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The Evolution of Pepsinogen C Genes in Vertebrates: Duplication, Loss and Functional Diversification
BACKGROUND: 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....
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2012
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3298455/ https://www.ncbi.nlm.nih.gov/pubmed/22427897 http://dx.doi.org/10.1371/journal.pone.0032852 |
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author | Castro, Luís Filipe Costa Lopes-Marques, Monica Gonçalves, Odete Wilson, Jonathan Mark |
author_facet | Castro, Luís Filipe Costa Lopes-Marques, Monica Gonçalves, Odete Wilson, Jonathan Mark |
author_sort | Castro, Luís Filipe Costa |
collection | PubMed |
description | BACKGROUND: 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. METHODOLOGY/PRINCIPAL FINDINGS: 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. CONCLUSIONS: 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 | Online Article Text |
id | pubmed-3298455 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2012 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-32984552012-03-16 The Evolution of Pepsinogen C Genes in Vertebrates: Duplication, Loss and Functional Diversification Castro, Luís Filipe Costa Lopes-Marques, Monica Gonçalves, Odete Wilson, Jonathan Mark PLoS One Research Article BACKGROUND: 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. METHODOLOGY/PRINCIPAL FINDINGS: 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. CONCLUSIONS: 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. Public Library of Science 2012-03-09 /pmc/articles/PMC3298455/ /pubmed/22427897 http://dx.doi.org/10.1371/journal.pone.0032852 Text en Castro et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. |
spellingShingle | Research Article Castro, Luís Filipe Costa Lopes-Marques, Monica Gonçalves, Odete Wilson, Jonathan Mark The Evolution of Pepsinogen C Genes in Vertebrates: Duplication, Loss and Functional Diversification |
title | 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_short | 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 |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3298455/ https://www.ncbi.nlm.nih.gov/pubmed/22427897 http://dx.doi.org/10.1371/journal.pone.0032852 |
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