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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
  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 Lab. (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.
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. doi:10.1038/s41598-018-20154-1.
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. doi:10.1038/s41598-018-20154-1. https://www.osti.gov/servlets/purl/1433138.
@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 = {2018},
month = {1}
}

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