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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.

Felix RC, Trindade M, Pires IR, Fonseca VG, Martins RS, Silveira H, Power DM, Cardoso JC - PLoS ONE (2015)

Bottom Line: 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.Diptera acquired and maintained functionally divergent duplicate AST-AR genes.

View Article: PubMed Central - PubMed

Affiliation: Comparative Endocrinology and Integrative Biology, Centre of Marine Sciences, Universidade do Algarve, Campus de Gambelas, 8005-139, Faro, Portugal.

ABSTRACT

Unlabelled: Allatostatin 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 Anopheles mosquitoes 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 iCa2+-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.

No MeSH data available.


Related in: MedlinePlus

Conserved gene synteny of the genome regions containing AST-A gene in A. gambiae, D. melanogaster and C. elegans (npl-5 and npl-6) compared to the human KISS/GAL/SPX chromosomes.The gene homologues in T. castaneum are also represented. Horizontal lines indicate chromosome fragments and coloured arrow identify genes and their orientation in the genome. Orthologue genes are indicated in the same colour and their positions are indicated below (Mb). Dotted boxes represent the absent human KISS and SPX2 genes (that emerged during early vertebrate tetraploidizations) [42,74] and the T. castaneum AST-A gene. Only shared gene family members are represented. The number of family members that map to the same chromosome is indicated and those closest to AST-A and KISS/GAL/SPX are represented. A full description of gene families and names and accession numbers is given in S4 Table.
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pone.0130347.g005: Conserved gene synteny of the genome regions containing AST-A gene in A. gambiae, D. melanogaster and C. elegans (npl-5 and npl-6) compared to the human KISS/GAL/SPX chromosomes.The gene homologues in T. castaneum are also represented. Horizontal lines indicate chromosome fragments and coloured arrow identify genes and their orientation in the genome. Orthologue genes are indicated in the same colour and their positions are indicated below (Mb). Dotted boxes represent the absent human KISS and SPX2 genes (that emerged during early vertebrate tetraploidizations) [42,74] and the T. castaneum AST-A gene. Only shared gene family members are represented. The number of family members that map to the same chromosome is indicated and those closest to AST-A and KISS/GAL/SPX are represented. A full description of gene families and names and accession numbers is given in S4 Table.

Mentions: The gene environment of insect receptor and peptide genes was compared with C. elegans and human (Figs 4 and 5). The genes in linkage with AST-AR in A. gambiae and D. melanogaster were compared to the homologue genomic regions of human GALR (GALR1, chr 18; GALR2, chr 17 and GALR3, chr 22), human KISSR1 (chr 19) and C. elegans npr-9 (chr X) (Fig 4, S3 Table). In A. gambiae GPRALS1 and GPRALS2 genes were localised on chr 2R, while in the D. melanogaster they mapped to chr X (DAR-1) and chr 3R (DAR-2), although gene synteny was retained. The genome arrangement of A. gambiae and D. melanogaster chromosome regions containing AST-ARs suggested that they underwent distinct evolutionary pressure after gene duplication. The conserved gene linkage between the insect and the nematode C. elegans orthologue regions suggested that duplication of AST-AR occurred after the divergence and radiation of the nematodes.


Unravelling the Evolution of the Allatostatin-Type A, KISS and Galanin Peptide-Receptor Gene Families in Bilaterians: Insights from Anopheles Mosquitoes.

Felix RC, Trindade M, Pires IR, Fonseca VG, Martins RS, Silveira H, Power DM, Cardoso JC - PLoS ONE (2015)

Conserved gene synteny of the genome regions containing AST-A gene in A. gambiae, D. melanogaster and C. elegans (npl-5 and npl-6) compared to the human KISS/GAL/SPX chromosomes.The gene homologues in T. castaneum are also represented. Horizontal lines indicate chromosome fragments and coloured arrow identify genes and their orientation in the genome. Orthologue genes are indicated in the same colour and their positions are indicated below (Mb). Dotted boxes represent the absent human KISS and SPX2 genes (that emerged during early vertebrate tetraploidizations) [42,74] and the T. castaneum AST-A gene. Only shared gene family members are represented. The number of family members that map to the same chromosome is indicated and those closest to AST-A and KISS/GAL/SPX are represented. A full description of gene families and names and accession numbers is given in S4 Table.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4489612&req=5

pone.0130347.g005: Conserved gene synteny of the genome regions containing AST-A gene in A. gambiae, D. melanogaster and C. elegans (npl-5 and npl-6) compared to the human KISS/GAL/SPX chromosomes.The gene homologues in T. castaneum are also represented. Horizontal lines indicate chromosome fragments and coloured arrow identify genes and their orientation in the genome. Orthologue genes are indicated in the same colour and their positions are indicated below (Mb). Dotted boxes represent the absent human KISS and SPX2 genes (that emerged during early vertebrate tetraploidizations) [42,74] and the T. castaneum AST-A gene. Only shared gene family members are represented. The number of family members that map to the same chromosome is indicated and those closest to AST-A and KISS/GAL/SPX are represented. A full description of gene families and names and accession numbers is given in S4 Table.
Mentions: The gene environment of insect receptor and peptide genes was compared with C. elegans and human (Figs 4 and 5). The genes in linkage with AST-AR in A. gambiae and D. melanogaster were compared to the homologue genomic regions of human GALR (GALR1, chr 18; GALR2, chr 17 and GALR3, chr 22), human KISSR1 (chr 19) and C. elegans npr-9 (chr X) (Fig 4, S3 Table). In A. gambiae GPRALS1 and GPRALS2 genes were localised on chr 2R, while in the D. melanogaster they mapped to chr X (DAR-1) and chr 3R (DAR-2), although gene synteny was retained. The genome arrangement of A. gambiae and D. melanogaster chromosome regions containing AST-ARs suggested that they underwent distinct evolutionary pressure after gene duplication. The conserved gene linkage between the insect and the nematode C. elegans orthologue regions suggested that duplication of AST-AR occurred after the divergence and radiation of the nematodes.

Bottom Line: 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.Diptera acquired and maintained functionally divergent duplicate AST-AR genes.

View Article: PubMed Central - PubMed

Affiliation: Comparative Endocrinology and Integrative Biology, Centre of Marine Sciences, Universidade do Algarve, Campus de Gambelas, 8005-139, Faro, Portugal.

ABSTRACT

Unlabelled: Allatostatin 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 Anopheles mosquitoes 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 iCa2+-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.

No MeSH data available.


Related in: MedlinePlus