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Unravelling the evolution of the Allatostatin-Type A, KISS and Galanin Peptide-Receptor gene families in Bilaterians: insights from Anopheles Mosquitoes

2015-07Journal article Open access
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dc.contributor.authorFelix, Rute C.
dc.contributor.authorTrindade, Marlene
dc.contributor.authorPires, Isa R. P.
dc.contributor.authorVera G Fonseca
dc.contributor.authorMartins, Rute S.
dc.contributor.authorSilveira, Henrique
dc.contributor.authorPower, Deborah M.
dc.contributor.authorCardoso, João CR
dc.date.accessioned2018-12-07T14:53:18Z
dc.date.available2018-12-07T14:53:18Z
dc.date.issued2015-07
dc.description.abstractAllatostatin type A receptors (AST-ARs) are a group of G-protein coupled receptors activated by members of the FGL-amide (AST-A) peptide family that inhibit food intake and development in arthropods. Despite their physiological importance the evolution of the AST-A system is poorly described and relatively few receptors have been isolated and functionally characterised in insects. The present study provides a comprehensive analysis of the origin and comparative evolution of the AST-A system. To determine how evolution and feeding modified the function of AST-AR the duplicate receptors in Anopheles mosquitoes, were characterised. Phylogeny and gene synteny suggested that invertebrate AST-A receptors and peptide genes shared a common evolutionary origin with KISS/GAL receptors and ligands. AST-ARs and KISSR emerged from a common gene ancestor after the divergence of GALRs in the bilaterian genome. In arthropods, the AST-A system evolved through lineage-specific events and the maintenance of two receptors in the flies and mosquitoes (Diptera) was the result of a gene duplication event. Speciation of Anophelesmosquitoes affected receptor gene organisation and characterisation of AST-AR duplicates (GPRALS1 and 2) revealed that in common with other insects, the mosquito receptors were activated by insect AST-A peptides and the iCa(2+)-signalling pathway was stimulated. GPRALS1 and 2 were expressed mainly in mosquito midgut and ovaries and transcript abundance of both receptors was modified by feeding. A blood meal strongly up-regulated expression of both GPRALS in the midgut (p < 0.05) compared to glucose fed females. Based on the results we hypothesise that the AST-A system in insects shared a common origin with the vertebrate KISS system and may also share a common function as an integrator of metabolism and reproduction. Highlights: AST-A and KISS/GAL receptors and ligands shared common ancestry prior to the protostome-deuterostome divergence. Phylogeny and gene synteny revealed that AST-AR and KISSR emerged after GALR gene divergence. AST-AR genes were present in the hemichordates but were lost from the chordates. In protostomes, AST-ARs persisted and evolved through lineage-specific events and duplicated in the arthropod radiation. Diptera acquired and maintained functionally divergent duplicate AST-AR genes.
dc.description.sponsorshipFoundation for Science and Technology, Portugal (FCT) [PTDC/BIA-BCM/114395/2009]; European Regional Development Fund (ERDF) COMPETE - Operational Competitiveness Programme; Portuguese funds through FCT Foundation for Science and Technology [PEst-C/MAR/LA0015/2013, UID/Multi/04326/2013, PEst-OE/SAU/LA0018/2013]; FCT [SFRH/BPD/89811/2012, SFRH/BPD/80447/2011, SFRH/BPD/66742/2009]; auxiliary research contract FCT Pluriannual funds [PEst-C/MAR/LA0015/2013, UID/Multi/04326/2013]
dc.description.versioninfo:eu-repo/semantics/publishedVersion
dc.identifier.doi10.1371/journal.pone.0130347
dc.identifier.issn1932-6203
dc.identifier.urihttp://hdl.handle.net/10400.1/11445
dc.language.isoeng
dc.peerreviewedyes
dc.publisherPublic Library of Science
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/
dc.subjectJuvenile-hormone synthesis
dc.subjectLarval Drosophila-Melanogaster
dc.subjectCockroach Blattella-Germanica
dc.subjectBeetle Tribolium-Castaneum
dc.subjectProtein-coupled receptors
dc.subjectCentral-nervous-system
dc.subjectDiploptera-Punctata
dc.subjectMolecular-cloning
dc.subjectAedes-Aegypti
dc.subjectGenomic organization
dc.titleUnravelling the evolution of the Allatostatin-Type A, KISS and Galanin Peptide-Receptor gene families in Bilaterians: insights from Anopheles Mosquitoes
dc.typejournal article
dspace.entity.typePublication
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/3599-PPCDT/PTDC%2FBIA-BCM%2F114395%2F2009/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/COMPETE/PEst-C%2FMAR%2FLA0015%2F2013/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/5876/UID%2FMulti%2F04326%2F2013/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/3599-PPCDT/PEst-OE%2FSAU%2FLA0018%2F2013/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/SFRH/SFRH%2FBPD%2F89811%2F2012/PT
oaire.citation.issue7
oaire.citation.startPagee0130347
oaire.citation.titlePLoS ONE
oaire.citation.volume10
oaire.fundingStream3599-PPCDT
oaire.fundingStreamCOMPETE
oaire.fundingStream5876
oaire.fundingStream3599-PPCDT
oaire.fundingStreamSFRH
person.familyNameTrindade
person.familyNameFonseca
person.familyNamePower
person.familyNameCardoso
person.givenNameMarlene
person.givenNameVera
person.givenNameDeborah Mary
person.givenNameJoão
person.identifier14332
person.identifier.ciencia-id891A-8A44-3CAE
person.identifier.ciencia-id8B16-F203-2AFC
person.identifier.orcid0000-0001-7072-3392
person.identifier.orcid0000-0002-5068-6253
person.identifier.orcid0000-0003-1366-0246
person.identifier.orcid0000-0001-7890-0170
person.identifier.ridM-4151-2013
person.identifier.scopus-author-id7101806760
person.identifier.scopus-author-id7201822956
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.identifierhttp://doi.org/10.13039/501100001871
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project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
rcaap.rightsopenAccess
rcaap.typearticle
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