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

PLoS One. 2015 Jul 2;10(7):e0130347. doi: 10.1371/journal.pone.0130347. eCollection 2015.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Anopheles / classification
  • Anopheles / genetics*
  • Anopheles / metabolism
  • Calcium Signaling
  • Evolution, Molecular
  • Fat Body / chemistry
  • Fat Body / metabolism
  • Female
  • Gene Expression
  • Genome, Insect*
  • Glucose / metabolism
  • Insect Proteins / chemistry
  • Insect Proteins / genetics*
  • Insect Proteins / metabolism
  • Intestinal Mucosa / metabolism
  • Intestines / chemistry
  • Mice
  • Molecular Sequence Data
  • Multigene Family
  • Ovary / chemistry
  • Ovary / metabolism
  • Phylogeny*
  • Receptors, G-Protein-Coupled / chemistry
  • Receptors, G-Protein-Coupled / genetics*
  • Receptors, G-Protein-Coupled / metabolism
  • Receptors, Galanin / chemistry
  • Receptors, Galanin / genetics*
  • Receptors, Galanin / metabolism
  • Receptors, Neuropeptide / chemistry
  • Receptors, Neuropeptide / genetics*
  • Receptors, Neuropeptide / metabolism
  • Reproduction / genetics
  • Sequence Alignment
  • Synteny

Substances

  • Insect Proteins
  • Receptors, G-Protein-Coupled
  • Receptors, Galanin
  • Receptors, Neuropeptide
  • Glucose

Grant support

This study was co-financed by the Foundation for Science and Technology, Portugal (FCT) project PTDC/BIA-BCM/114395/2009 and the European Regional Development Fund (ERDF) COMPETE - Operational Competitiveness Programme and Portuguese funds through FCT – Foundation for Science and Technology, under the project PEst-C/MAR/LA0015/2013, UID/Multi/04326/2013 and PEst-OE/SAU/LA0018/2013. RCF, VGF and RSM are in receipt of FCT post-doctoral grants SFRH/BPD/89811/2012, SFRH/BPD/80447/2011 and SFRH/BPD/66742/2009, respectively. JCRC is supported by an auxiliary research contract FCT Pluriannual funds attributed to CCMAR under the project PEst-C/MAR/LA0015/2013 and UID/Multi/04326/2013.