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

• Published in: Nature communications 2015-07, Vol.6 (1), p.7814, Article 7814
• Main Authors: Finn, Roderick Nigel, Chauvigné, François, Stavang, Jon Anders, Belles, Xavier, Cerdà, Joan
• Format: Article
• Language: English
• Subjects: 13; 13/44; 38/77; 631/181/2474; 631/181/757; 631/92/577; 64/114; 64/24; 82/80; Animals; Aquaglyceroporins; Aquaporin 4 - genetics; Aquaporin 4 - metabolism; Aquaporins - metabolism; Biological Transport - genetics; Cell Membrane - metabolism; Computer Simulation; Drosophila melanogaster; Evolution, Molecular; Glycerol - metabolism; Humanities and Social Sciences; Humans; Insecta - genetics; Insecta - metabolism; multidisciplinary; Mutagenesis, Site-Directed; Oocytes - metabolism; Phylogeny; Science; Science (multidisciplinary); Xenopus laevis
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/ncomms8814

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. Insects can accumulate high levels of glycerol as an adaptive response to dessication and freezing. Here, the authors show that glycerol transporters evolved from water-selective channels that co-opted the glycerol transport function of ancestral aquaglyceroporins in the oldest lineages of insects.