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

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      Scientific Reports
      Nature Publishing Group UK

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          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. The L. decemlineata genome provides opportunities to investigate a broad range of phenotypes and to develop sustainable methods to control this widely successful pest.

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          TRP channels.

          The TRP (Transient Receptor Potential) superfamily of cation channels is remarkable in that it displays greater diversity in activation mechanisms and selectivities than any other group of ion channels. The domain organizations of some TRP proteins are also unusual, as they consist of linked channel and enzyme domains. A unifying theme in this group is that TRP proteins play critical roles in sensory physiology, which include contributions to vision, taste, olfaction, hearing, touch, and thermo- and osmosensation. In addition, TRP channels enable individual cells to sense changes in their local environment. Many TRP channels are activated by a variety of different stimuli and function as signal integrators. The TRP superfamily is divided into seven subfamilies: the five group 1 TRPs (TRPC, TRPV, TRPM, TRPN, and TRPA) and two group 2 subfamilies (TRPP and TRPML). TRP channels are important for human health as mutations in at least four TRP channels underlie disease.
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            Control of coleopteran insect pests through RNA interference.

            Commercial biotechnology solutions for controlling lepidopteran and coleopteran insect pests on crops depend on the expression of Bacillus thuringiensis insecticidal proteins, most of which permeabilize the membranes of gut epithelial cells of susceptible insects. However, insect control strategies involving a different mode of action would be valuable for managing the emergence of insect resistance. Toward this end, we demonstrate that ingestion of double-stranded (ds)RNAs supplied in an artificial diet triggers RNA interference in several coleopteran species, most notably the western corn rootworm (WCR) Diabrotica virgifera virgifera LeConte. This may result in larval stunting and mortality. Transgenic corn plants engineered to express WCR dsRNAs show a significant reduction in WCR feeding damage in a growth chamber assay, suggesting that the RNAi pathway can be exploited to control insect pests via in planta expression of a dsRNA.
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              The genome of the model beetle and pest Tribolium castaneum.

              Tribolium castaneum is a member of the most species-rich eukaryotic order, a powerful model organism for the study of generalized insect development, and an important pest of stored agricultural products. We describe its genome sequence here. This omnivorous beetle has evolved the ability to interact with a diverse chemical environment, as shown by large expansions in odorant and gustatory receptors, as well as P450 and other detoxification enzymes. Development in Tribolium is more representative of other insects than is Drosophila, a fact reflected in gene content and function. For example, Tribolium has retained more ancestral genes involved in cell-cell communication than Drosophila, some being expressed in the growth zone crucial for axial elongation in short-germ development. Systemic RNA interference in T. castaneum functions differently from that in Caenorhabditis elegans, but nevertheless offers similar power for the elucidation of gene function and identification of targets for selective insect control.
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                Author and article information

