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

Authors: MCKENNA, DUANE - University Of Memphis; Scully, Erin; PAUCHET, YANNICK - Max Planck Society; HOOVER, KELLI - Pennsylvania State University; KIRSCH, ROY - Max Planck Society; Geib, Scott; MITCHELL, ROBERT - University Of Arizona; WATERHOUSE, ROBERT - Massachusetts Institute Of Technology; AHN, SEUNG-JOON - Max Planck Society; ARSALA, DEANNA - University Of Illinois; Childers, Anna; BENOIT, JOSHUA - University Of Cincinnati; BLACKMON, HEATH - University Of Texas; BLEDSOE, TIFFANY - University Of Arizona; BOWSHER, JULIA - North Dakota State University; BUSCH, ANDRE - Max Planck Society; Calla, Bernarda; CHAO, HSU - Baylor College Of Medicine; Childers, Christopher; CLARK, DAVE - University Of Memphis; COHEN, LORNA - University Of Illinois; DEMUTH, JEFFERY - University Of Texas; DINH, HUYEN - Baylor College Of Medicine; DODDAPANENI, HARSHAVARDHAN - Baylor College Of Medicine; DOLAN, AMANDA - University Of Rochester; Duan, Jian; DUGAN, SHANNON - Baylor College Of Medicine; FRIEDRICH, MARKUS - Wayne State University; GLASTAD, KARL - Georgia Institute Of Technology; GOODISMAN, MICHAEL A. - Georgia Institute Of Technology; HADDAD, STEPHANIE - University Of Memphis; HAN, YI - Baylor College Of Medicine; HUGHES, DANIEL S. - Baylor College Of Medicine; IOANNIDIS, PANAGIOTIS - University Of Geneva; VARGAS JENTZSCH, IRIS - University Of Cologne; JOHNSTON, J. SPENCER - Texas A&M University; JONES, JEFFERY - Wayne State University; KUHN, LESLIE - Michigan State University; LANCE, DAVID - Animal And Plant Health Inspection Service (APHIS); LEE, CHIEN-YUEH - National Taiwan University; LEE, SANDRA - Baylor College Of Medicine; LIN, HAN - National Taiwan University; LYNCH, JEREMY - University Of Illinois; MOCZEK, ARMIN - Indiana University; MURALI, SHWETHA - Baylor College Of Medicine; MUZNY, DONNA - Baylor College Of Medicine; NELSON, DAVID - University Of Tennessee; PALLI, SUBBA - University Of Kentucky; PANFILIO, KRISTEN - University Of Cologne; PERS, DAN - University Of Illinois; Poelchau, Monica; QUAN, HONGHU - University Of Illinois; QU, JIAXIN - Baylor College Of Medicine; RAY, ANN - Xavier University; Rinehart, Joe; ROBERTSON, HUGH - University Of Illinois; Roehrdanz, Richard; ROSENDALE, ANDREW - University Of Cincinnati; SHIN, SEUNGGWAN - University Of Memphis; SILVA, CHRISTIAN - University Of Rochester; TORSON, ALEX - North Dakota State University; WERREN, JOHN - University Of Rochester; WORLEY, KIM - Baylor College Of Medicine; Yocum, George; ZDOBNOV, EVGENY - University Of Geneva; GIBBS, RICHARD - Baylor College Of Medicine; RICHARDS, STEPHEN - Baylor College Of Medicine

