Insect glycerol transporters evolved by functional co-option and gene replacement.

Roderick Nigel Finn,François Chauvigné,Joan Cerdà,Xavier Belles,Jon Anders Stavang

doi:10.1038/ncomms8814

Abstract

Transmembrane glycerol transport is typically facilitated by aquaglyceroporins in Prokaryota and Eukaryota. In holometabolan insects however, aquaglyceroporins are absent, yet several species possess polyol permeable aquaporins. It thus remains unknown how glycerol transport evolved in the Holometabola. By combining phylogenetic and functional studies, here we show that a more efficient form of glycerol transporter related to the water-selective channel AQP4 specifically evolved and multiplied in the insect lineage, resulting in the replacement of the ancestral branch of aquaglyceroporins in holometabolan insects. To recapitulate this evolutionary process, we generate specific mutants in distantly related insect aquaporins and human AQP4 and show that a single mutation in the selectivity filter converted a water-selective channel into a glycerol transporter at the root of the crown clade of hexapod insects. Integration of phanerozoic climate models suggests that these events were associated with the emergence of complete metamorphosis and the unparalleled radiation of insects.

Highlights

Transmembrane glycerol transport is typically facilitated by aquaglyceroporins in Prokaryota and Eukaryota
While maximum glycerol accumulation and cold tolerance predominantly occurs in the pupal stage[8,9,10], recent phylogenetic studies of insect aquaporins have suggested that members of the aquaporin gene superfamily known as aquaglyceroporin (Glp) channels, which typically transport water and glycerol, are absent in holometabolan insects[11,12,13]
The structural basis for the selective aquaporin permeation properties was resolved through crystallographic studies, which determined that conserved central Asn-Pro-Ala (NPA) motifs and a quartet of aromatic arginine residues in the outer channel vestibule form the major selectivity filters[22,23]

Summary

Introduction

Transmembrane glycerol transport is typically facilitated by aquaglyceroporins in Prokaryota and Eukaryota. Our data reveal that mutated water-selective channels co-opted the glycerol transport function of the ancestral Glps in the oldest lineages of hexapod insects.

Results

Conclusion