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

Michael R Kanost; Estela L Arrese; Xiaolong Cao; Yun-Ru Chen; Sanjay Chellapilla; Marian R Goldsmith; Ewald Grosse-Wilde; David G Heckel; Nicolae Herndon; Haobo Jiang; Alexie Papanicolaou; Jiaxin Qu; Jose L Soulages; Heiko Vogel; James Walters; Robert M Waterhouse; Seung-Joon Ahn; Francisca C Almeida; Chunju An; Peshtewani Aqrawi; Anne Bretschneider; William B Bryant; Sascha Bucks; Hsu Chao; Germain Chevignon; Jayne M Christen; David F Clarke; Neal T Dittmer; Laura C F Ferguson; Spyridoula Garavelou; Karl H J Gordon; Ramesh T Gunaratna; Yi Han; Frank Hauser; Yan He; Hanna Heidel-Fischer; Ariana Hirsh; Yingxia Hu; Hongbo Jiang; Divya Kalra; Christian Klinner; Christopher König; Christie Kovar; Ashley R Kroll; Suyog S Kuwar; Sandy L Lee; Rüdiger Lehman; Kai Li; Zhaofei Li; Hanquan Liang; Shanna Lovelace; Zhiqiang Lu; Jennifer H Mansfield; Kyle J McCulloch; Tittu Mathew; Brian Morton; Donna M Muzny; David Neunemann; Fiona Ongeri; Yannick Pauchet; Ling-Ling Pu; Ioannis Pyrousis; Xiang-Jun Rao; Amanda Redding; Charles Roesel; Alejandro Sanchez-Gracia; Sarah Schaack; Aditi Shukla; Guillaume Tetreau; Yang Wang; Guang-Hua Xiong; Walther Traut; Tom K Walsh; Kim C Worley; Di Wu; Wenbi Wu; Yuan-Qing Wu; Xiufeng Zhang; Zhen Zou; Hannah Zucker; Adriana D Briscoe; Thorsten Burmester; Rollie J Clem; René Feyereisen; Cornelis Grimmelikhuijzen; Stavros J Hamodrakas; Bill S Hansson; Elisabeth Huguet; Lars S Jermiin; Que Lan; Herman K Lehman; Marce Lorenzen; Hans Merzendorfer; Ioannis Michalopoulos; David B Morton; Subbaratnam Muthukrishnan; John G Oakeshott; Will Palmer; Yoonseong Park; A Lorena Passarelli; Julio Rozas; Lawrence M Schwartz; Wendy Smith; Agnes Southgate; Andreas Vilcinskas; Richard Vogt; Ping Wang; John Werren; Xiao-Qiang Yu; Jing-Jiang Zhou; Susan J Brown; Steven E Scherer; Stephen Richards; Gary W Blissard

doi:10.1016/j.ibmb.2016.07.005

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

Michael R Kanost, Estela L Arrese, Xiaolong Cao, Yun-Ru Chen, Sanjay Chellapilla, Marian R Goldsmith, Ewald Grosse-Wilde, David G Heckel, Nicolae Herndon, Haobo Jiang, Alexie Papanicolaou, Jiaxin Qu, Jose L Soulages, Heiko Vogel, James Walters, Robert M Waterhouse, Seung-Joon Ahn, Francisca C Almeida, Chunju An, Peshtewani AqrawiAnne Bretschneider, William B Bryant, Sascha Bucks, Hsu Chao, Germain Chevignon, Jayne M Christen, David F Clarke, Neal T Dittmer, Laura C F Ferguson, Spyridoula Garavelou, Karl H J Gordon, Ramesh T Gunaratna, Yi Han, Frank Hauser, Yan He, Hanna Heidel-Fischer, Ariana Hirsh, Yingxia Hu, Hongbo Jiang, Divya Kalra, Christian Klinner, Christopher König, Christie Kovar, Ashley R Kroll, Suyog S Kuwar, Sandy L Lee, Rüdiger Lehman, Kai Li, Zhaofei Li, Hanquan Liang, Shanna Lovelace, Zhiqiang Lu, Jennifer H Mansfield, Kyle J McCulloch, Tittu Mathew, Brian Morton, Donna M Muzny, David Neunemann, Fiona Ongeri, Yannick Pauchet, Ling-Ling Pu, Ioannis Pyrousis, Xiang-Jun Rao, Amanda Redding, Charles Roesel, Alejandro Sanchez-Gracia, Sarah Schaack, Aditi Shukla, Guillaume Tetreau, Yang Wang, Guang-Hua Xiong, Walther Traut, Tom K Walsh, Kim C Worley, Di Wu, Wenbi Wu, Yuan-Qing Wu, Xiufeng Zhang, Zhen Zou, Hannah Zucker, Adriana D Briscoe, Thorsten Burmester, Rollie J Clem, René Feyereisen, Cornelis Grimmelikhuijzen, Stavros J Hamodrakas, Bill S Hansson, Elisabeth Huguet, Lars S Jermiin, Que Lan, Herman K Lehman, Marce Lorenzen, Hans Merzendorfer, Ioannis Michalopoulos, David B Morton, Subbaratnam Muthukrishnan, John G Oakeshott, Will Palmer, Yoonseong Park, A Lorena Passarelli, Julio Rozas, Lawrence M Schwartz, Wendy Smith, Agnes Southgate, Andreas Vilcinskas, Richard Vogt, Ping Wang, John Werren, Xiao-Qiang Yu, Jing-Jiang Zhou, Susan J Brown, Steven E Scherer, Stephen Richards, Gary W Blissard

