Journal Article
Title | Unravelling the Evolution of the Allatostatin-Type A, KISS and Galanin Peptide-Receptor Gene Families in Bilaterians: Insights from Anopheles Mosquitoes. |
Publication Type | Journal Article |
Authors | Félix, RC, Trindade, M, Pires, IRP, Fonseca, VG, Martins, RS, Silveira, H, Power, DM, Cardoso, JCR |
Year of Publication | 2015 |
Journal | PLoS One |
Volume | 10 |
Issue | 7 |
Date Published | 2015 |
Pagination | e0130347 |
ISSN | 1932-6203 |
Keywords | Amino Acid Sequence, Animals, Anopheles, Calcium Signaling, Evolution, Molecular, Fat Body, Female, Gene Expression, Genome, Insect, Glucose, Insect Proteins, Intestines, Mice, Molecular Sequence Data, Multigene Family, Ovary, Phylogeny, Receptors, G-Protein-Coupled, Receptors, Galanin, Receptors, Neuropeptide, Reproduction, Sequence Alignment, Synteny |
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. |
DOI | 10.1371/journal.pone.0130347 |
Sapientia | |
Alternate Journal | PLoS ONE |
PubMed ID | 26135459 |
PubMed Central ID | PMC4489612 |