Origin and functional diversification of an amphibian defense peptide arsenal.
The skin secretion of many amphibians contains an arsenal of bioactive molecules, including hormone-like peptides (HLPs) acting as defense toxins against predators, and antimicrobial peptides (AMPs) providing protection against infectious microorganisms. Several amphibian taxa seem to have independe...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2013-01-01
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| Series: | PLoS Genetics |
| Online Access: | http://europepmc.org/articles/PMC3731216?pdf=render |
| _version_ | 1811296187595096064 |
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| author | Kim Roelants Bryan G Fry Lumeng Ye Benoit Stijlemans Lea Brys Philippe Kok Elke Clynen Liliane Schoofs Pierre Cornelis Franky Bossuyt |
| author_facet | Kim Roelants Bryan G Fry Lumeng Ye Benoit Stijlemans Lea Brys Philippe Kok Elke Clynen Liliane Schoofs Pierre Cornelis Franky Bossuyt |
| author_sort | Kim Roelants |
| collection | DOAJ |
| description | The skin secretion of many amphibians contains an arsenal of bioactive molecules, including hormone-like peptides (HLPs) acting as defense toxins against predators, and antimicrobial peptides (AMPs) providing protection against infectious microorganisms. Several amphibian taxa seem to have independently acquired the genes to produce skin-secreted peptide arsenals, but it remains unknown how these originated from a non-defensive ancestral gene and evolved diverse defense functions against predators and pathogens. We conducted transcriptome, genome, peptidome and phylogenetic analyses to chart the full gene repertoire underlying the defense peptide arsenal of the frog Silurana tropicalis and reconstruct its evolutionary history. Our study uncovers a cluster of 13 transcriptionally active genes, together encoding up to 19 peptides, including diverse HLP homologues and AMPs. This gene cluster arose from a duplicated gastrointestinal hormone gene that attained a HLP-like defense function after major remodeling of its promoter region. Instead, new defense functions, including antimicrobial activity, arose by mutation of the precursor proteins, resulting in the proteolytic processing of secondary peptides alongside the original ones. Although gene duplication did not trigger functional innovation, it may have subsequently facilitated the convergent loss of the original function in multiple gene lineages (subfunctionalization), completing their transformation from HLP gene to AMP gene. The processing of multiple peptides from a single precursor entails a mechanism through which peptide-encoding genes may establish new functions without the need for gene duplication to avoid adaptive conflicts with older ones. |
| first_indexed | 2024-04-13T05:45:41Z |
| format | Article |
| id | doaj.art-3bcbf6501db44138810dbda65599068f |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-04-13T05:45:41Z |
| publishDate | 2013-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-3bcbf6501db44138810dbda65599068f2022-12-22T02:59:58ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042013-01-0198e100366210.1371/journal.pgen.1003662Origin and functional diversification of an amphibian defense peptide arsenal.Kim RoelantsBryan G FryLumeng YeBenoit StijlemansLea BrysPhilippe KokElke ClynenLiliane SchoofsPierre CornelisFranky BossuytThe skin secretion of many amphibians contains an arsenal of bioactive molecules, including hormone-like peptides (HLPs) acting as defense toxins against predators, and antimicrobial peptides (AMPs) providing protection against infectious microorganisms. Several amphibian taxa seem to have independently acquired the genes to produce skin-secreted peptide arsenals, but it remains unknown how these originated from a non-defensive ancestral gene and evolved diverse defense functions against predators and pathogens. We conducted transcriptome, genome, peptidome and phylogenetic analyses to chart the full gene repertoire underlying the defense peptide arsenal of the frog Silurana tropicalis and reconstruct its evolutionary history. Our study uncovers a cluster of 13 transcriptionally active genes, together encoding up to 19 peptides, including diverse HLP homologues and AMPs. This gene cluster arose from a duplicated gastrointestinal hormone gene that attained a HLP-like defense function after major remodeling of its promoter region. Instead, new defense functions, including antimicrobial activity, arose by mutation of the precursor proteins, resulting in the proteolytic processing of secondary peptides alongside the original ones. Although gene duplication did not trigger functional innovation, it may have subsequently facilitated the convergent loss of the original function in multiple gene lineages (subfunctionalization), completing their transformation from HLP gene to AMP gene. The processing of multiple peptides from a single precursor entails a mechanism through which peptide-encoding genes may establish new functions without the need for gene duplication to avoid adaptive conflicts with older ones.http://europepmc.org/articles/PMC3731216?pdf=render |
| spellingShingle | Kim Roelants Bryan G Fry Lumeng Ye Benoit Stijlemans Lea Brys Philippe Kok Elke Clynen Liliane Schoofs Pierre Cornelis Franky Bossuyt Origin and functional diversification of an amphibian defense peptide arsenal. PLoS Genetics |
| title | Origin and functional diversification of an amphibian defense peptide arsenal. |
| title_full | Origin and functional diversification of an amphibian defense peptide arsenal. |
| title_fullStr | Origin and functional diversification of an amphibian defense peptide arsenal. |
| title_full_unstemmed | Origin and functional diversification of an amphibian defense peptide arsenal. |
| title_short | Origin and functional diversification of an amphibian defense peptide arsenal. |
| title_sort | origin and functional diversification of an amphibian defense peptide arsenal |
| url | http://europepmc.org/articles/PMC3731216?pdf=render |
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