Cell and Neurobiology

94 Citations (Scopus)

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.

Original language	English
Journal	Insect Biochemistry and Molecular Biology
Volume	76
Pages (from-to)	118-147
Number of pages	30
ISSN	0965-1748
DOIs	https://doi.org/10.1016/j.ibmb.2016.07.005
Publication status	Published - 1 Sept 2016

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Journal Article

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10.1016/j.ibmb.2016.07.005

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Kanost, M. R., Arrese, E. L., Cao, X., Chen, Y-R., Chellapilla, S., Goldsmith, M. R., Grosse-Wilde, E., Heckel, D. G., Herndon, N., Jiang, H., Papanicolaou, A., Qu, J., Soulages, J. L., Vogel, H., Walters, J., Waterhouse, R. M., Ahn, S-J., Almeida, F. C., An, C., ... Blissard, G. 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. https://doi.org/10.1016/j.ibmb.2016.07.005

Kanost, MR, Arrese, EL, Cao, X, Chen, Y-R, Chellapilla, S, Goldsmith, MR, Grosse-Wilde, E, Heckel, DG, Herndon, N, Jiang, H, Papanicolaou, A, Qu, J, Soulages, JL, Vogel, H, Walters, J, Waterhouse, RM, Ahn, S-J, Almeida, FC, An, C, Aqrawi, P, Bretschneider, A, Bryant, WB, Bucks, S, Chao, H, Chevignon, G, Christen, JM, Clarke, DF, Dittmer, NT, Ferguson, LCF, Garavelou, S, Gordon, KHJ, Gunaratna, RT, Han, Y, Hauser, F, He, Y, Heidel-Fischer, H, Hirsh, A, Hu, Y, Jiang, H, Kalra, D, Klinner, C, König, C, Kovar, C, Kroll, AR, Kuwar, SS, Lee, SL, Lehman, R, Li, K, Li, Z, Liang, H, Lovelace, S, Lu, Z, Mansfield, JH, McCulloch, KJ, Mathew, T, Morton, B, Muzny, DM, Neunemann, D, Ongeri, F, Pauchet, Y, Pu, L-L, Pyrousis, I, Rao, X-J, Redding, A, Roesel, C, Sanchez-Gracia, A, Schaack, S, Shukla, A, Tetreau, G, Wang, Y, Xiong, G-H, Traut, W, Walsh, TK, Worley, KC, Wu, D, Wu, W, Wu, Y-Q, Zhang, X, Zou, Z, Zucker, H, Briscoe, AD, Burmester, T, Clem, RJ, Feyereisen, R, Grimmelikhuijzen, C, Hamodrakas, SJ, Hansson, BS, Huguet, E, Jermiin, LS, Lan, Q, Lehman, HK, Lorenzen, M, Merzendorfer, H, Michalopoulos, I, Morton, DB, Muthukrishnan, S, Oakeshott, JG, Palmer, W, Park, Y, Passarelli, AL, Rozas, J, Schwartz, LM, Smith, W, Southgate, A, Vilcinskas, A, Vogt, R, Wang, P, Werren, J, Yu, X-Q, Zhou, J-J, Brown, SJ, Scherer, SE, Richards, S & Blissard, GW 2016, 'Multifaceted biological insights from a draft genome sequence of the tobacco hornworm moth, Manduca sexta', Insect Biochemistry and Molecular Biology, vol. 76, pp. 118-147. https://doi.org/10.1016/j.ibmb.2016.07.005

