Multifaceted biological insights from a draft genome sequence of the tobacco hornworm moth, Manduca sexta

Type Article
Date 2016-09
Language English
Author(s) Kanost Michael R.1, Arrese Estela L.2, Cao XiaolongORCID3, Chen Yun-Ru4, Chellapilla Sanjay5, Goldsmith Marian R.6, Grosse-Wilde Ewald7, Heckel David G.8, Herndon Nicolae5, Jiang Haobo3, Papanicolaou AlexieORCID9, Qu Jiaxin10, Soulages Jose L.2, Vogel Heiko8, Walters James11, Waterhouse Robert M.12, 13, 14, 15, Ahn Seung-JoonORCID8, Almeida Francisca C.16, 17, An Chunju18, Aqrawi Peshtewani10, Bretschneider Anne8, Bryant William B.19, Bucks Sascha7, Chao Hsu10, Chevignon GermainORCID20, Christen Jayne M.1, Clarke David F.21, Dittmer Neal T.1, Ferguson Laura C. F.22, Garavelou Spyridoula23, Gordon Karl H. J.24, Gunaratna Ramesh T.3, Han Yi10, Hauser FrankORCID25, He Yan3, Heidel-Fischer Hanna8, Hirsh Ariana26, Hu Yingxia3, Jiang Hongbo27, Kalra Divya10, Klinner Christian7, Konig Christopher7, Kovar Christie10, Kroll Ashley R.28, Kuwar Suyog S.ORCID8, Lee Sandy L.10, Lehman Rudiger29, Li Kai30, Li Zhaofei31, Liang Hanquan32, Lovelace Shanna33, Lu Zhiqiang31, Mansfield Jennifer H.26, McCulloch Kyle J.8, 34, Mathew Tittu10, Morton Brian8, 26, Muzny Donna M.10, McCulloch Kyle J.8, 34, Mathew Tittu10, Morton Brian8, 26, Muzny Donna M.10, Neunemann David23, Ongeri Fiona35, Pauchet YannickORCID36, Pu Ling -Ling37, Pyrousis IoannisORCID16, 17, Rao Xiang -Jun28, Redding Amanda26, Roesel Charles38, Sanchez-Gracia AlejandroORCID3, Schaack Sarah39, Shukla Aditi40, Tetreau GuillaumeORCID21, Wang Yang10, Xiong Guang-Hua1, Traut Walther40, Walsh Tom K.21, Worley Kim C.10, Wu Di1, Wu Wenbi21, Wu Yuan-Qing10, Zhang Xiufeng3, Zou Zhen39, Zucker Hannah41, Briscoe Adriana D.34, Burmester ThorstenORCID42, Clem Rollie J.19, Feyereisen ReneORCID43, Grimmelikhuijzen Cornelis J. P.25, Hamodrakas Stavros J.44, Hansson Bill S.7, Huguet Elisabeth20, Jermiin Lars S.ORCID21, Lan Que45, Lehman Herman K.46, Lorenzen Marce47, Merzendorfer Hans48, Michalopoulos Ioannis23, Morton David B.49, Muthukrishnan Subbaratnam1, Oakeshott John G.21, Palmer Will50, Park Yoonseong51, Passarelli A. Lorena19, Rozas JulioORCID16, 17, Schwartz Lawrence M.52, Smith Wendy53, Southgate Agnes54, Vilcinskas Andreas55, Vogt Richard56, Wang Ping38, Werren John36, Yu Xiao-Qiang57, Zhou Jing-Jiang58, Brown Susan J.5, Scherer Steven E.10, Richards StephenORCID10, Blissard Gary W.4
Affiliation(s) 1 : Kansas State Univ, Dept Biochem & Mol Biophys, Manhattan, KS 66506 USA.
2 : Oklahoma State Univ, Dept Biochem & Mol Biol, Stillwater, OK 74078 USA.
3 : Oklahoma State Univ, Dept Entomol & Plant Pathol, Stillwater, OK 74078 USA.
4 : Cornell Univ, Boyce Thompson Inst, Tower Rd, Ithaca, NY 14853 USA.
5 : Kansas State Univ, Div Biol, KSU Bioinformat Ctr, Manhattan, KS 66506 USA.
6 : Univ Rhode Isl, Dept Biol Sci, Kingston, RI 02881 USA.
7 : Max Planck Inst Chem Ecol, Dept Evolutionary Neuroethol, Hans Knoell Str 8, D-07745 Jena, Germany.
8 : Max Planck Inst Chem Ecol, Dept Entomol, Hans Knoell Strasse 8, D-07745 Jena, Germany.
9 : Univ Western Sydney, Hawkesbury Inst Environm, Richmond, NSW 2753, Australia.
10 : Baylor Coll Med, Human Genome Sequencing Ctr, 1 Baylor Plaza, Houston, TX 77030 USA.
11 : Univ Kansas, Dept Ecol & Evolutionary Biol, Lawrence, KS 66045 USA.
12 : Univ Geneva, Dept Genet Med & Dev, Sch Med, Rue Michel Servet 1, CH-1211 Geneva, Switzerland.
