Expansion of the fatty acyl reductase gene family shaped pheromone communication in Hymenoptera.

Michal Tupec,Petra Wenzelová,Irena Valterová,Heiko Vogel,Václav Janoušek,Darina Prchalová,Iva Pichová,Tereza Pavlíčková,Aleš Buček,Ullrich Jahn,Jiří Kindl

doi:10.7554/elife.39231

Abstract

Fatty acyl reductases (FARs) are involved in the biosynthesis of fatty alcohols that serve a range of biological roles. Insects typically harbor numerous FAR gene family members. While some FARs are involved in pheromone biosynthesis, the biological significance of the large number of FARs in insect genomes remains unclear.Using bumble bee (Bombini) FAR expression analysis and functional characterization, hymenopteran FAR gene tree reconstruction, and inspection of transposable elements (TEs) in the genomic environment of FARs, we uncovered a massive expansion of the FAR gene family in Hymenoptera, presumably facilitated by TEs. The expansion occurred in the common ancestor of bumble bees and stingless bees (Meliponini). We found that bumble bee FARs from the expanded FAR-A ortholog group contribute to the species-specific pheromone composition. Our results indicate that expansion and functional diversification of the FAR gene family played a key role in the evolution of pheromone communication in Hymenoptera.

Highlights

Accumulation of DNA sequencing data is greatly outpacing our ability to experimentally assess the function of the sequenced genes, and most of these genes are expected to never be functionally characterized (Koonin, 2005)
We assigned the names Fatty acyl reductases (FARs)-A to FAR-K to 11 FAR ortholog groups that were retrieved as branches with high bootstrap support in the FAR gene tree
The experimentally determined reductase specificity of FARs that are abundantly expressed in bumble bee male labial gland (LG) is consistent with their role in male marking pheromones (MMPs) biosynthesis

Summary

Introduction

Accumulation of DNA sequencing data is greatly outpacing our ability to experimentally assess the function of the sequenced genes, and most of these genes are expected to never be functionally characterized (Koonin, 2005). Direct experimental evidence of the function of gene family members is often unavailable or limited (Lespinet et al, 2002; Demuth et al, 2006; Rispe et al, 2008; Cortesi et al, 2015; Niimura and Nei, 2006). The most probable evolutionary fate of duplicated genes is the loss of one copy, the temporary redundancy accelerates gene sequence divergence and can result in gene subfunctionalization or neofunctionalization—acquisition of slightly different or completely novel functions in one copy of the gene (Innan and Kondrashov, 2010; Lynch and Conery, 2000). The alcohol-forming fatty acyl-CoA reductases (FARs, EC 1.2.1.84) belong to a multigene family that underwent a series of gene duplications and subsequent gene losses, pseudogenizations and possibly functional diversification of some of the maintained copies, following the birth-and-death

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