Authors

Duane D. McKenna, University of Memphis
Erin D. Scully, US Department of Agriculture
Yannick Pauchet, Max Planck Institute for Chemical Ecology, Germany
Kelli Hoover, The Pennsylvania State University
Roy Kirsch, Max Planck Institute for Chemical Ecology, Germany
Scott M. Geib, US Department of Agriculture
Robert F. Mitchell, University of Arizona
Robert M. Waterhouse, University of Geneva, Switzerland
Seung-Joon Ahn, Max Planck Institute for Chemical Ecology, Germany
Deanna Arsala, University of Illinois - Chicago
Joshua B. Benoit, University of Cincinnati
Heath Blackmon, University of Texas - Arlington
Tiffany Bledsoe, University of Arizona
Julia H. Bowsher, North Dakota State University
André Busch, Max Planck Institute for Chemical Ecology, Germany
Bernarda Calla, US Department of Agriculture
Hsu Chao, Baylor College of Medicine
Anna K. Childers, US Department of Agriculture
Christopher Childers, US Department of Agriculture
Dave J. Clarke, University of Memphis
Lorna Cohen, University of Illinois - Chicago
Jeffery P. Demuth, University of Texas - Arlington
Huyen Dinh, Baylor College of Medicine
HarshaVardhan Doddapaneni, Baylor College of Medicine
Amanda Dolan, University of Rochester
Jian J. Duan, US Department of Agriculture
Shannon Dugan, Baylor College of Medicine
Markus Friedrich, Wayne State University
Karl M. Glastad, Georgia Institute of Technology
Michael A. D. Goodisman, Georgia Institute of Technology
Stephanie Haddad, University of Memphis
Yi Han, Baylor College of Medicine
Daniel S. T. Hughes, Baylor College of Medicine
Panagiotis Ioannidis, University of Geneva, Switzerland
J. Spencer Johnston, Texas A & M University
Jeffery W. Jones, Wayne State University
Leslie A. Kuhn, Michigan State University
David R. Lance, US Department of Agriculture
Chien-Yueh Lee, US Department of Agriculture
Sandra L. Lee, Baylor College of Medicine
Han Lin, US Department of Agriculture
Jeremy A. Lynch, University of Illinois - Chicago
Armin P. Moczek, Indiana University
Shwetha C. Murali, Baylor College of Medicine
Donna M. Muzny, Baylor College of Medicine
David R. Nelson, University of Tennessee
Subba R. Palli, University of KentuckyFollow
Kristen A. Panfilio, University of Cologne, Germany
Dan Pers, University of Illinois - Chicago
Monica F. Poelchau, US Department of Agriculture
Honghu Quan, University of Illinois - Chicago
Jiaxin Qu, Baylor College of Medicine
Ann M. Ray, Xavier University
Joseph P. Rinehart, US Department of Agriculture
Hugh M. Robertson, University of Illinois - Urbana-Champaign
Richard Roehrdanz, US Department of Agriculture
Andrew J. Rosendale, University of Cincinnati
Seunggwan Shin, University of Memphis
Christian Silva, University of Rochester
Alex S. Torson, North Dakota State University
Iris M. Vargas Jentzsch, University of Cologne, Germany
John H. Werren, University of Rochester
Kim C. Worley, Baylor College of Medicine
George Yocum, US Department of Agriculture
Evgeny M. Zdobnov, University of Geneva, Switzerland
Richard A. Gibbs, Baylor College of Medicine
Stephen Richards, Baylor College of Medicine

Abstract

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.

Document Type

Article

Publication Date

11-11-2016

Notes/Citation Information

Published in Genome Biology, v. 17, 277, p. 1-18.

© The Author(s). 2016

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Digital Object Identifier (DOI)

https://doi.org/10.1186/s13059-016-1088-8

Funding Information

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.

Related Content

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).

13059_2016_1088_MOESM1_ESM.docx (37347 kB)
Additional file 1: Supplementary figures, tables, methods, and other text.

13059_2016_1088_MOESM2_ESM.xlsx (344 kB)
Additional file 2: Large supporting tables.

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