TY - JOUR

T1 - Odorant binding proteins promote flight activity in the migratory insect, Helicoverpa armigera

AU - Wang, S.

AU - Minter, M.

AU - Homem, R.A.

AU - Michaelson, L.V.

AU - Venthur, H.

AU - Lim, K.S.

AU - Withers, A.

AU - Xi, J.

AU - Jones, C.M.

AU - Zhou, J.-J.

PY - 2020/10/1

Y1 - 2020/10/1

N2 - 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. 

AB - 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. 

KW - Helicoverpa

KW - insect migration

KW - odorant binding proteins

U2 - 10.1111/mec.15556

DO - 10.1111/mec.15556

M3 - Journal article

VL - 29

SP - 3795

EP - 3808

JO - Molecular Ecology

JF - Molecular Ecology

SN - 0962-1083

IS - 19

ER -