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Title: A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)

Abstract

The Colorado potato beetle is one of the most challenging agricultural pests to manage. It has shown a spectacular ability to adapt to a variety of solanaceaeous plants and variable climates during its global invasion, and, notably, to rapidly evolve insecticide resistance. To examine evidence of rapid evolutionary change, and to understand the genetic basis of herbivory and insecticide resistance, we tested for structural and functional genomic changes relative to other arthropod species using genome sequencing, transcriptomics, and community annotation. Two factors that might facilitate rapid evolutionary change include transposable elements, which comprise at least 17% of the genome and are rapidly evolving compared to other Coleoptera, and high levels of nucleotide diversity in rapidly growing pest populations. Adaptations to plant feeding are evident in gene expansions and differential expression of digestive enzymes in gut tissues, as well as expansions of gustatory receptors for bitter tasting. Surprisingly, the suite of genes involved in insecticide resistance is similar to other beetles. Finally, duplications in the RNAi pathway might explain why Leptinotarsa decemlineata has high sensitivity to dsRNA. In conclusion, the L. decemlineata genome provides opportunities to investigate a broad range of phenotypes and to develop sustainable methods to control this widelymore » successful pest.« less

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [5];  [6];  [2];  [7];  [8]; ORCiD logo [9]; ORCiD logo [8];  [7];  [1];  [4];  [10];  [11];  [12]; ORCiD logo [13];  [14];  [15] more »; ORCiD logo [16];  [17];  [18];  [19]; ORCiD logo [4];  [12];  [20];  [21]; ORCiD logo [22];  [23];  [24];  [23]; ORCiD logo [25];  [26];  [27];  [28];  [18];  [29]; ORCiD logo [20];  [30]; ORCiD logo [31];  [29];  [17];  [8];  [32];  [33];  [34];  [4];  [13]; ORCiD logo [7];  [35];  [36];  [6];  [37]; ORCiD logo [38];  [39];  [40];  [20];  [14] « less
+ Show Author Affiliations
  1. Univ. of Wisconsin, Madison, WI (United States). Dept. of Entomology
  2. Univ. of Vermont, Burlington, VT (United States). Dept. of Plant and Soil Sciences
  3. Lund Univ. (Sweden). Dept. of Biology
  4. Univ. of Cincinnati, OH (United States). Dept. of Biological Sciences
  5. Christian-Albrechts-Univ., Kiel (Germany). Dept. of Molecular Physiology
  6. North Dakota State Univ., Fargo, ND (United States). Dept. of Biological Sciences
  7. Ghent Univ., Ghent (Belgium). Dept. of Crop Protection
  8. US Dept. of Agriculture, Agricultural Research Service (USDA-ARS)., Beltsville, MD (United States). National Agricultural Library
  9. US Dept. of Agriculture, Agricultural Research Service (USDA-ARS)., Beltsville, MD (United States). Bee Research Lab.; US Dept. of Agriculture, Agricultural Research Service (USDA-ARS)., Fargo, ND (United States). Insect Genetics and Biochemistry Research Unit
  10. Lomonosov Moscow State Univ., Moskva (Russia). A.N. Belozersky Inst. of Physico-Chemical Biology
  11. Prince of Songkla Univ., Amphoe Hat Yai (Thailand). Dept. of Biology, Faculty of Science
  12. Wayne State Univ., Detroit, MI (United States). Dept. of Biological Sciences
  13. Univ. of Valencia (Spain). Dept. of Genetics
  14. Baylor College of Medicine, Houston, TX (United States). Dept. of Molecular and Human Genetics
  15. National Inst. of Science Education and Research, Bhubaneswar (India)
  16. Univ. of Padova, Padova (Italy). Dept. of Biology
  17. National Inst. of Biology, Ljubljana (Slovenia). Dept. of Biotechnology and Systems Biology
  18. Polish Academy of Sciences, Warsaw (Poland). Inst. of Biochemistry and Biophysics
  19. Aix-Marseille Univ., and CNRS, Marseille (France). Architecture et Fonction des Macromolecules Biologiques; French National Inst. for Agricultural Research (INRA), Paris (France); King Abdulaziz Univ., Jeddah (Saudi Arabia). Dept. of Biological Sciences
  20. Univ. of Kentucky, Lexington, KY (United States). Dept. of Entomology
  21. Texas A & M Univ., College Station, TX (United States). Dept. of Entomology
  22. Christian-Albrechts-Univ., Kiel (Germany). Dept. of Genetics & Molecular Biology in Botany; German Cancer Research Center, Heidelberg (Germany). Division of Molecular Genetic Epidemiology
  23. Nanjing Agricultural Univ., Nanjing (China). Dept. of Entomology
  24. Aix-Marseille Univ., and CNRS, Marseille (France). Architecture et Fonction des Macromolecules Biologiques; French National Inst. for Agricultural Research (INRA), Paris (France)