13 : Swiss Inst Bioinformat, Rue Michel Servet 1, CH-1211 Geneva, Switzerland.
14 : MIT, Comp Sci & Artificial Intelligence Lab, 32 Vassar St, Cambridge, MA 02139 USA.
15 : Broad Inst MIT & Harvard, 415 Main St, Cambridge, MA 02142 USA.
16 : Univ Barcelona, Dept Genet, Barcelona, Spain.
17 : Univ Barcelona, Inst Recerca Biodiversitat IRBio, Barcelona, Spain.
18 : China Agr Univ, Dept Entomol, Beijing, Peoples R China.
19 : Kansas State Univ, Div Biol, Manhattan, KS 66506 USA.
20 : Univ Tours, UMR CNRS 7261, Inst Rech Biol IInsecte, UFR Sci & Techn, Tours, France.
21 : CSIRO Land & Water, Clunies Ross St, Canberra, ACT 2601, Australia.
22 : Dept Zool, South Parks Rd, Oxford, England.
23 : Acad Athens, Biomed Res Fdn, Ctr Syst Biol, Athens, Greece.
24 : CSIRO Hlth & Biosecur, Clunies Ross St,Acton,2601, Acton, ACT, Australia.
25 : Univ Copenhagen, Ctr Funct & Comparat Insect Genom, Dept Biol, Univ Pk 15, DK-2100 Copenhagen, Denmark.
26 : Columbia Univ, Dept Biol, Barnard Coll, 3009 Broadway, New York, NY 10027 USA.
27 : Southwest Univ, Coll Plant Protect, Key Lab Entomol & Pest Control Engn, Chongqing 400715, Peoples R China.
28 : Dept Biol, Reed Coll, Portland, OR 97202 USA.
29 : Fraunhofer Inst Mol Biol & Appl Ecol IME, Bioresources Project Grp, Winchesterstr 2, D-35394 Giessen, Germany.
30 : Donghua Univ, Coll Chem Chem Engn & Biotechnol, Shanghai 201620, Peoples R China.
31 : Northwest A&F Univ, Coll Plant Protect, Yangling 712100, Shaanxi, Peoples R China.
32 : UT Southwestern Med Ctr, McDermott Ctr Human Growth & Dev, 5323 Harry Hines Blvd, Dallas, TX 75390 USA.
33 : Univ So Maine, Dept Biol Sci, Portland, ME 04104 USA.
34 : Univ Calif Irvine, Dept Ecol & Evolutionary Biol, Irvine, CA 92697 USA.
35 : Anhui Agr Univ, Sch Plant Protect, Hefei, Anhui, Peoples R China.
36 : Univ Rochester, Dept Biol, Rochester, NY 14627 USA.
37 : Northeastern Univ, Dept Marine & Environm Sci, Boston, MA 02115 USA.
38 : Cornell Univ, Dept Entomol, New York State Agr Expt Stn, Geneva, NY 14456 USA.
39 : Chinese Acad Sci, Inst Zool, State Key Lab Integrated Management Pest Insects, Beijing, Peoples R China.
40 : Med Univ Lubeck, Inst Biol, D-23538 Lubeck, Germany.
41 : Hamilton Coll, Neurosci Program, Clinton, NY 13323 USA.
42 : Univ Hamburg, Inst Zool, Hamburg, Germany.
43 : Univ Ghent, Fac Bioscience Engn, Dept Crop Protect, Ghent, Belgium.
44 : Univ Athens, Dept Cell Biol & Biophys, Fac Biol, Athens, Greece.
45 : Univ Wisconsin, Dept Entomol, Madison, WI USA.
46 : Hamilton Coll, Biol Dept & Neurosci Program, Clinton, NY 13323 USA.
47 : North Carolina State Univ, Dept Entomol, Raleigh, NC 27695 USA.
48 : Univ Siegen, Inst Biol Mol Biol, Sch Nat Sci & Engn, Adolf Reichwein Str 2,AR C3010, D-57076 Siegen, Germany.
49 : Oregon Hlth & Sci Univ, Sch Dent, Dept Integrat Biosciences, 3181 SW Sam Jackson Pk Rd,BRB421,L595, Portland, OR 97239 USA.
50 : Univ Cambridge, Dept Genet, Downing St, Cambridge CB2 3EH, England.
51 : Kansas State Univ, Dept Entomol, Manhattan, KS 66506 USA.
52 : Univ Massachusetts, Dept Biol, Amherst, MA 01003 USA.
53 : Northeastern Univ, Dept Biol, Boston, MA 02115 USA.
54 : Coll Charleston, Dept Biol, Charleston, SC 29424 USA.
55 : Justus Liebig Univ, Inst Insect Biotechnol, Heinrich Buff Ring 26-32, D-35392 Giessen, Germany.
56 : Univ South Carolina, Dept Biol Sci, Columbia, SC 29205 USA.
57 : Univ Missouri Kansas City, 5007 Rockhill Rd, Kansas City, MO 64110 USA.
58 : Rothamsted Res, Dept Biol Chem & Crop Protect, Harpenden AL5 2JQ, Herts, England.
