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Odorant receptors and antennal lobe morphology offer a new approach to understanding olfaction in the Asian longhorned beetle

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Abstract

The Asian longhorned beetle Anoplophora glabripennis (Motchulsky) is an exotic forest pest that has repeatedly invaded North America and Europe from Asia, and has the potential to kill millions of trees and cause billions of dollars in damage. Traps baited with an attractive mixture of volatile organic compounds from hosts have been of limited success in monitoring invasion sites. We propose that lures might be improved through studying the olfactory system of adult beetles, especially the gene family of odorant receptors (ORs) and the structure of the antennal lobes of the brain. Here, we report identification of 132 ORs in the genome of A. glabripennis (inclusive of one Orco gene and 11 pseudogenes), some of which are orthologous to known pheromone receptors of other cerambycid beetles. We also identified three ORs that are strongly biased toward expression in the female transcriptome, and a single OR strongly biased toward males. Three-dimensional reconstruction of the antennal lobes of adults suggested a male-specific macroglomerulus and several enlarged glomeruli in females. We predict that functional characterization of ORs and glomeruli will lead to identification of key odorants in the life history of A. glabripennis that may aid in monitoring and controlling future invasions.

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Abbreviations

AL:

Antennal lobe

IR:

Ionotropic receptor

MGC:

Macroglomerular complex

OR:

Odorant receptor

OSN:

Olfactory sensory neuron

VOC:

Volatile organic compound

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Acknowledgements

We thank Stephen Richards (Baylor College of Medicine Human Genome Sequencing Center) and other members of the Insect 5000 Genomes Asian Longhorned Beetle Genome Consortium for access to genomic and transcriptomic data. We also thank Patty Jansma, Hong Lei, and Kim Lance at the University of Arizona for assistance with brain imaging. Additional thanks to Carrie Crook and David Lance at the USDA-APHIS CPHST Lab and Kelli Hoover of PSU for providing live specimens of Anoplophora glabripennis. Funding was provided through an NIH postdoctoral training Grant (K12 GM000708) to RFM, the University of Memphis FedEx Institute, U.S. NSF Grant DEB1355169 and USDA-APHIS cooperative agreement 15-8130-0547-CA to DDM, and USDA-APHIS cooperative agreement 15-8130-1430-CA to TCB.

Note added in proof

As this paper went to press, we became aware of the recent work of Hu et al. (2016) Antennal transcriptome analysis of the Asian longhorned beetle Anoplophora glabripennis. Scientific Reports 6:26652, doi: 10.1038/srep26652, which reports findings complementary to ours.

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Author notes

  1. Robert F. Mitchell

    Present address: Department of Biology, University of Wisconsin Oshkosh, 142 Halsey Science Center, 800 Algoma Blvd., Oshkosh, WI, 54901, USA

Authors and Affiliations

  1. Department of Neuroscience, University of Arizona, Tucson, AZ, 85721, USA

    Robert F. Mitchell & John G. Hildebrand

  2. Center for Insect Science, University of Arizona, Tucson, AZ, 85721, USA

    Robert F. Mitchell & John G. Hildebrand

  3. Department of Entomology, Pennsylvania State University, University Park, PA, 16802, USA

    Loyal P. Hall & Thomas C. Baker

  4. USDA APHIS PPQ, San Diego, CA, 92154, USA

    Peter F. Reagel

  5. Department of Biological Sciences, University of Memphis, Memphis, TN, 38152, USA

    Duane D. McKenna

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Corresponding author

Correspondence to Robert F. Mitchell.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (Online Resource 1): Documentation (PDF 6 kb)

359_2016_1138_MOESM2_ESM.pdf

Supplementary material 2 (Online Resource 1A): Odorant receptors annotated from the genome of Anoplophora glabripennis. Model notes and missing exons (PDF 50 kb)

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Supplementary material 3 (Online Resource 1B): Odorant receptors annotated from the genome of Anoplophora glabripennis. Nucleotide sequences in FASTA format (FASTA 141 kb)

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Supplementary material 4 (Online Resource 1C): Odorant receptors annotated from the genome of Anoplophora glabripennis. Peptide sequences in FASTA format (FASTA 48 kb)

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Supplementary material 5 (Online Resource 2): Reads and sex bias of odorant receptor genes from transcriptomes of male and female Anoplophora glabripennis (PDF 67 kb)

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Supplementary material 6 (Online Resource 3): Description and volume of named glomeruli in the antennal lobe of Anoplophora glabripennis (PDF 327 kb)

Supplementary material 7 (Online Resource 4): Documentation (PDF 62 kb)

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Supplementary material 8 (Online Resource 4A): Confocal images stacks illustrating glomeruli in the antennal lobes of female Anoplophora glabripennis (AVI 23814 kb)

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Supplementary material 9 (Online Resource 4B): Confocal images stacks illustrating glomeruli in the antennal lobes of male Anoplophora glabripennis (AVI 18437 kb)

Supplementary material 10 (Online Resource 5): Documentation (PDF 6 kb)

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Supplementary material 11 (Online Resource 5A): Example 3D reconstruction of the antennal lobes of a female Anoplophora glabripennis. See Figure 4 for names of glomeruli and reference orientation (WRL 4749 kb)

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Supplementary material 12 (Online Resource 5B): Example 3D reconstructions of the antennal lobes of female Anoplophora glabripennis (WRL 3697 kb)

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Supplementary material 13 (Online Resource 5C): Example 3D reconstruction of the antennal lobes of a male Anoplophora glabripennis (WRL 3609 kb)

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Supplementary material 14 (Online Resource 5D): Example 3D reconstruction of the antennal lobes of a male Anoplophora glabripennis (WRL 2330 kb)

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Mitchell, R.F., Hall, L.P., Reagel, P.F. et al. Odorant receptors and antennal lobe morphology offer a new approach to understanding olfaction in the Asian longhorned beetle. J Comp Physiol A 203, 99–109 (2017). https://doi.org/10.1007/s00359-016-1138-4

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