  25. Skolkovo Inst. of Science and Technology, Moscow, (Russia). Center for Data-Intensive Biomedicine and Biotechnology
  26. Illinois Inst. of Technology, Chicago, IL (United States). Dept. of Biology
  27. Univ. of Wisconsin, Oshkosh, WI (United States). Dept. of Biology
  28. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
  29. US Dept. of Agriculture, Agricultural Research Service (USDA-ARS)., NY (United States). Center for Grain and Animal Health Research
  30. Univ. of Cologne, Koln (Germany). Inst. for Developmental Biology; Univ. of Warwick, Gibbet Hill (United Kingdom). School of Life Sciences
  31. Max Planck Inst. for Chemical Ecology, Jena (Germany). Dept. of Entomology
  32. French National Inst. for Agricultural Research (INRA), Paris (France); Aix-Marseille Univ., Marseille (France). Biodiversite et Biotechnologie Fongiques
  33. US Dept. of Agriculture, Agricultural Research Service (USDA-ARS)., Fargo, ND (United States). Insect Genetics and Biochemistry Research Unit
  34. Univ. of Illinois, Urbana-Champaign, IL (United States). Dept. of Entomology
  35. Michigan State Univ., East Lansing, MI (United States). Dept. of Entomology
  36. Indiana Univ., Bloomington, IN (United States). Dept. of Biology and School of Informatics and Computing
  37. Univ. of Cologne, Koln (Germany). Inst. for Developmental Biology
  38. Cincinnati Children's Hospital Medical Center, Cincinnati, OH (United States). Center for Autoimmune Genomics and Etiology, Division of Biomedical Informatics and Division of Developmental Biology; Univ. of Cincinnati, OH (United States). College of Medicine, Dept. of Pediatrics
  39. The Ohio State Univ., Columbus, OH (United States). Dept of Entomology; The Ohio State Univ., Columbus, OH (United States). Center for Applied Plant Sciences
  40. USDA-ARS Insect Genetics and Biochemistry Research Unit, Fargo, ND (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH)
OSTI Identifier:
1433138
Grant/Contract Number:  
AC02-05CH11231; NHGRI U54 HG003273; K12 GM000708; 5R01GM080203; 5R01HG004483
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Schoville, Sean D., Chen, Yolanda H., Andersson, Martin N., Benoit, Joshua B., Bhandari, Anita, Bowsher, Julia H., Brevik, Kristian, Cappelle, Kaat, Chen, Mei-Ju M., Childers, Anna K., Childers, Christopher, Christiaens, Olivier, Clements, Justin, Didion, Elise M., Elpidina, Elena N., Engsontia, Patamarerk, Friedrich, Markus, Garcia-Robles, Inmaculada, Gibbs, Richard A., Goswami, Chandan, Grapputo, Alessandro, Gruden, Kristina, Grynberg, Marcin, Henrissat, Bernard, Jennings, Emily C., Jones, Jeffery W., Kalsi, Megha, Khan, Sher A., Kumar, Abhishek, Li, Fei, Lombard, Vincent, Ma, Xingzhou, Martynov, Alexander, Miller, Nicholas J., Mitchell, Robert F., Munoz-Torres, Monica, Muszewska, Anna, Oppert, Brenda, Palli, Subba Reddy, Panfilio, Kristen A., Pauchet, Yannick, Perkin, Lindsey C., Petek, Marko, Poelchau, Monica F., Record, Eric, Rinehart, Joseph P., Robertson, Hugh M., Rosendale, Andrew J., Ruiz-Arroyo, Victor M., Smagghe, Guy, Szendrei, Zsofia, Thomas, Gregg W. C., Torson, Alex S., Vargas Jentzsch, Iris M., Weirauch, Matthew T., Yates, Ashley D., Yocum, George D., Yoon, June-Sun, and Richards, Stephen. A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). United States: N. p., 2018. Web. doi:10.1038/s41598-018-20154-1.
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Schoville, Sean D., Chen, Yolanda H., Andersson, Martin N., Benoit, Joshua B., Bhandari, Anita, Bowsher, Julia H., Brevik, Kristian, Cappelle, Kaat, Chen, Mei-Ju M., Childers, Anna K., Childers, Christopher, Christiaens, Olivier, Clements, Justin, Didion, Elise M., Elpidina, Elena N., Engsontia, Patamarerk, Friedrich, Markus, Garcia-Robles, Inmaculada, Gibbs, Richard A., Goswami, Chandan, Grapputo, Alessandro, Gruden, Kristina, Grynberg, Marcin, Henrissat, Bernard, Jennings, Emily C., Jones, Jeffery W., Kalsi, Megha, Khan, Sher A., Kumar, Abhishek, Li, Fei, Lombard, Vincent, Ma, Xingzhou, Martynov, Alexander, Miller, Nicholas J., Mitchell, Robert F., Munoz-Torres, Monica, Muszewska, Anna, Oppert, Brenda, Palli, Subba Reddy, Panfilio, Kristen A., Pauchet, Yannick, Perkin, Lindsey C., Petek, Marko, Poelchau, Monica F., Record, Eric, Rinehart, Joseph P., Robertson, Hugh M., Rosendale, Andrew J., Ruiz-Arroyo, Victor M., Smagghe, Guy, Szendrei, Zsofia, Thomas, Gregg W. C., Torson, Alex S., Vargas Jentzsch, Iris M., Weirauch, Matthew T., Yates, Ashley D., Yocum, George D., Yoon, June-Sun, & Richards, Stephen. A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). United States. https://doi.org/10.1038/s41598-018-20154-1