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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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doi = "10.1016/j.ibmb.2016.07.005",

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T1 - Multifaceted biological insights from a draft genome sequence of the tobacco hornworm moth, Manduca sexta

AU - Kanost, Michael R

AU - Arrese, Estela L

AU - Cao, Xiaolong

AU - Chen, Yun-Ru

AU - Chellapilla, Sanjay

AU - Goldsmith, Marian R

AU - Grosse-Wilde, Ewald

AU - Heckel, David G

AU - Herndon, Nicolae

AU - Jiang, Haobo

AU - Papanicolaou, Alexie

AU - Qu, Jiaxin

AU - Soulages, Jose L

AU - Vogel, Heiko

AU - Walters, James

AU - Waterhouse, Robert M

AU - Ahn, Seung-Joon

AU - Almeida, Francisca C

AU - An, Chunju

AU - Aqrawi, Peshtewani

AU - Bretschneider, Anne

AU - Bryant, William B

AU - Bucks, Sascha

AU - Chao, Hsu

AU - Chevignon, Germain

AU - Christen, Jayne M

AU - Clarke, David F

AU - Dittmer, Neal T

AU - Ferguson, Laura C F

AU - Garavelou, Spyridoula

AU - Gordon, Karl H J

AU - Gunaratna, Ramesh T

AU - Han, Yi

AU - Hauser, Frank

AU - He, Yan

AU - Heidel-Fischer, Hanna

AU - Hirsh, Ariana

AU - Hu, Yingxia

AU - Jiang, Hongbo

AU - Kalra, Divya

AU - Klinner, Christian

AU - König, Christopher

AU - Kovar, Christie

AU - Kroll, Ashley R

AU - Kuwar, Suyog S

AU - Lee, Sandy L

AU - Lehman, Rüdiger

AU - Li, Kai

AU - Li, Zhaofei

AU - Liang, Hanquan

AU - Lovelace, Shanna

AU - Lu, Zhiqiang

AU - Mansfield, Jennifer H

AU - McCulloch, Kyle J

AU - Mathew, Tittu

AU - Morton, Brian

AU - Muzny, Donna M

AU - Neunemann, David

AU - Ongeri, Fiona

AU - Pauchet, Yannick

AU - Pu, Ling-Ling

AU - Pyrousis, Ioannis

AU - Rao, Xiang-Jun

AU - Redding, Amanda

AU - Roesel, Charles

AU - Sanchez-Gracia, Alejandro

AU - Schaack, Sarah

AU - Shukla, Aditi

AU - Tetreau, Guillaume

AU - Wang, Yang

AU - Xiong, Guang-Hua

AU - Traut, Walther

AU - Walsh, Tom K

AU - Worley, Kim C

AU - Wu, Di

AU - Wu, Wenbi

AU - Wu, Yuan-Qing

AU - Zhang, Xiufeng

AU - Zou, Zhen

AU - Zucker, Hannah

AU - Briscoe, Adriana D

AU - Burmester, Thorsten

AU - Clem, Rollie J

AU - Feyereisen, René

AU - Grimmelikhuijzen, Cornelis

AU - Hamodrakas, Stavros J

AU - Hansson, Bill S

AU - Huguet, Elisabeth

AU - Jermiin, Lars S

AU - Lan, Que

AU - Lehman, Herman K

AU - Lorenzen, Marce

AU - Merzendorfer, Hans

AU - Michalopoulos, Ioannis

AU - Morton, David B

AU - Muthukrishnan, Subbaratnam

AU - Oakeshott, John G

AU - Palmer, Will

AU - Park, Yoonseong

AU - Passarelli, A Lorena

AU - Rozas, Julio

AU - Schwartz, Lawrence M

AU - Smith, Wendy

AU - Southgate, Agnes

AU - Vilcinskas, Andreas

AU - Vogt, Richard

AU - Wang, Ping

AU - Werren, John

AU - Yu, Xiao-Qiang

AU - Zhou, Jing-Jiang

AU - Brown, Susan J

AU - Scherer, Steven E

AU - Richards, Stephen

AU - Blissard, Gary W

PY - 2016/9/1

Y1 - 2016/9/1

N2 - 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.

AB - 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.

KW - Journal Article

U2 - 10.1016/j.ibmb.2016.07.005

DO - 10.1016/j.ibmb.2016.07.005

M3 - Journal article

C2 - 27522922

SN - 0965-1748

VL - 76

SP - 118

EP - 147

JO - Insect Biochemistry and Molecular Biology

JF - Insect Biochemistry and Molecular Biology

ER -

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

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