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Genome Biol. 2016 Nov 11;17(1):227.

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 information

1
Department of Biological Sciences, University of Memphis, 3700 Walker Ave., Memphis, TN, 38152, USA. dmckenna@memphis.edu.
2
Feinstone Center for Genomic Research, University of Memphis, Memphis, TN, 38152, USA. dmckenna@memphis.edu.
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 Biological Sciences, University of Memphis, 3700 Walker Ave., Memphis, TN, 38152, USA.
19
Department of Biology, University of Rochester, Rochester, NY, 14627, USA.
20
USDA, Agricultural Research Service, Beneficial Insects Introduction Research, Newark, DE, 19713, USA.
21
Department of Biological Sciences, Wayne State University, Detroit, MI, 48202, USA.
22
School of Biology, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
23
Department of Entomology, Texas A&M University, College Station, TX, 77843, USA.
24
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.
25
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.
26
Graduate Institute of Biomedical Electronics and Bioinformatics, National Taiwan University, Taipei, 10617, Taiwan.
27
Department of Biology, Indiana University, Blomington, IN, 47405, USA.
28
Department of Microbiology, Immunology, and Biochemistry, University of Tennessee Health Science Center, Memphis, TN, 38163, USA.
29
Department of Entomology, University of Kentucky, Lexington, KY, 40546, USA.
30
Institute for Developmental Biology, University of Cologne, Cologne, 50674, Germany.
31
Department of Biology, Xavier University, Cincinnati, OH, 45207, USA.
32
Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA.
33
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA. stephenr@bcm.edu.

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.

KEYWORDS:

Chemoperception; Detoxification; Glycoside hydrolase; Horizontal gene transfer; Phytophagy; Xylophagy

PMID:
27832824
PMCID:
PMC5105290
DOI:
10.1186/s13059-016-1088-8
[Indexed for MEDLINE]
Free PMC Article

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