                Contributors
                sean.schoville@wisc.edu
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                31 January 2018
                31 January 2018
                2018
                : 8
                : 1931
                Affiliations
                [1 ]ISNI 0000 0001 2167 3675, GRID grid.14003.36, Department of Entomology, , University of Wisconsin-Madison, ; Madison, USA
                [2 ]ISNI 0000 0004 1936 7689, GRID grid.59062.38, Department of Plant and Soil Sciences, , University of Vermont, ; Burlington, USA
                [3 ]ISNI 0000 0001 0930 2361, GRID grid.4514.4, Department of Biology, , Lund University, ; Lund, Sweden
                [4 ]ISNI 0000 0001 2179 9593, GRID grid.24827.3b, Department of Biological Sciences, , University of Cincinnati, ; Cincinnati, USA
                [5 ]ISNI 0000 0001 2153 9986, GRID grid.9764.c, Department of Molecular Physiology, , Christian-Albrechts-University at Kiel, ; Kiel, Germany
                [6 ]ISNI 0000 0001 2293 4611, GRID grid.261055.5, Department of Biological Sciences, , North Dakota State University, ; Fargo, USA
                [7 ]ISNI 0000 0001 2069 7798, GRID grid.5342.0, Department of Crop Protection, , Ghent University, ; Ghent, Belgium
                [8 ]ISNI 0000 0001 2113 2895, GRID grid.483014.a, USDA-ARS National Agricultural Library, ; Beltsville, MD USA
                [9 ]USDA-ARS Bee Research Lab, Beltsville, MD USA
                [10 ]ISNI 0000 0004 0404 0958, GRID grid.463419.d, USDA-ARS Insect Genetics and Biochemistry Research Unit, ; Fargo, ND USA
                [11 ]ISNI 0000 0001 2342 9668, GRID grid.14476.30, A.N. Belozersky Institute of Physico-Chemical Biology, , Lomonosov Moscow State University, ; Moskva, Russia
                [12 ]ISNI 0000 0004 0470 1162, GRID grid.7130.5, Department of Biology, Faculty of Science, , Prince of Songkla University, ; Amphoe Hat Yai, Thailand
                [13 ]ISNI 0000 0001 1456 7807, GRID grid.254444.7, Department of Biological Sciences, , Wayne State University, ; Detroit, USA
                [14 ]ISNI 0000 0001 2173 938X, GRID grid.5338.d, Department of Genetics, , University of Valencia, ; Valencia, Spain
                [15 ]ISNI 0000 0001 2160 926X, GRID grid.39382.33, Department of Molecular and Human Genetics, , Baylor College of Medicine, ; Houston, Texas USA
                [16 ]ISNI 0000 0004 1764 227X, GRID grid.419643.d, National Institute of Science Education and Research, ; Bhubaneswar, India
                [17 ]ISNI 0000 0004 1757 3470, GRID grid.5608.b, Department of Biology, , University of Padova, ; Padova, Italy
                [18 ]ISNI 0000 0004 0637 0790, GRID grid.419523.8, Department of Biotechnology and Systems Biology, , National Institute of Biology, ; Ljubljana, Slovenia
                [19 ]ISNI 0000 0001 1958 0162, GRID grid.413454.3, Institute of Biochemistry and Biophysics, , Polish Academy of Sciences, ; Warsaw, Poland
                [20 ]ISNI 0000 0001 2176 4817, GRID grid.5399.6, Architecture et Fonction des Macromolécules Biologiques, , CNRS, Aix-Marseille Université, ; 13288 Marseille, France
                [21 ]INRA, USC 1408 AFMB, F-13288 Marseille, France
                [22 ]ISNI 0000 0001 0619 1117, GRID grid.412125.1, Department of Biological Sciences, , King Abdulaziz University, ; King Abdulaziz, Saudi Arabia
                [23 ]ISNI 0000 0004 1936 8438, GRID grid.266539.d, Department of Entomology, , University of Kentucky, ; Lexington, USA
                [24 ]ISNI 0000 0004 4687 2082, GRID grid.264756.4, Department of Entomology, , Texas A&M University, ; College Station, USA
                [25 ]ISNI 0000 0001 2153 9986, GRID grid.9764.c, Department of Genetics & Molecular Biology in Botany, , Christian-Albrechts-University at Kiel, ; Kiel, Germany
                [26 ]ISNI 0000 0004 0492 0584, GRID grid.7497.d, Division of Molecular Genetic Epidemiology, , German Cancer Research Center, ; Heidelberg, Germany
                [27 ]ISNI 0000 0000 9750 7019, GRID grid.27871.3b, Department of Entomology, , Nanjing Agricultural University, ; Nanjing, China
                [28 ]ISNI 0000 0004 0555 3608, GRID grid.454320.4, Center for Data-Intensive Biomedicine and Biotechnology, , Skolkovo Institute of Science and Technology, ; Moscow, Russia
                [29 ]ISNI 0000 0004 1936 7806, GRID grid.62813.3e, Department of Biology, , Illinois Institute of Technology, ; Chicago, USA
                [30 ]ISNI 0000 0001 0674 4543, GRID grid.267474.4, Department of Biology, , University of Wisconsin-Oshkosh, ; Oshkosh, USA
                [31 ]ISNI 0000 0001 2231 4551, GRID grid.184769.5, Environmental Genomics and Systems Biology Division, , Lawrence Berkeley National Laboratory, ; Berkeley, USA
                [32 ]USDA-ARS Center for Grain and Animal Health Research, New York, USA
                [33 ]ISNI 0000 0000 8580 3777, GRID grid.6190.e, Institute for Developmental Biology, , University of Cologne, ; Köln, Germany
                [34 ]ISNI 0000 0000 8809 1613, GRID grid.7372.1, School of Life Sciences, , University of Warwick, Gibbet Hill Campus, ; England, UK
                [35 ]ISNI 0000 0004 0491 7131, GRID grid.418160.a, Department of Entomology, , Max Planck Institute for Chemical Ecology, ; Jena, Germany
                [36 ]ISNI 0000 0001 2176 4817, GRID grid.5399.6, INRA, , Aix-Marseille Université, UMR1163, Biodiversité et Biotechnologie Fongiques, ; Marseille, France
                [37 ]ISNI 0000 0004 1936 9991, GRID grid.35403.31, Department of Entomology, , University of Illinois at Urbana-Champaign, ; Champaign, IL USA
                [38 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Department of Entomology, , Michigan State University, ; East Lansing, USA
                [39 ]ISNI 0000 0001 0790 959X, GRID grid.411377.7, Department of Biology and School of Informatics and Computing, , Indiana University, ; Bloomington, USA
                [40 ]ISNI 0000 0000 9025 8099, GRID grid.239573.9, Center for Autoimmune Genomics and Etiology, Division of Biomedical Informatics and Division of Developmental Biology, , Cincinnati Children’s Hospital Medical Center, ; Cincinnati, USA
                [41 ]ISNI 0000 0001 2179 9593, GRID grid.24827.3b, Department of Pediatrics, , University of Cincinnati College of Medicine, ; Cincinnati, USA
                [42 ]ISNI 0000 0001 2285 7943, GRID grid.261331.4, Department of Entomology, , The Ohio State University, ; Columbus, USA
                [43 ]ISNI 0000 0001 2285 7943, GRID grid.261331.4, Center for Applied Plant Sciences, , The Ohio State University, ; Columbus, USA
                Author information
                http://orcid.org/0000-0001-7364-434X
                http://orcid.org/0000-0002-0747-8539
                http://orcid.org/0000-0002-1253-5550
                http://orcid.org/0000-0002-0165-399X
                http://orcid.org/0000-0001-9255-4294
                http://orcid.org/0000-0002-7687-5319
                http://orcid.org/0000-0003-4172-4059
                http://orcid.org/0000-0002-4578-844X
                http://orcid.org/0000-0002-0873-3247
                http://orcid.org/0000-0002-2918-8946
                http://orcid.org/0000-0001-8334-3313
                http://orcid.org/0000-0001-7977-9122
                Article
                20154
                10.1038/s41598-018-20154-1
                5792627
                29386578
                d60b24e2-a719-4814-bd2e-143fb0c9925e
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 17 October 2017
                : 13 January 2018
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