Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface

Abstract

BackgroundRelatively little is known about the genomic basis and evolution of wood-feeding in beetles. We undertook genome sequencing and annotation, gene expression assays, studies of plant cell wall degrading enzymes, and other functional and comparative studies of the Asian longhorned beetle, Anoplophora glabripennis, a globally significant invasive species capable of inflicting severe feeding damage on many important tree species. Complementary studies of genes encoding enzymes involved in digestion of woody plant tissues or detoxification of plant allelochemicals were undertaken with the genomes of 14 additional insects, including the newly sequenced emerald ash borer and bull-headed dung beetle.ResultsThe Asian longhorned beetle genome encodes a uniquely diverse arsenal of enzymes that can degrade the main polysaccharide networks in plant cell walls, detoxify plant allelochemicals, and otherwise facilitate feeding on woody plants. It has the metabolic plasticity needed to feed on diverse plant species, contributing to its highly invasive nature. Large expansions of chemosensory genes involved in the reception of pheromones and plant kairomones are consistent with the complexity of chemical cues it uses to find host plants and mates.ConclusionsAmplification and functional divergence of genes associated with specialized feeding on plants, including genes originally obtained via horizontal gene transfer from fungi and bacteria, contributed to the addition, expansion, and enhancement of the metabolic repertoire of the Asian longhorned beetle, certain other phytophagous beetles, and to a lesser degree, other phytophagous insects. Our results thus begin to establish a genomic basis for the evolutionary success of beetles on plants.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1088-8) contains supplementary material, which is available to authorized users.

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

“…Genomic data were made available through the Asian longhorned beetle genome project (McKenna et al 2016). Using TBLASTN (Altschul et al 1997), we searched the first draft of the A. glabripennis genome (NCBI: BioProject PRJNA167479) against a database of available coleopteran OR sequences: Tribolium castaneum (Herbst) (Engsontia et al 2008); Megacyllene caryae (Gahan) (Mitchell et al 2012); and Ips typographus (L.) and Dendroctonus ponderosae (Hopkins) (Andersson et al 2013).…”

“…All of these beetles belong to a single species-rich clade (series Cucujiformia) containing ~190,000 described extant species (McKenna et al 2015). Models of ORs were constructed from a combination of predictions by MAKER 2.0 (Canterel et al 2008), transcriptome support (McKenna et al 2016), and manual annotation in Geneious R6.1 (Biomatters, Ltd., Auckland, NZ). We discarded most partial models that were <100 amino acids in length or consisted of only a single apparent exon, to avoid designating separated exons of one receptor with two names.…”

“…Here, we present the OR family of A. glabripennis , annotated from the recent Asian longhorned beetle genome project (McKenna et al 2016). We compare these OR genes in the transcriptomes of male and female A. glabripennis to identify potential ORs that may be biased toward expression in one sex.…”

Anchored hybrid enrichment provides new insights into the phylogeny and evolution of longhorned beetles (Cerambycidae)

“…Compared to the subfamilies Lepturinae, Prioninae and Parandrinae, whose larvae mostly develop in decaying wood, species of Cerambycinae and Lamiinae also have higher capacities for introduction in living or freshly dead plants or construction wood and wood products (Cocquempot & Lindelöw, 2010;Raje et al, 2016). For instance, the Asian longhorned beetle, Anoplophora glabripennis Motschulsky, has recently shown the potential to spread after introduction and cause significant ecological and economic damage (Nowak et al, 2001;Meng et al, 2015;McKenna et al, 2016). Also, some terricolous root feeders (such as Philus Saunders or Migdolus Westwood of Vesperidae) may cause considerable damage to forest or agricultural plantations (Svacha et al, 1997;Machado & Habib, 2006).…”

Morphological and Molecular Perspectives on the Phylogeny, Evolution, and Classification of Weevils (Coleoptera: Curculionoidea): Proceedings from the 2016 International Weevil Meeting

“…Two scolytine genomes have been published (see [107]), but many more have now been sequenced by the McKenna lab from across the Phytophaga, including another 22 genomes from exemplars of Curculionoidea. He discussed collaborative studies on the glycoside hydrolase family of genes in the Phytophaga, some of which function in the digestion of wood (e.g., [108,109]). He talked briefly about the evolution of genes underlying specialized phytophagy in beetles and how this is related to the macroevolution of specialized plant feeding in weevils and other phytophagous beetles [110].…”