Background: Relatively 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.
Results: The 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.
Conclusions: Amplification 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.
Digital Object Identifier (DOI)
Funding for genome sequencing, assembly and automated annotation was provided by NHGRI grant U54 HG003273 to RAG. We acknowledge funding from the University of Memphis FedEx Institute, US NSF grant DEB1355169 and USDA-APHIS cooperative agreement 15-8130-0547-CA to DDM, USDA NIFA grant 2015-67013-23287 to KH and ES, NSF grant DEB1257053 to JHW, NSF grants IOS1120209 and IOS1256689 to APM, University of Cincinnati Faculty Development Research grant to JBB, Marie Curie International Outgoing Fellowship PIOF-GA-2011-303312 to RMW, Swiss NSF awards 31003A-125350 and 31003A-143936 to EMZ, Max-Planck-Gesellschaft to YP, RK and AB, German Research Foundation (DFG) grants PA 2044/1-1 and SFB 680 to KAP, and NIH postdoctoral training grant 5 K12 GM000708-15 to RFM.
All sequence data are publically available at the NCBI, bioproject number PRJNA167479. Additional file 1: Table S3 gives specific details of accession numbers for specific raw and assembled DNA and RNA sequences. In addition, gene models and a browser are available at the National Agricultural Library (https://i5k.nal.usda.gov/Anoplophora_glabripennis).
McKenna, Duane D.; Scully, Erin D.; Pauchet, Yannick; Hoover, Kelli; Kirsch, Roy; Geib, Scott M.; Mitchell, Robert F.; Waterhouse, Robert M.; Ahn, Seung-Joon; Arsala, Deanna; Benoit, Joshua B.; Blackmon, Heath; Bledsoe, Tiffany; Bowsher, Julia H.; Busch, André; Calla, Bernarda; Chao, Hsu; Childers, Anna K.; Childers, Christopher; Clarke, Dave J.; Cohen, Lorna; Demuth, Jeffery P.; Dinh, Huyen; Doddapaneni, HarshaVardhan; Dolan, Amanda; Duan, Jian J.; Dugan, Shannon; Friedrich, Markus; Glastad, Karl M.; Goodisman, Michael A. D.; Haddad, Stephanie; Han, Yi; Hughes, Daniel S. T.; Ioannidis, Panagiotis; Johnston, J. Spencer; Jones, Jeffery W.; Kuhn, Leslie A.; Lance, David R.; Lee, Chien-Yueh; Lee, Sandra L.; Lin, Han; Lynch, Jeremy A.; Moczek, Armin P.; Murali, Shwetha C.; Muzny, Donna M.; Nelson, David R.; Palli, Subba R.; Panfilio, Kristen A.; Pers, Dan; Poelchau, Monica F.; Quan, Honghu; Qu, Jiaxin; Ray, Ann M.; Rinehart, Joseph P.; Robertson, Hugh M.; Roehrdanz, Richard; Rosendale, Andrew J.; Shin, Seunggwan; Silva, Christian; Torson, Alex S.; Jentzsch, Iris M. Vargas; Werren, John H.; Worley, Kim C.; Yocum, George; Zdobnov, Evgeny M.; Gibbs, Richard A.; and Richards, Stephen, "Genome of the Asian Longhorned Beetle (Anoplophora glabripennis), a Globally Significant Invasive Species, Reveals Key Functional and Evolutionary Innovations at the Beetle-Plant Interface" (2016). Entomology Faculty Publications. 103.