Odorant binding proteins promote flight activity in the migratory insect, Helicoverpa armigera.

Jinghui Xi,Ka S Lim,Herbert Venthur,Amy Withers,Rafael A Homem,Shang Wang,Jing‐Jiang Zhou,Melissa Minter,Louise V Michaelson,Christopher M Jones

doi:10.1111/mec.15556

Abstract

Migratory insects are capable of actively sustaining powered flight for several hours. This extraordinary phenomenon requires a highly efficient transport system to cope with the energetic demands placed on the flight muscles. Here, we provide evidence that the role of the hydrophobic ligand binding of odorant binding proteins (OBPs) extends beyond their typical function in the olfactory system to support insect flight activity via lipid interactions. Transcriptomic and candidate gene analyses show that two phylogenetically clustered OBPs (OBP3/OBP6) are consistently over-expressed in adult moths of the migrant Old-World bollworm, Helicoverpa armigera, displaying sustained flight performance in flight activity bioassays. Tissue-specific over-expression of OBP6 was observed in the antennae, wings and thorax in long-fliers of H.armigera. Transgenic Drosophila flies over-expressing an H.armigera transcript of OBP6 (HarmOBP6) in the flight muscle attained higher flight speeds on a modified tethered flight system. Quantification of lipid molecules using mass spectrometry showed a depletion of triacylglyerol and phospholipids in flown moths. Protein homology models built from the crystal structure of a fatty acid carrier protein identified the binding site of OBP3 and OBP6 for hydrophobic ligand binding with both proteins exhibiting a stronger average binding affinity with triacylglycerols and phospholipids compared with other groups of ligands. We propose that HarmOBP3 and HarmOBP6 contribute to the flight capacity of a globally invasive and highly migratory noctuid moth, and in doing so, extend the function of this group of proteins beyond their typical role as chemosensory proteins in insects.

Highlights

Insect flight is one of the most energetically demanding processes in the animal kingdom
3.1 | Two Helicoverpa armigera-specific odorant binding proteins (OBPs) are overexpressed in the thorax of moths displaying prolonged flight activity
Each gene has a reported role in insect migration or sustained flight activity including those involved in circadian and photoreceptor processes (Reppert, Guerra, & Merlin, 2016), lipid metabolism (Arrese & Soulages, 2010), OBPs (Jones et al, 2015), flight muscle structure (Zhan et al, 2014), and the metabolism of proline and phenylalaine/tryptophan (Arrese & Soulages, 2010; Rio, Attardo, & Weiss, 2016; Figure 1b)

Summary

| INTRODUCTION

Insect flight is one of the most energetically demanding processes in the animal kingdom. Our recent transcriptomic work (RNA sequencing [RNA-seq]) in the Old World bollworm, Helicoverpa armigera, has shown that specific odorant binding proteins (OBPs), OBP3 and OBP6, are highly and consistently over-expressed in moths displaying sustained flight activity (Jones et al, 2015) This suggests that OBPs have a direct or indirect role in supporting insect flight and their function extends beyond their part in host-seeking and mating behaviour. A key characteristic that makes them such devastating pests is their ability to spread hundreds of kilometres in response to deteriorating local conditions This exacerbates their potential to invade new territories, as observed with the current fall armyworm (Spodoptera frugiperda), which has spread eastwards into the Asian continent and the rapid expansion of H. armigera in the Americas following its recent incursion (Fitt, 1989; Jones, Parry, Tay, Reynolds, & Chapman, 2019). Our findings provide evidence that a subset of OBPs are responsible for binding key lipids commonly used by insect migrants and that this relationship promotes insect flight

| MATERIALS AND METHODS

Experiment 3

| RESULTS AND DISCUSSION

| SUMMARY