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

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, A...

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Autores principales: 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, HarshaVardhan, 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5105290/
https://www.ncbi.nlm.nih.gov/pubmed/27832824
http://dx.doi.org/10.1186/s13059-016-1088-8
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author 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, HarshaVardhan
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
author_facet 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, HarshaVardhan
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
author_sort McKenna, Duane D.
collection PubMed
description 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. ELECTRONIC SUPPLEMENTARY MATERIAL: 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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spelling pubmed-51052902016-11-14 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, HarshaVardhan 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 Biol Research 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-016-1088-8) contains supplementary material, which is available to authorized users. BioMed Central 2016-11-11 /pmc/articles/PMC5105290/ /pubmed/27832824 http://dx.doi.org/10.1186/s13059-016-1088-8 Text en © The Author(s). 2016 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.
spellingShingle Research
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, HarshaVardhan
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
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
title_full Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface
title_fullStr Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface
title_full_unstemmed Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface
title_short Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface
title_sort genome of the asian longhorned beetle (anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5105290/
https://www.ncbi.nlm.nih.gov/pubmed/27832824
http://dx.doi.org/10.1186/s13059-016-1088-8
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