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

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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.

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The online version of this article (doi:10.1186/s13059-016-1088-8) contains supplementary material, which is available to authorized users.

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Most cited references 58

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The genome of the model beetle and pest Tribolium castaneum.

Stephen H. Richards, Richard A. Gibbs, George Weinstock … (2008)

Tribolium castaneum is a member of the most species-rich eukaryotic order, a powerful model organism for the study of generalized insect development, and an important pest of stored agricultural products. We describe its genome sequence here. This omnivorous beetle has evolved the ability to interact with a diverse chemical environment, as shown by large expansions in odorant and gustatory receptors, as well as P450 and other detoxification enzymes. Development in Tribolium is more representative of other insects than is Drosophila, a fact reflected in gene content and function. For example, Tribolium has retained more ancestral genes involved in cell-cell communication than Drosophila, some being expressed in the growth zone crucial for axial elongation in short-germ development. Systemic RNA interference in T. castaneum functions differently from that in Caenorhabditis elegans, but nevertheless offers similar power for the elucidation of gene function and identification of targets for selective insect control.

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Temporal lags and overlap in the diversification of weevils and flowering plants.

Duane D McKenna, Andrea S Sequeira, Adriana E Marvaldi … (2009)

The extraordinary diversity of herbivorous beetles is usually attributed to coevolution with angiosperms. However, the degree and nature of contemporaneity in beetle and angiosperm diversification remain unclear. Here we present a large-scale molecular phylogeny for weevils (herbivorous beetles in the superfamily Curculionoidea), one of the most diverse lineages of insects, based on approximately 8 kilobases of DNA sequence data from a worldwide sample including all families and subfamilies. Estimated divergence times derived from the combined molecular and fossil data indicate diversification into most families occurred on gymnosperms in the Jurassic, beginning approximately 166 Ma. Subsequent colonization of early crown-group angiosperms occurred during the Early Cretaceous, but this alone evidently did not lead to an immediate and major diversification event in weevils. Comparative trends in weevil diversification and angiosperm dominance reveal that massive diversification began in the mid-Cretaceous (ca. 112.0 to 93.5 Ma), when angiosperms first rose to widespread floristic dominance. These and other evidence suggest a deep and complex history of coevolution between weevils and angiosperms, including codiversification, resource tracking, and sequential evolution.

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Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest

Christopher I. Keeling, Macaire Yuen, Nancy Y Liao … (2013)

Background The mountain pine beetle, Dendroctonus ponderosae Hopkins, is the most serious insect pest of western North American pine forests. A recent outbreak destroyed more than 15 million hectares of pine forests, with major environmental effects on forest health, and economic effects on the forest industry. The outbreak has in part been driven by climate change, and will contribute to increased carbon emissions through decaying forests. Results We developed a genome sequence resource for the mountain pine beetle to better understand the unique aspects of this insect's biology. A draft de novo genome sequence was assembled from paired-end, short-read sequences from an individual field-collected male pupa, and scaffolded using mate-paired, short-read genomic sequences from pooled field-collected pupae, paired-end short-insert whole-transcriptome shotgun sequencing reads of mRNA from adult beetle tissues, and paired-end Sanger EST sequences from various life stages. We describe the cytochrome P450, glutathione S-transferase, and plant cell wall-degrading enzyme gene families important to the survival of the mountain pine beetle in its harsh and nutrient-poor host environment, and examine genome-wide single-nucleotide polymorphism variation. A horizontally transferred bacterial sucrose-6-phosphate hydrolase was evident in the genome, and its tissue-specific transcription suggests a functional role for this beetle. Conclusions Despite Coleoptera being the largest insect order with over 400,000 described species, including many agricultural and forest pest species, this is only the second genome sequence reported in Coleoptera, and will provide an important resource for the Curculionoidea and other insects.

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Author and article information

