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

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.

SUBMITTER: Mitchell RF

PROVIDER: S-EPMC5330384 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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

Mitchell Robert F RF Hall Loyal P LP Reagel Peter F PF McKenna Duane D DD Baker Thomas C TC Hildebrand John G JG

Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology 20170111 2

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 ...[more]

PMID: 28078425

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Project description:Wood is a highly intractable food source, yet many insects successfully colonize and thrive in this challenging niche. Overcoming the lignin barrier of wood is a key challenge in nutrient acquisition, but full depolymerization of intact lignin polymers has only been conclusively demonstrated in fungi and is not known to occur by enzymes produced by insects or bacteria. Previous research validated that lignocellulose and hemicellulose degradation occur within the gut of the wood boring insect, Anoplophora glabripennis (Asian longhorned beetle), and that a fungal species, Fusarium solani (ATCC MYA 4552), is consistently associated with the larval stage. While the nature of this relationship is unresolved, we sought to assess this fungal isolate's ability to degrade lignocellulose and cell wall polysaccharides and to extract nutrients from woody tissue. This gut-derived fungal isolate was inoculated onto a wood-based substrate and shotgun proteomics using Multidimensional Protein Identification Technology (MudPIT) was employed to identify 400 expressed proteins. Through this approach, we detected proteins responsible for plant cell wall polysaccharide degradation, including proteins belonging to 28 glycosyl hydrolase families and several cutinases, esterases, lipases, pectate lyases, and polysaccharide deacetylases. Proteinases with broad substrate specificities and ureases were observed, indicating that this isolate has the capability to digest plant cell wall proteins and recycle nitrogenous waste under periods of nutrient limitation. Additionally, several laccases, peroxidases, and enzymes involved in extracellular hydrogen peroxide production previously implicated in lignin depolymerization were detected. In vitro biochemical assays were conducted to corroborate MudPIT results and confirmed that cellulases, glycosyl hydrolases, xylanases, laccases, and Mn- independent peroxidases were active in culture; however, lignin- and Mn- dependent peroxidase activities were not detected While little is known about the role of filamentous fungi and their associations with insects, these findings suggest that this isolate has the endogenous potential to degrade lignocellulose and extract nutrients from woody tissue.

Project description:Culture-independent analysis of the gut of a wood-boring insect, Anoplophora glabripennis (Coleoptera: Cerambycidae), revealed a consistent association between members of the fungal Fusarium solani species complex and the larval stage of both colony-derived and wild A. glabripennis populations. Using the translation elongation factor 1-alpha region for culture-independent phylogenetic and operational taxonomic unit (OTU)-based analyses, only two OTUs were detected, suggesting that genetic variance at this locus was low among A. glabripennis-associated isolates. To better survey the genetic variation of F. solani associated with A. glabripennis, and establish its phylogenetic relationship with other members of the F. solani species complex, single spore isolates were created from different populations and multi-locus phylogenetic analysis was performed using a combination of the translation elongation factor alpha-1, internal transcribed spacer, and large subunit rDNA regions. These analyses revealed that colony-derived larvae reared in three different tree species or on artificial diet, as well as larvae from wild populations collected from three additional tree species in New York City and from a single tree species in Worcester, MA, consistently harbored F. solani within their guts. While there is some genetic variation in the F. solani carried between populations, within-population variation is low. We speculate that F. solani is able to fill a broad niche in the A. glabripennis gut, providing it with fungal lignocellulases to allow the larvae to grow and develop on woody tissue. However, it is likely that many F. solani genotypes could potentially fill this niche, so the relationship may not be limited to a single member of the F. solani species complex. While little is known about the role of filamentous fungi and their symbiotic associations with insects, this report suggests that larval A. glabripennis has developed an intimate relationship with F. solani that is not limited by geographic location or host tree.

Project description:BackgroundThe red turpentine beetle (RTB), Dendroctonus valens LeConte (Coleoptera: Curculionidae, Scolytinae), is a destructive invasive pest of conifers which has become the second most important forest pest nationwide in China. Dendroctonus valens is known to use host odors and aggregation pheromones, as well as non-host volatiles, in host location and mass-attack modulation, and thus antennal olfaction is of the utmost importance for the beetles' survival and fitness. However, information on the genes underlying olfaction has been lacking in D. valens. Here, we report the antennal transcriptome of D. valens from next-generation sequencing, with the goal of identifying the olfaction gene repertoire that is involved in D. valens odor-processing.ResultsWe obtained 51 million reads that were assembled into 61,889 genes, including 39,831 contigs and 22,058 unigenes. In total, we identified 68 novel putative odorant reception genes, including 21 transcripts encoding for putative odorant binding proteins (OBP), six chemosensory proteins (CSP), four sensory neuron membrane proteins (SNMP), 22 odorant receptors (OR), four gustatory receptors (GR), three ionotropic receptors (IR), and eight ionotropic glutamate receptors. We also identified 155 odorant/xenobiotic degradation enzymes from the antennal transcriptome, putatively identified to be involved in olfaction processes including cytochrome P450s, glutathione-S-transferases, and aldehyde dehydrogenase. Predicted protein sequences were compared with counterparts in Tribolium castaneum, Megacyllene caryae, Ips typographus, Dendroctonus ponderosae, and Agrilus planipennis.ConclusionThe antennal transcriptome described here represents the first study of the repertoire of odor processing genes in D. valens. The genes reported here provide a significant addition to the pool of identified olfactory genes in Coleoptera, which might represent novel targets for insect management. The results from our study also will assist with evolutionary analyses of coleopteran olfaction.

Dataset Information

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

Publications

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

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