Source Insect Biochemistry And Molecular Biology (0965-1748) (Pergamon-elsevier Science Ltd), 2016-09 , Vol. 76 , P. 118-147
DOI 10.1016/j.ibmb.2016.07.005
WOS© Times Cited 98
Keyword(s) Lepidoptera, Insect, Tobacco hornworm, Synteny, Moth, Insect biochemistry, Innate immunity
Abstract

Manduca sexta, known as the tobacco hornworm or Carolina sphinx moth, is a lepidopteran insect that is used extensively as a model system for research in insect biochemistry, physiology, neurobiology, development, and immunity. One important benefit of this species as an experimental model is its extremely large size, reaching more than 10 g in the larval stage. M. sexta larvae feed on solanaceous plants and thus must tolerate a substantial challenge from plant allelochemicals, including nicotine. We report the sequence and annotation of the M. sexta genome, and a survey of gene expression in various tissues and developmental stages. The Msex_1.0 genome assembly resulted in a total genome size of 419.4 Mbp. Repetitive sequences accounted for 25.8% of the assembled genome. The official gene set is comprised of 15,451 protein-coding genes, of which 2498 were manually curated. Extensive RNA-seq data from many tissues and developmental stages were used to improve gene models and for insights into gene expression patterns. Genome wide synteny analysis indicated a high level of macrosynteny in the Lepidoptera. Annotation and analyses were carried out for gene families involved in a wide spectrum of biological processes, including apoptosis, vacuole sorting, growth and development, structures of exoskeleton, egg shells, and muscle, vision, chemosensation, ion channels, signal transduction, neuropeptide signaling, neurotransmitter synthesis and transport, nicotine tolerance, lipid metabolism, and immunity. This genome sequence, annotation, and analysis provide an important new resource from a well-studied model insect species and will facilitate further biochemical and mechanistic experimental studies of many biological systems in insects.

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Kanost Michael R., Arrese Estela L., Cao Xiaolong, Chen Yun-Ru, Chellapilla Sanjay, Goldsmith Marian R., Grosse-Wilde Ewald, Heckel David G., Herndon Nicolae, Jiang Haobo, Papanicolaou Alexie, Qu Jiaxin, Soulages Jose L., Vogel Heiko, Walters James, Waterhouse Robert M., Ahn Seung-Joon, Almeida Francisca C., An Chunju, Aqrawi Peshtewani, Bretschneider Anne, Bryant William B., Bucks Sascha, Chao Hsu, Chevignon Germain, Christen Jayne M., Clarke David F., Dittmer Neal T., Ferguson Laura C. F., Garavelou Spyridoula, Gordon Karl H. J., Gunaratna Ramesh T., Han Yi, Hauser Frank, He Yan, Heidel-Fischer Hanna, Hirsh Ariana, Hu Yingxia, Jiang Hongbo, Kalra Divya, Klinner Christian, Konig Christopher, Kovar Christie, Kroll Ashley R., Kuwar Suyog S., Lee Sandy L., Lehman Rudiger, Li Kai, Li Zhaofei, Liang Hanquan, Lovelace Shanna, Lu Zhiqiang, Mansfield Jennifer H., McCulloch Kyle J., Mathew Tittu, Morton Brian, Muzny Donna M., McCulloch Kyle J., Mathew Tittu, Morton Brian, Muzny Donna M., Neunemann David, Ongeri Fiona, Pauchet Yannick, Pu Ling -Ling, Pyrousis Ioannis, Rao Xiang -Jun, Redding Amanda, Roesel Charles, Sanchez-Gracia Alejandro, Schaack Sarah, Shukla Aditi, Tetreau Guillaume, Wang Yang, Xiong Guang-Hua, Traut Walther, Walsh Tom K., Worley Kim C., Wu Di, Wu Wenbi, Wu Yuan-Qing, Zhang Xiufeng, Zou Zhen, Zucker Hannah, Briscoe Adriana D., Burmester Thorsten, Clem Rollie J., Feyereisen Rene, Grimmelikhuijzen Cornelis J. P., Hamodrakas Stavros J., Hansson Bill S., Huguet Elisabeth, Jermiin Lars S., Lan Que, Lehman Herman K., Lorenzen Marce, Merzendorfer Hans, Michalopoulos Ioannis, Morton David B., Muthukrishnan Subbaratnam, Oakeshott John G., Palmer Will, Park Yoonseong, Passarelli A. Lorena, Rozas Julio, Schwartz Lawrence M., Smith Wendy, Southgate Agnes, Vilcinskas Andreas, Vogt Richard, Wang Ping, Werren John, Yu Xiao-Qiang, Zhou Jing-Jiang, Brown Susan J., Scherer Steven E., Richards Stephen, Blissard Gary W. (2016). Multifaceted biological insights from a draft genome sequence of the tobacco hornworm moth, Manduca sexta. Insect Biochemistry And Molecular Biology, 76, 118-147. Publisher's official version : https://doi.org/10.1016/j.ibmb.2016.07.005 , Open Access version : https://archimer.ifremer.fr/doc/00635/74667/