Contributors

Duane D. McKenna: dmckenna@memphis.edu

Erin D. Scully: Erin.Scully@ARS.USDA.GOV

Yannick Pauchet: ypauchet@ice.mpg.de

Kelli Hoover: kxh25@psu.edu

Roy Kirsch: rkirsch@ice.mpg.de

Scott M. Geib: Scott.Geib@ars.usda.gov

Robert F. Mitchell: mitchellr@uwosh.edu

Robert M. Waterhouse: robert.waterhouse@gmail.com

Seung-Joon Ahn: sahn@ice.mpg.de

Deanna Arsala: darsal2@uic.edu

Joshua B. Benoit: benoitja@ucmail.uc.edu

Heath Blackmon: coleoguy@gmail.com

Tiffany Bledsoe: nikitaur1@gmail.com

Julia H. Bowsher: julia.bowsher@ndsu.edu

André Busch: abusch@ice.mpg.de

Bernarda Calla: calla2@illinois.edu

Hsu Chao: hchao@bcm.edu

Anna K. Childers: Anna.Bennett@ARS.USDA.GOV

Christopher Childers: christopher.childers@ars.usda.gov

Dave J. Clarke: djclarke@memphis.edu

Lorna Cohen: cohen36@uic.edu

Jeffery P. Demuth: jpdemuth@uta.edu

Huyen Dinh: hdinh@bcm.edu

HarshaVardhan Doddapaneni: doddapan@bcm.edu

Amanda Dolan: amanda.r.avery@rochester.edu

Jian J. Duan: Jian.Duan@ARS.USDA.GOV

Shannon Dugan: sdugan@bcm.edu

Markus Friedrich: friedrichwsu@gmail.com

Karl M. Glastad: karlglastad@gatech.edu

Michael A. D. Goodisman: michael.goodisman@biology.gatech.edu

Stephanie Haddad: stephanyhaddad@gmail.com

Yi Han: yhan@bcm.edu

Daniel S. T. Hughes: Daniel.Hughes@bcm.edu

Panagiotis Ioannidis: panos.ioannidis@gmail.com

J. Spencer Johnston: spencerj@TAMU.EDU

Jeffery W. Jones: jonesjefferyw@gmail.com

Leslie A. Kuhn: kuhnl@msu.edu

David R. Lance: David.R.Lance@aphis.usda.gov

Chien-Yueh Lee: chien-yueh.lee@ars.usda.gov

Sandra L. Lee: sllee@bcm.edu

Han Lin: hlin@ars.usda.gov

Jeremy A. Lynch: jlynch42@uic.edu

Armin P. Moczek: armin@indiana.edu

Shwetha C. Murali: ShwethaCanchi.Murali@bcm.edu

Donna M. Muzny: donnam@bcm.edu

David R. Nelson: drnelson1@gmail.com

Subba R. Palli: RPALLI@UKY.EDU

Kristen A. Panfilio: kpanfili@uni-koeln.de

Dan Pers: dpers3@uic.edu

Monica F. Poelchau: monica.poelchau@ars.usda.gov

Honghu Quan: hquan2@uic.edu

Jiaxin Qu: jiaxinqu@yahoo.com

Ann M. Ray: raya6@xavier.edu

Joseph P. Rinehart: joseph.rinehart@ars.usda.gov

Hugh M. Robertson: hughrobe@uiuc.edu

Richard Roehrdanz: richard.Roehrdanz@ars.usda.gov

Andrew J. Rosendale: andrew.rosendale@uc.edu

Seunggwan Shin: sshin4@memphis.edu

Christian Silva: christian.silva@rochester.edu

Alex S. Torson: alex.s.torson@my.ndsu.edu

Iris M. Vargas Jentzsch: ivargasj@uni-koeln.de

John H. Werren: jack.werren@rochester.edu

Kim C. Worley: kworley@bcm.edu

George Yocum: george.yocum@ars.usda.gov

Evgeny M. Zdobnov: Evgeny.Zdobnov@unige.ch

Richard A. Gibbs: agibbs@bcm.edu

Stephen Richards: stephenr@bcm.edu

Journal

Journal ID (nlm-ta): Genome Biol

Journal ID (iso-abbrev): Genome Biol

Title: Genome Biology

Publisher: BioMed Central (London )

ISSN (Print): 1474-7596

ISSN (Electronic): 1474-760X

Publication date (Electronic): 11 November 2016

Publication date PMC-release: 11 November 2016

Publication date Collection: 2016

Volume: 17

Electronic Location Identifier: 227

Affiliations

[1 ]Department of Biological Sciences, University of Memphis, 3700 Walker Ave., Memphis, TN 38152 USA

[2 ]Feinstone Center for Genomic Research, University of Memphis, Memphis, TN 38152 USA

[3 ]USDA, Agricultural Research Service, Center for Grain and Animal Health, Stored Product Insect and Engineering Research Unit, Manhattan, KS 66502 USA

[4 ]Department of Entomology, Max Planck Institute for Chemical Ecology, Jena, 07745, Germany

[5 ]Department of Entomology and Center for Chemical Ecology, The Pennsylvania State University, University Park, PA 16802 USA

[6 ]USDA, Agricultural Research Service, Daniel K Inouye US Pacific Basin Agricultural Research Center, Tropical Crop and Commodity Protection Research Unit, Hilo, HI 96720 USA

[7 ]Center for Insect Science and Department of Neuroscience, University of Arizona, Tucson, AZ 85721 USA

[8 ]Department of Biology, University of Wisconsin Oshkosh, Oshkosh, WI 54901 USA

[9 ]Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, Geneva, 1211 Switzerland