Submitted to: Genome Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/17/2016
Publication Date: 11/14/2016
Publication URL: https://handle.nal.usda.gov/10113/5696757
Citation: McKenna, D.D., Scully, E.D., Pauchet, Y., Hoover, K., Kirsch, R., Geib, S.M., Mitchell, R.F., Waterhouse, R.M., Ahn, S., Arsala, D., Childers, A.K., Benoit, J.B., Blackmon, H., Bledsoe, T., Bowsher, J., Busch, A., Calla Zalles, B., Chao, H., Childers, C., Clark, D.J., Cohen, L., Demuth, J.P., Dinh, H., Doddapaneni, H., Dolan, A., Duan, J.J., Dugan, S., Friedrich, M., Glastad, K.M., Goodisman, M.D., Haddad, S., Han, Y., Hughes, D.T., Ioannidis, P., Vargas Jentzsch, I.M., Johnston, J., Jones, J.W., Kuhn, L.A., Lance, D.R., Lee, C., Lee, S.L., Lin, H., Lynch, J.A., Moczek, A.P., Murali, S.C., Muzny, D.M., Nelson, D.R., Palli, S.R., Panfilio, K.A., Pers, D., Poelchau, M.F., Quan, H., Qu, J., Ray, A.M., Rinehart, J.P., Robertson, H.M., Roehrdanz, R.L., Rosendale, A.J., Shin, S., Silva, C., Torson, A., Werren, J.H., Worley, K.C., Yocum, G.D., Zdobnov, E.M., Gibbs, R.A., Richards, S. 2016. Genome of the Asian longhorned beetle, Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle-plant interface. Genome Biology. 17:227. doi:10.1186/s13059-016-1088-8.

Interpretive Summary: The Asian longhorned beetle (AGLAB) is a globally significant pest that has become locally established in North America. This insect can attack at least 100 different hardwood tree species, including economically important orchard, ornamental and forest tree species and, unlike many other wood-borers, it can colonize both healthy and stressed hosts. Genome sequencing of AGLAB led to the identification of several families of genes capable of degrading plant cell walls and detoxifying plant defensive chemicals. Overall, these features provide AGLAB with the metabolic plasticity needed to feed on a broad range of host trees with different defense chemistry profiles, and contribute to its invasiveness. Functional characterization led to the identification of genes with the abilities to degrade cellulose, xylan, pectin, and xyloglucan, the main components of plant cell walls. Comparative genomic analyses involving 14 additional insect species revealed that many of the genes involved in plant cell wall digestion were originally acquired from bacteria and/or fungi. Many of these genes duplicated several times after their original introduction and diverged functionally, a process that was fundamental to the addition, expansion and enhancement of metabolic pathways in AGLAB. Our results thus begin to establish a genomic basis for the apparent evolutionary success of beetles on plants and allow us to begin to identify genomic factors linked to host range determination and invasiveness, which can provide new tools for risk assessment. Additionally, the identification of genes linked to key digestive and detoxification processes will ultimately provide novel tools for pest management against AGLAB and other invasive pests.

Technical Abstract: The Asian longhorned beetle (Anoplophora glabripennis; AGLAB) is a globally significant invasive species capable of inflicting severe feeding damage on many important orchard, ornamental and forest trees. Genome sequencing, annotation, gene expression assays, and functional and comparative genomic studies reveal that the AGLAB genome encodes a uniquely diverse arsenal of enzymes – some encoded by genes originally obtained from bacteria and fungi via horizontal gene transfer (HGT) – that can degrade the main polysaccharide networks in plant cell walls, detoxify plant allelochemicals, and otherwise facilitate specialized feeding on woody plants. AGLAB has the metabolic plasticity needed to feed on plant species with different chemistries, permitting colonization of a diverse range of host plants, and contributing to its highly invasive nature. Its metabolic capacity is further expanded through affiliations with gut microbes. Large expansions of chemosensory genes involved in the reception of pheromones and plant kairomones are consistent with the complexity of chemical cues used by AGLAB to find host plants and mates. Complimentary comparative studies of genes encoding key enzymes involved in the digestion of woody plant tissues or the detoxification of plant allelochemicals were undertaken with the genomes of AGLAB and 14 additional insects, including two additional newly-sequenced beetle genomes (studied here for the first time). These analyses reveal that HGT from bacteria and fungi, followed by gene amplification and functional divergence were fundamental to the addition, expansion and enhancement of the metabolic repertoire of AGLAB and certain other beetles, and to a lesser degree in other phytophagous insects.