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

Duane D. McKenna, Erin D. Scully, Yannick Pauchet, Kelli Hoover, Roy Kirsch, Scott M. Geib, Robert F. Mitchell, Robert M. Waterhouse, Seung Joon Ahn, Deanna Arsala, Joshua B. Benoit, Heath Blackmon, Tiffany Bledsoe, Julia H. Bowsher, André Busch, Bernarda Calla, Hsu Chao, Anna K. Childers, Christopher Childers, Dave J. ClarkeLorna Cohen, Jeffery P. Demuth, Huyen Dinh, Harsha Vardhan Doddapaneni, Amanda Dolan, Jian J. Duan, Shannon Dugan, Markus Friedrich, Karl M. Glastad, Michael A.D. Goodisman, Stephanie Haddad, Yi Han, Daniel S.T. Hughes, Panagiotis Ioannidis, J. Spencer Johnston, Jeffery W. Jones, Leslie A. Kuhn, David R. Lance, Chien Yueh Lee, Sandra L. Lee, Han Lin, Jeremy A. Lynch, Armin P. Moczek, Shwetha C. Murali, Donna M. Muzny, David R. Nelson, Subba R. Palli, Kristen A. Panfilio, Dan Pers, Monica F. Poelchau, Honghu Quan, Jiaxin Qu, Ann M. Ray, Joseph P. Rinehart, Hugh M. Robertson, Richard Roehrdanz, Andrew J. Rosendale, Seunggwan Shin, Christian Silva, Alex S. Torson, Iris M.Vargas Jentzsch, John H. Werren, Kim C. Worley, George Yocum, Evgeny M. Zdobnov, Richard A. Gibbs, Stephen Richards

Research output: Contribution to journalArticle

70 Citations (Scopus)

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.

Original languageEnglish (US)
Article number227
JournalGenome biology
Volume17
Issue number1
DOIs
StatePublished - Nov 11 2016

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Anoplophora glabripennis
Introduced Species
Beetles
invasive species
beetle
innovation
genome
Genome
Coleoptera
Pheromones
allelochemical
gene
woody plant
enzyme
allelochemicals
Plant Cells
woody plants
genomics
Cell Wall
Insects

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Cell Biology

Cite this

Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle-plant interface. / McKenna, Duane D.; Scully, Erin D.; Pauchet, Yannick; Hoover, Kelli; Kirsch, Roy; Geib, Scott M.; Mitchell, Robert F.; Waterhouse, Robert M.; Ahn, Seung Joon; Arsala, Deanna; Benoit, Joshua B.; Blackmon, Heath; Bledsoe, Tiffany; Bowsher, Julia H.; Busch, André; Calla, Bernarda; Chao, Hsu; Childers, Anna K.; Childers, Christopher; Clarke, Dave J.; Cohen, Lorna; Demuth, Jeffery P.; Dinh, Huyen; Doddapaneni, Harsha Vardhan; Dolan, Amanda; Duan, Jian J.; Dugan, Shannon; Friedrich, Markus; Glastad, Karl M.; Goodisman, Michael A.D.; Haddad, Stephanie; Han, Yi; Hughes, Daniel S.T.; Ioannidis, Panagiotis; Johnston, J. Spencer; Jones, Jeffery W.; Kuhn, Leslie A.; Lance, David R.; Lee, Chien Yueh; Lee, Sandra L.; Lin, Han; Lynch, Jeremy A.; Moczek, Armin P.; Murali, Shwetha C.; Muzny, Donna M.; Nelson, David R.; Palli, Subba R.; Panfilio, Kristen A.; Pers, Dan; Poelchau, Monica F.; Quan, Honghu; Qu, Jiaxin; Ray, Ann M.; Rinehart, Joseph P.; Robertson, Hugh M.; Roehrdanz, Richard; Rosendale, Andrew J.; Shin, Seunggwan; Silva, Christian; Torson, Alex S.; Jentzsch, Iris M.Vargas; Werren, John H.; Worley, Kim C.; Yocum, George; Zdobnov, Evgeny M.; Gibbs, Richard A.; Richards, Stephen.

In: Genome biology, Vol. 17, No. 1, 227, 11.11.2016.