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Schoville, Sean D., Chen, Yolanda H., Andersson, Martin N., Benoit, Joshua B., Bhandari, Anita, Bowsher, Julia H., Brevik, Kristian, Cappelle, Kaat, Chen, Mei-Ju M., Childers, Anna K., Childers, Christopher, Christiaens, Olivier, Clements, Justin, Didion, Elise M., Elpidina, Elena N., Engsontia, Patamarerk, Friedrich, Markus, Garcia-Robles, Inmaculada, Gibbs, Richard A., Goswami, Chandan, Grapputo, Alessandro, Gruden, Kristina, Grynberg, Marcin, Henrissat, Bernard, Jennings, Emily C., Jones, Jeffery W., Kalsi, Megha, Khan, Sher A., Kumar, Abhishek, Li, Fei, Lombard, Vincent, Ma, Xingzhou, Martynov, Alexander, Miller, Nicholas J., Mitchell, Robert F., Munoz-Torres, Monica, Muszewska, Anna, Oppert, Brenda, Palli, Subba Reddy, Panfilio, Kristen A., Pauchet, Yannick, Perkin, Lindsey C., Petek, Marko, Poelchau, Monica F., Record, Eric, Rinehart, Joseph P., Robertson, Hugh M., Rosendale, Andrew J., Ruiz-Arroyo, Victor M., Smagghe, Guy, Szendrei, Zsofia, Thomas, Gregg W. C., Torson, Alex S., Vargas Jentzsch, Iris M., Weirauch, Matthew T., Yates, Ashley D., Yocum, George D., Yoon, June-Sun, and Richards, Stephen. Wed . "A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)". United States. https://doi.org/10.1038/s41598-018-20154-1. https://www.osti.gov/servlets/purl/1433138.
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@article{osti_1433138,
title = {A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)},
author = {Schoville, Sean D. and Chen, Yolanda H. and Andersson, Martin N. and Benoit, Joshua B. and Bhandari, Anita and Bowsher, Julia H. and Brevik, Kristian and Cappelle, Kaat and Chen, Mei-Ju M. and Childers, Anna K. and Childers, Christopher and Christiaens, Olivier and Clements, Justin and Didion, Elise M. and Elpidina, Elena N. and Engsontia, Patamarerk and Friedrich, Markus and Garcia-Robles, Inmaculada and Gibbs, Richard A. and Goswami, Chandan and Grapputo, Alessandro and Gruden, Kristina and Grynberg, Marcin and Henrissat, Bernard and Jennings, Emily C. and Jones, Jeffery W. and Kalsi, Megha and Khan, Sher A. and Kumar, Abhishek and Li, Fei and Lombard, Vincent and Ma, Xingzhou and Martynov, Alexander and Miller, Nicholas J. and Mitchell, Robert F. and Munoz-Torres, Monica and Muszewska, Anna and Oppert, Brenda and Palli, Subba Reddy and Panfilio, Kristen A. and Pauchet, Yannick and Perkin, Lindsey C. and Petek, Marko and Poelchau, Monica F. and Record, Eric and Rinehart, Joseph P. and Robertson, Hugh M. and Rosendale, Andrew J. and Ruiz-Arroyo, Victor M. and Smagghe, Guy and Szendrei, Zsofia and Thomas, Gregg W. C. and Torson, Alex S. and Vargas Jentzsch, Iris M. and Weirauch, Matthew T. and Yates, Ashley D. and Yocum, George D. and Yoon, June-Sun and Richards, Stephen},
abstractNote = {The Colorado potato beetle is one of the most challenging agricultural pests to manage. It has shown a spectacular ability to adapt to a variety of solanaceaeous plants and variable climates during its global invasion, and, notably, to rapidly evolve insecticide resistance. To examine evidence of rapid evolutionary change, and to understand the genetic basis of herbivory and insecticide resistance, we tested for structural and functional genomic changes relative to other arthropod species using genome sequencing, transcriptomics, and community annotation. Two factors that might facilitate rapid evolutionary change include transposable elements, which comprise at least 17% of the genome and are rapidly evolving compared to other Coleoptera, and high levels of nucleotide diversity in rapidly growing pest populations. Adaptations to plant feeding are evident in gene expansions and differential expression of digestive enzymes in gut tissues, as well as expansions of gustatory receptors for bitter tasting. Surprisingly, the suite of genes involved in insecticide resistance is similar to other beetles. Finally, duplications in the RNAi pathway might explain why Leptinotarsa decemlineata has high sensitivity to dsRNA. In conclusion, the L. decemlineata genome provides opportunities to investigate a broad range of phenotypes and to develop sustainable methods to control this widely successful pest.},
doi = {10.1038/s41598-018-20154-1},
journal = {Scientific Reports},
number = 1,
volume = 8,
place = {United States},
year = {Wed Jan 31 00:00:00 EST 2018},
month = {Wed Jan 31 00:00:00 EST 2018}
}
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    • DOI: 10.1042/bst20180344

