). Although gene sequences with similarity to Pgc have been described in some vertebrate groups, no exhaustive evolutionary framework has been considered so far.<h4>Methodology/principal findings</h4>By combining phylogenetics and genomic analysis, we find an unexpected Pgc diversity in the vertebrate sub-phylum. We were able to reconstruct gene duplication timings relative to the divergence of major vertebrate clades. Before tetrapod divergence, a single Pgc gene tandemly expanded to produce two gene lineages (Pgbc and Pgc2). These have been differentially retained in various classes. Accordingly, we find Pgc2 in sauropsids, amphibians and marsupials, but not in eutherian mammals. Pgbc was retained in amphibians, but duplicated in the ancestor of amniotes giving rise to Pgb and Pgc1. The latter was retained in mammals and probably in reptiles and marsupials but not in birds. Pgb was kept in all of the amniote clade with independent episodes of loss in some mammalian species. Lineage specific expansions of Pgc2 and Pgbc have also occurred in marsupials and amphibians respectively. We find that teleost and tetrapod Pgc genes reside in distinct genomic regions hinting at a possible translocation.<h4>Conclusions</h4>We conclude that the repertoire of Pgc genes is larger than previously reported, and that tandem duplications have modelled the history of Pgc genes. We hypothesize that gene expansion lead to functional divergence in tetrapods, coincident with the invasion of terrestrial habitats.Luís Filipe Costa CastroMonica Lopes-MarquesOdete GonçalvesJonathan Mark WilsonPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 7, Iss 3, p e32852 (2012) |
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Medicine R Science Q Luís Filipe Costa Castro Monica Lopes-Marques Odete Gonçalves Jonathan Mark Wilson The evolution of pepsinogen C genes in vertebrates: duplication, loss and functional diversification. |
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<h4>Background</h4>Aspartic proteases comprise a large group of enzymes involved in peptide proteolysis. This collection includes prominent enzymes globally categorized as pepsins, which are derived from pepsinogen precursors. Pepsins are involved in gastric digestion, a hallmark of vertebrate physiology. An important member among the pepsinogens is pepsinogen C (Pgc). A particular aspect of Pgc is its apparent single copy status, which contrasts with the numerous gene copies found for example in pepsinogen A (Pga). Although gene sequences with similarity to Pgc have been described in some vertebrate groups, no exhaustive evolutionary framework has been considered so far.<h4>Methodology/principal findings</h4>By combining phylogenetics and genomic analysis, we find an unexpected Pgc diversity in the vertebrate sub-phylum. We were able to reconstruct gene duplication timings relative to the divergence of major vertebrate clades. Before tetrapod divergence, a single Pgc gene tandemly expanded to produce two gene lineages (Pgbc and Pgc2). These have been differentially retained in various classes. Accordingly, we find Pgc2 in sauropsids, amphibians and marsupials, but not in eutherian mammals. Pgbc was retained in amphibians, but duplicated in the ancestor of amniotes giving rise to Pgb and Pgc1. The latter was retained in mammals and probably in reptiles and marsupials but not in birds. Pgb was kept in all of the amniote clade with independent episodes of loss in some mammalian species. Lineage specific expansions of Pgc2 and Pgbc have also occurred in marsupials and amphibians respectively. We find that teleost and tetrapod Pgc genes reside in distinct genomic regions hinting at a possible translocation.<h4>Conclusions</h4>We conclude that the repertoire of Pgc genes is larger than previously reported, and that tandem duplications have modelled the history of Pgc genes. We hypothesize that gene expansion lead to functional divergence in tetrapods, coincident with the invasion of terrestrial habitats. |
format |
article |
author |
Luís Filipe Costa Castro Monica Lopes-Marques Odete Gonçalves Jonathan Mark Wilson |
author_facet |
Luís Filipe Costa Castro Monica Lopes-Marques Odete Gonçalves Jonathan Mark Wilson |
author_sort |
Luís Filipe Costa Castro |
title |
The evolution of pepsinogen C genes in vertebrates: duplication, loss and functional diversification. |
title_short |
The evolution of pepsinogen C genes in vertebrates: duplication, loss and functional diversification. |
title_full |
The evolution of pepsinogen C genes in vertebrates: duplication, loss and functional diversification. |
title_fullStr |
The evolution of pepsinogen C genes in vertebrates: duplication, loss and functional diversification. |
title_full_unstemmed |
The evolution of pepsinogen C genes in vertebrates: duplication, loss and functional diversification. |
title_sort |
evolution of pepsinogen c genes in vertebrates: duplication, loss and functional diversification. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2012 |
url |
https://doaj.org/article/236f0682c5b743899ed5a0088b9a3d55 |
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