Research output: Contribution to journalArticle

McKenna, DD, Scully, ED, Pauchet, Y, Hoover, K, Kirsch, R, Geib, SM, Mitchell, RF, Waterhouse, RM, Ahn, SJ, Arsala, D, Benoit, JB, Blackmon, H, Bledsoe, T, Bowsher, JH, Busch, A, Calla, B, Chao, H, Childers, AK, Childers, C, Clarke, DJ, Cohen, L, Demuth, JP, Dinh, H, Doddapaneni, HV, Dolan, A, Duan, JJ, Dugan, S, Friedrich, M, Glastad, KM, Goodisman, MAD, Haddad, S, Han, Y, Hughes, DST, Ioannidis, P, Johnston, JS, Jones, JW, Kuhn, LA, Lance, DR, Lee, CY, Lee, SL, Lin, H, Lynch, JA, Moczek, AP, Murali, SC, Muzny, DM, Nelson, DR, Palli, SR, Panfilio, KA, Pers, D, Poelchau, MF, Quan, H, Qu, J, Ray, AM, Rinehart, JP, Robertson, HM, Roehrdanz, R, Rosendale, AJ, Shin, S, Silva, C, Torson, AS, Jentzsch, IMV, Werren, JH, Worley, KC, Yocum, G, Zdobnov, EM, Gibbs, RA & 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, vol. 17, no. 1, 227. https://doi.org/10.1186/s13059-016-1088-8
McKenna, Duane D. ; Scully, Erin D. ; Pauchet, Yannick ; Hoover, Kelli ; Kirsch, Roy ; Geib, Scott M. ; Mitchell, Robert F. ; Waterhouse, Robert M. ; Ahn, Seung Joon ; Arsala, Deanna ; Benoit, Joshua B. ; Blackmon, Heath ; Bledsoe, Tiffany ; Bowsher, Julia H. ; Busch, André ; Calla, Bernarda ; Chao, Hsu ; Childers, Anna K. ; Childers, Christopher ; Clarke, Dave J. ; Cohen, Lorna ; Demuth, Jeffery P. ; Dinh, Huyen ; Doddapaneni, Harsha Vardhan ; Dolan, Amanda ; Duan, Jian J. ; Dugan, Shannon ; Friedrich, Markus ; Glastad, Karl M. ; Goodisman, Michael A.D. ; Haddad, Stephanie ; Han, Yi ; Hughes, Daniel S.T. ; Ioannidis, Panagiotis ; Johnston, J. Spencer ; Jones, Jeffery W. ; Kuhn, Leslie A. ; Lance, David R. ; Lee, Chien Yueh ; Lee, Sandra L. ; Lin, Han ; Lynch, Jeremy A. ; Moczek, Armin P. ; Murali, Shwetha C. ; Muzny, Donna M. ; Nelson, David R. ; Palli, Subba R. ; Panfilio, Kristen A. ; Pers, Dan ; Poelchau, Monica F. ; Quan, Honghu ; Qu, Jiaxin ; Ray, Ann M. ; Rinehart, Joseph P. ; Robertson, Hugh M. ; Roehrdanz, Richard ; Rosendale, Andrew J. ; Shin, Seunggwan ; Silva, Christian ; Torson, Alex S. ; Jentzsch, Iris M.Vargas ; Werren, John H. ; Worley, Kim C. ; Yocum, George ; Zdobnov, Evgeny M. ; Gibbs, Richard A. ; Richards, Stephen. / Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle-plant interface. In: Genome biology. 2016 ; Vol. 17, No. 1.
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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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T1 - Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle-plant interface

AU - McKenna, Duane D.

AU - Scully, Erin D.

AU - Pauchet, Yannick

AU - Hoover, Kelli

AU - Kirsch, Roy

AU - Geib, Scott M.

AU - Mitchell, Robert F.

AU - Waterhouse, Robert M.

AU - Ahn, Seung Joon

AU - Arsala, Deanna

AU - Benoit, Joshua B.

AU - Blackmon, Heath

AU - Bledsoe, Tiffany

AU - Bowsher, Julia H.

AU - Busch, André

AU - Calla, Bernarda

AU - Chao, Hsu

AU - Childers, Anna K.

AU - Childers, Christopher

AU - Clarke, Dave J.

AU - Cohen, Lorna

AU - Demuth, Jeffery P.

AU - Dinh, Huyen

AU - Doddapaneni, Harsha Vardhan

AU - Dolan, Amanda

AU - Duan, Jian J.

AU - Dugan, Shannon

AU - Friedrich, Markus

AU - Glastad, Karl M.

AU - Goodisman, Michael A.D.

AU - Haddad, Stephanie

AU - Han, Yi

AU - Hughes, Daniel S.T.

AU - Ioannidis, Panagiotis

AU - Johnston, J. Spencer

AU - Jones, Jeffery W.

AU - Kuhn, Leslie A.

AU - Lance, David R.

AU - Lee, Chien Yueh

AU - Lee, Sandra L.

AU - Lin, Han

AU - Lynch, Jeremy A.

AU - Moczek, Armin P.

AU - Murali, Shwetha C.

AU - Muzny, Donna M.

AU - Nelson, David R.

AU - Palli, Subba R.

AU - Panfilio, Kristen A.

AU - Pers, Dan

AU - Poelchau, Monica F.

AU - Quan, Honghu

AU - Qu, Jiaxin

AU - Ray, Ann M.

AU - Rinehart, Joseph P.

AU - Robertson, Hugh M.

AU - Roehrdanz, Richard

AU - Rosendale, Andrew J.

AU - Shin, Seunggwan

AU - Silva, Christian

AU - Torson, Alex S.

AU - Jentzsch, Iris M.Vargas

AU - Werren, John H.

AU - Worley, Kim C.

AU - Yocum, George

AU - Zdobnov, Evgeny M.

AU - Gibbs, Richard A.

AU - Richards, Stephen

PY - 2016/11/11

Y1 - 2016/11/11

N2 - 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.

AB - 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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