    Transcriptomics illuminate the phylogenetic backbone of tiger beetles
    journal, January 2020

    • Gough, Harlan M.; Allen, Julie M.; Toussaint, Emmanuel F. A.
    • Biological Journal of the Linnean Society, Vol. 129, Issue 3
    • DOI: 10.1093/biolinnean/blz195

    Identification of Cuticular Protein Genes in the Colorado Potato Beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)
    journal, January 2019

    • Wang, Yan-Wei; Li, Yu-Zhe; Li, Guo-Qing
    • Journal of Economic Entomology, Vol. 112, Issue 2
    • DOI: 10.1093/jee/toy396

    Functional diversification of horizontally acquired glycoside hydrolase family 45 (GH45) proteins in Phytophaga beetles
    journal, May 2019

    • Busch, André; Danchin, Etienne G. J.; Pauchet, Yannick
    • BMC Evolutionary Biology, Vol. 19, Issue 1
    • DOI: 10.1186/s12862-019-1429-9

    Genomic content of chemosensory genes correlates with host range in wood-boring beetles (Dendroctonus ponderosae, Agrilus planipennis, and Anoplophora glabripennis)
    journal, September 2019

    • Andersson, Martin N.; Keeling, Christopher I.; Mitchell, Robert F.
    • BMC Genomics, Vol. 20, Issue 1
    • DOI: 10.1186/s12864-019-6054-x

    Repertoire-wide gene structure analyses: a case study comparing automatically predicted and manually annotated gene models
    journal, October 2019

