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ARS Home » Plains Area » Manhattan, Kansas » Center for Grain and Animal Health Research » Stored Product Insect and Engineering Research » Research » Publications at this Location » Publication #327762

Research Project: Ecology, Genomics, and Management of Stored Product Insects

Location: Stored Product Insect and Engineering Research

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

Author
item Mckenna, Duane - University Of Memphis
item Scully, Erin
item Pauchet, Yannick - Max Planck Society
item Hoover, Kelli - Pennsylvania State University
item Kirsch, Roy - Max Planck Society
item Geib, Scott
item Mitchell, Robert - University Of Arizona
item Waterhouse, Robert - Massachusetts Institute Of Technology
item Ahn, Seung-joon - Max Planck Society
item Arsala, Deanna - University Of Illinois
item Childers, Anna
item Benoit, Joshua - University Of Cincinnati
item Blackmon, Heath - University Of Texas
item Bledsoe, Tiffany - University Of Arizona
item Bowsher, Julia - North Dakota State University
item Busch, Andre - Max Planck Society
item Calla Zalles, Bernarda
item Chao, Hsu - Baylor College Of Medicine
item Childers, Christopher
item Clark, Dave - University Of Memphis
item Cohen, Lorna - University Of Illinois
item Demuth, Jeffery - University Of Texas
item Dinh, Huyen - Baylor College Of Medicine
item Doddapaneni, Harshavardhan - Baylor College Of Medicine
item Dolan, Amanda - University Of Rochester
item Duan, Jian
item Dugan, Shannon - Baylor College Of Medicine
item Friedrich, Markus - Wayne State University
item Glastad, Karl - Georgia Institute Of Technology
item Goodisman, Michael A. - Georgia Institute Of Technology
item Haddad, Stephanie - University Of Memphis
item Han, Yi - Baylor College Of Medicine
item Hughes, Daniel S. - Baylor College Of Medicine
item Ioannidis, Panagiotis - University Of Geneva
item Vargas Jentzsch, Iris - University Of Cologne
item Johnston, J. Spencer - Texas A&M University
item Jones, Jeffery - Wayne State University
item Kuhn, Leslie - Michigan State University
item Lance, David - Animal And Plant Health Inspection Service (APHIS)
item Lee, Chien-yueh - National Taiwan University
item Lee, Sandra - Baylor College Of Medicine
item Lin, Han - National Taiwan University
item Lynch, Jeremy - University Of Illinois
item Moczek, Armin - Indiana University
item Murali, Shwetha - Baylor College Of Medicine
item Muzny, Donna - Baylor College Of Medicine
item Nelson, David - University Of Tennessee
item Palli, Subba - University Of Kentucky
item Panfilio, Kristen - University Of Cologne
item Pers, Dan - University Of Illinois
item Poelchau, Monica
item Quan, Honghu - University Of Illinois
item Qu, Jiaxin - Baylor College Of Medicine
item Ray, Ann - Xavier University
item Rinehart, Joseph - Joe
item Robertson, Hugh - University Of Illinois
item Roehrdanz, Richard
item Rosendale, Andrew - University Of Cincinnati
item Shin, Seunggwan - University Of Memphis
item Silva, Christian - University Of Rochester
item Torson, Alex - North Dakota State University
item Werren, John - University Of Rochester
item Worley, Kim - Baylor College Of Medicine
item Yocum, George
item Zdobnov, Evgeny - University Of Geneva
item Gibbs, Richard - Baylor College Of Medicine
item 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
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.