Flexible origin of hydrocarbon/pheromone precursors in Drosophila melanogaster

Claude Wicker-Thomas,Damien Garrido,Gwénaëlle Bontonou,Laura Napal,Nicolas Mazuras,Béatrice Denis,Thomas Rubin,Jean-Philippe Parvy,Jacques Montagne

doi:10.1194/jlr.m060368

Abstract

In terrestrial insects, cuticular hydrocarbons (CHCs) provide protection from desiccation. Specific CHCs can also act as pheromones, which are important for successful mating. Oenocytes are abdominal cells thought to act as specialized units for CHC biogenesis that consists of long-chain fatty acid (LCFA) synthesis, optional desaturation(s), elongation to very long-chain fatty acids (VLCFAs), and removal of the carboxyl group. By investigating CHC biogenesis in Drosophila melanogaster, we showed that VLCFA synthesis takes place only within the oenocytes. Conversely, several pathways, which may compensate for one another, can feed the oenocyte pool of LCFAs, suggesting that this step is a critical node for regulating CHC synthesis. Importantly, flies deficient in LCFA synthesis sacrificed their triacylglycerol stores while maintaining some CHC production. Moreover, pheromone production was lower in adult flies that emerged from larvae that were fed excess dietary lipids, and their mating success was lower. Further, we showed that pheromone production in the oenocytes depends on lipid metabolism in the fat tissue and that fatty acid transport protein, a bipartite acyl-CoA synthase (ACS)/FA transporter, likely acts through its ACS domain in the oenocyte pathway of CHC biogenesis. Our study highlights the importance of environmental and physiological inputs in regulating LCFA synthesis to eventually control sexual communication in a polyphagous animal.

Highlights

In terrestrial insects, cuticular hydrocarbons (CHCs) provide protection from desiccation
CHCs were almost fully depleted (Fig. 1C; supplementary Table 2A, B). This defect was a direct consequence of acetyl-CoA carboxylase (ACC) knockdown in the oenocytes: expression of svp-gal80 [25], which blocks Gal4 activity in the oenocytes (Fig. 1B, B’), completely rescued CHC production (Fig. 1D; supplementary Table 2A, B)
These findings indicate that very long-chain fatty acid (VLCFA) synthesis of CHC precursors takes place exclusively within the oenocytes

Summary

Introduction

Cuticular hydrocarbons (CHCs) provide protection from desiccation. Specific CHCs can act as pheromones, which are important for successful mating. We showed that pheromone production in the oenocytes depends on lipid metabolism in the fat tissue and that fatty acid transport protein, a bipartite acyl-CoA synthase (ACS)/FA transporter, likely acts through its ACS domain in the oenocyte pathway of CHC biogenesis. The integument is covered by molecules derived from lipids, including triacylglycerols (TAGs), waxes, and cuticular hydrocarbons (CHCs) [4, 5]. They may act as pheromones, where the chain length, the structure, and the position of double bonds in specific CHCs play a key role in sexual communication [6].

Methods

Results

Conclusion