    Genomic insights into mite phylogeny, fitness, development, and reproduction
    journal, December 2019

    Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome
    journal, April 2019

    • Panfilio, Kristen A.; Vargas Jentzsch, Iris M.; Benoit, Joshua B.
    • Genome Biology, Vol. 20, Issue 1
    • DOI: 10.1186/s13059-019-1660-0

    Genomic signatures accompanying the dietary shift to phytophagy in polyphagan beetles
    journal, May 2019

    Gene content evolution in the arthropods
    journal, January 2020

    Evolution of Mutator transposable elements across eukaryotic diversity
    journal, March 2019

    Apollo: Democratizing genome annotation
    journal, February 2019

    Transcriptome Surveys in Silverfish Suggest a Multistep Origin of the Insect Odorant Receptor Gene Family
    journal, July 2019

    • Thoma, Michael; Missbach, Christine; Jordan, Melissa D.
    • Frontiers in Ecology and Evolution, Vol. 7
    • DOI: 10.3389/fevo.2019.00281

    Antennal Transcriptome Analysis of the Chemosensory Gene Families From Trichoptera and Basal Lepidoptera
    journal, September 2018

    • Yuvaraj, Jothi Kumar; Andersson, Martin N.; Zhang, Dan-Dan
    • Frontiers in Physiology, Vol. 9
    • DOI: 10.3389/fphys.2018.01365

    Genomic Signals of Adaptation towards Mutualism and Sociality in Two Ambrosia Beetle Complexes
    journal, December 2018

    • Blaz, Jazmín; Barrera-Redondo, Josué; Vázquez-Rosas-Landa, Mirna
    • Life, Vol. 9, Issue 1
    • DOI: 10.3390/life9010002

    Firefly genomes illuminate parallel origins of bioluminescence in beetles
    journal, October 2018

    Elevated rates of positive selection drive the evolution of pestiferousness in the Colorado potato beetle ( Leptinotarsa decemlineata , Say)
    journal, November 2020

    • Cohen, Zachary P.; Brevik, Kristian; Chen, Yolanda H.
    • Molecular Ecology, Vol. 30, Issue 1
    • DOI: 10.1111/mec.15703

    Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome.
    text, January 2019

    • Panfilio, Kristen A.; Vargas Jentzsch, Iris M.; Benoit, Joshua B.
    • Apollo - University of Cambridge Repository
    • DOI: 10.17863/cam.39052

    Genomic signatures accompanying the dietary shift to phytophagy in polyphagan beetles
    text, January 2019

    Changes in emergence phenology, fatty acid composition, and xenobiotic‐metabolizing enzyme expression is associated with increased insecticide resistance in the Colorado potato beetle
    journal, September 2019

    • Clements, Justin; Olson, Jake M.; Sanchez‐Sedillo, Benjamin
    • Archives of Insect Biochemistry and Physiology, Vol. 103, Issue 3
    • DOI: 10.1002/arch.21630

    Unzipping haplotypes in diploid and polyploid genomes
    journal, January 2020

    • Zhang, Xingtan; Wu, Ruoxi; Wang, Yibin
    • Computational and Structural Biotechnology Journal, Vol. 18
    • DOI: 10.1016/j.csbj.2019.11.011

    Transposable elements contribute to fungal genes and impact fungal lifestyle
    journal, March 2019

    • Muszewska, Anna; Steczkiewicz, Kamil; Stepniewska-Dziubinska, Marta
    • Scientific Reports, Vol. 9, Issue 1
    • DOI: 10.1038/s41598-019-40965-0

    Identification and evolution of glucosinolate sulfatases in a specialist flea beetle
    journal, October 2019

    Functional diversification of horizontally acquired glycoside hydrolase family 45 (GH45) proteins in Phytophaga beetles
    journal, May 2019

    • Busch, André; Danchin, Etienne G. J.; Pauchet, Yannick
    • BMC Evolutionary Biology, Vol. 19, Issue 1
    • DOI: 10.1186/s12862-019-1429-9

    Repertoire-wide gene structure analyses: a case study comparing automatically predicted and manually annotated gene models
    journal, October 2019

    Genomic insights into mite phylogeny, fitness, development, and reproduction
    journal, December 2019

    Draft Genome of a Blister Beetle Mylabris aulica
    journal, January 2020

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