[10 ]The Massachusetts Institute of Technology and The Broad Institute of MIT and Harvard, Cambridge, MA 02142 USA

[11 ]Department of Biological Sciences, University of Illinois at Chicago, Chicago, IL 60607 USA

[12 ]Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221 USA

[13 ]Department of Biology, University of Texas at Arlington, Arlington, TX 76019 USA

[14 ]Department of Biological Sciences, North Dakota State University, Fargo, ND 58108 USA

[15 ]Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030 USA

[16 ]USDA, Agricultural Research Service, Red River Valley Agricultural Research Center, Biosciences Research Laboratory, Fargo, ND 58102, USA

[17 ]USDA, Agricultural Research Service, National Agricultural Library, Beltsville, MD 20705 USA

[18 ]Department of Biology, University of Rochester, Rochester, NY 14627 USA

[19 ]USDA, Agricultural Research Service, Beneficial Insects Introduction Research, Newark, DE 19713 USA

[20 ]Department of Biological Sciences, Wayne State University, Detroit, MI 48202 USA

[21 ]School of Biology, Georgia Institute of Technology, Atlanta, GA 30332 USA

[22 ]Department of Entomology, Texas A&M University, College Station, TX 77843 USA

[23 ]Department of Biochemistry and Molecular Biology, Department of Computers Science and Engineering, and Department of Fisheries and Wildlife, Michigan State University, East Lansing, MI 48824 USA

[24 ]USDA, Animal and Plant Health Inspection Service, Plant Pest and Quarantine, Center for Plant Health Science and Technology, Otis Laboratory, Buzzards Bay, MA 02542 USA

[25 ]Graduate Institute of Biomedical Electronics and Bioinformatics, National Taiwan University, Taipei, 10617 Taiwan

[26 ]Department of Biology, Indiana University, Blomington, IN 47405 USA

[27 ]Department of Microbiology, Immunology, and Biochemistry, University of Tennessee Health Science Center, Memphis, TN 38163 USA

[28 ]Department of Entomology, University of Kentucky, Lexington, KY 40546 USA

[29 ]Institute for Developmental Biology, University of Cologne, Cologne, 50674 Germany

[30 ]Department of Biology, Xavier University, Cincinnati, OH 45207 USA

[31 ]Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL 61801 USA

Article

Publisher ID: 1088

DOI: 10.1186/s13059-016-1088-8

PMC ID: 5105290

PubMed ID: 27832824

SO-VID: a4a342f2-152f-41f0-8fce-c4edbfb401c0

License:

Open AccessThis 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.

History

Date received : 4 August 2016

Date accepted : 19 October 2016

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000051, National Human Genome Research Institute;

Award ID: U54 HG003273

Award Recipient : Richard A. Gibbs

Funded by: FundRef http://dx.doi.org/10.13039/100006588, FedEx Institute of Technology, University of Memphis;

Funded by: U.S. National Science Foundation

Award ID: DEB1355169

Award Recipient : Duane D. McKenna

Funded by: USDA-APHIS

Award ID: cooperative agreement 15-8130-0547-CA

Award Recipient : Duane D. McKenna

Funded by: USDA NIFA

Award ID: 2015-67013-23287

Award Recipient : Erin D. Scully Kelli Hoover

Funded by: U. S. National Science Foundation

Award ID: IOS1120209

Award ID: IOS1256689

Award Recipient : Armin P. Moczek

Funded by: University of Cincinnati Faculty Development Research Grant

Funded by: Marie Curie International Outgoing Fellowship

Award ID: PIOF-GA-2011-303312

Award Recipient : Robert M. Waterhouse

Funded by: Swiss NSF

Award ID: 31003A-125350

Award ID: 31003A-143936

Award Recipient : Evgeny M. Zdobnov

Funded by: FundRef http://dx.doi.org/10.13039/501100004189, Max-Planck-Gesellschaft;

Funded by: German Research Foundation

Award ID: PA 2044/1-1

Award ID: SFB 680

Award Recipient : Kristen A. Panfilio

Funded by: NIH postdoctoral training grant

Award ID: 5K12 GM000708-15

Award Recipient : Robert F. Mitchell

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: chemoperception,detoxification,glycoside hydrolase,horizontal gene transfer,phytophagy,xylophagy

Data availability:

ScienceOpen disciplines: Genetics

Keywords: chemoperception, detoxification, glycoside hydrolase, horizontal gene transfer, phytophagy, xylophagy

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

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Abstract

Background

Results

Conclusions

Electronic supplementary material

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Evolutionary Cell Biology

Most cited references 58

The genome of the model beetle and pest Tribolium castaneum.

Temporal lags and overlap in the diversification of weevils and flowering plants.

Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest

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