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3. Retrotransposon-mediated variation of a chitin synthase gene confers insect resistance toBacillus thuringiensisVip3Aa toxin

Author

Liu, Zhenxing, primary, Liao, Chongyu, additional, Zou, Luming, additional, Jin, Minghui, additional, Shan, Yinxue, additional, Quan, Yudong, additional, Yao, Hui, additional, Zhang, Lei, additional, Wang, Peng, additional, Liu, Zhuangzhuang, additional, Wang, Na, additional, Li, Anjing, additional, Liu, Kaiyu, additional, Heckel, David G., additional, Wu, Kongming, additional, and Xiao, Yutao, additional

Published
2024
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4. Retrotransposon-mediated disruption of a chitin synthase gene confers insect resistance to Bacillus thuringiensis Vip3Aa toxin.

Author

Liu, Zhenxing, Liao, Chongyu, Zou, Luming, Jin, Minghui, Shan, Yinxue, Quan, Yudong, Yao, Hui, Zhang, Lei, Wang, Peng, Liu, Zhuangzhuang, Wang, Na, Li, Anjing, Liu, Kaiyu, Tabashnik, Bruce E., Heckel, David G., Wu, Kongming, and Xiao, Yutao

Abstract

The vegetative insecticidal protein Vip3Aa from Bacillus thuringiensis (Bt) has been produced by transgenic crops to counter pest resistance to the widely used crystalline (Cry) insecticidal proteins from Bt. To proactively manage pest resistance, there is an urgent need to better understand the genetic basis of resistance to Vip3Aa, which has been largely unknown. We discovered that retrotransposon-mediated alternative splicing of a midgut-specific chitin synthase gene was associated with 5,560-fold resistance to Vip3Aa in a laboratory-selected strain of the fall armyworm, a globally important crop pest. The same mutation in this gene was also detected in a field population. Knockout of this gene via CRISPR/Cas9 caused high levels of resistance to Vip3Aa in fall armyworm and 2 other lepidopteran pests. The insights provided by these results could help to advance monitoring and management of pest resistance to Vip3Aa. The insecticidal protein Vip3Aa is used in genetically engineered crops to overcome pest resistance to other insecticidal transgenes. This study shows that insertion of a transposable element into a gut-specific chitin synthase gene causes Vip3Aa resistance in field-collected individuals of the lepidopteran pest Spodoptera frugiperda (fall armyworm). [ABSTRACT FROM AUTHOR]

Published
2024
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6. Multifaceted biological insights from a draft genome sequence of the tobacco hornworm moth, Manduca sexta

Author

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 CF, Garavelou, Spyridoula, Gordon, Karl HJ, Gunaratna, Ramesh T, Han, Yi, Hauser, Frank, He, Yan, Heidel-Fischer, Hanna, Hirsh, Ariana, Hu, Yingxia, Jiang, Hongbo, Kalra, Divya, Klinner, Christian, König, Christopher, Kovar, Christie, Kroll, Ashley R, Kuwar, Suyog S, Lee, Sandy L, Lehman, Rüdiger, Li, Kai, Li, Zhaofei, Liang, Hanquan, Lovelace, Shanna, Lu, Zhiqiang, Mansfield, Jennifer H, 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, René, Grimmelikhuijzen, Cornelis JP, 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, and Passarelli, A Lorena

Subjects
Biological Sciences, Bioinformatics and Computational Biology, Genetics, Tobacco, 1.1 Normal biological development and functioning, Underpinning research, Generic health relevance, Animals, Gene Expression, Gene Expression Profiling, Genome, Insect, Larva, Manduca, Pupa, Sequence Analysis, DNA, Synteny, Lepidoptera, Insect, Tobacco hornworm, Moth, Insect biochemistry, Innate immunity, Medicinal and Biomolecular Chemistry, Biochemistry and Cell Biology, Zoology, Entomology, Biochemistry and cell biology
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.

Published
2016

11. Escalation by duplication: Milkweed bug trumps Monarch butterfly.

Author

Beran, Franziska and Heckel, David G.

Subjects
*MONARCH butterfly, *CARDIAC glycosides, *MILKWEEDS, *PLANT toxins, *CARDENOLIDES, *BACTERIAL toxins
Abstract

The iconic Monarch butterfly is probably the best‐known example of chemical defence against predation, as pictures of vomiting naive blue jays in countless textbooks vividly illustrate. Larvae of the butterfly take up toxic cardiac glycosides from their milkweed hostplants and carry them over to the adult stage. These compounds (cardiotonic steroids, including cardenolides and bufadienolides) inhibit the animal transmembrane sodium‐potassium ATPase (Na,K‐ATPase), but the Monarch enzyme resists this inhibition thanks to amino acid substitutions in its catalytic alpha‐subunit. Some birds also have substitutions and can feast on cardiac glycoside‐sequestering insects with impunity. A flurry of recent work has shown how the alpha‐subunit gene has been duplicated multiple times in separate insect lineages specializing in cardiac glycoside‐producing plants. In this issue of Molecular Ecology, Herbertz et al. toss the beta‐subunit into the mix, by expressing all nine combinations of three alpha‐ and three beta‐subunits of the milkweed bug Na,K‐ATPase and testing their response to a cardenolide from the hostplant. The findings suggest that the diversification and subfunctionalization of genes allow milkweed bugs to balance trade‐offs between resistance towards sequestered host plant toxins that protect the bugs from predators, and physiological costs in terms of Na,K‐ATPase activity. [ABSTRACT FROM AUTHOR]

Published
2024
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14. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species

Author

Dasmahapatra, Kanchon K, Walters, James R, Briscoe, Adriana D, Davey, John W, Whibley, Annabel, Nadeau, Nicola J, Zimin, Aleksey V, Hughes, Daniel ST, Ferguson, Laura C, Martin, Simon H, Salazar, Camilo, Lewis, James J, Adler, Sebastian, Ahn, Seung-Joon, Baker, Dean A, Baxter, Simon W, Chamberlain, Nicola L, Chauhan, Ritika, Counterman, Brian A, Dalmay, Tamas, Gilbert, Lawrence E, Gordon, Karl, Heckel, David G, Hines, Heather M, Hoff, Katharina J, Holland, Peter WH, Jacquin-Joly, Emmanuelle, Jiggins, Francis M, Jones, Robert T, Kapan, Durrell D, Kersey, Paul, Lamas, Gerardo, Lawson, Daniel, Mapleson, Daniel, Maroja, Luana S, Martin, Arnaud, Moxon, Simon, Palmer, William J, Papa, Riccardo, Papanicolaou, Alexie, Pauchet, Yannick, Ray, David A, Rosser, Neil, Salzberg, Steven L, Supple, Megan A, Surridge, Alison, Tenger-Trolander, Ayse, Vogel, Heiko, Wilkinson, Paul A, Wilson, Derek, Yorke, James A, Yuan, Furong, Balmuth, Alexi L, Eland, Cathlene, Gharbi, Karim, Thomson, Marian, Gibbs, Richard A, Han, Yi, Jayaseelan, Joy C, Kovar, Christie, Mathew, Tittu, Muzny, Donna M, Ongeri, Fiona, Pu, Ling-Ling, Qu, Jiaxin, Thornton, Rebecca L, Worley, Kim C, Wu, Yuan-Qing, Linares, Mauricio, Blaxter, Mark L, Ffrench-Constant, Richard H, Joron, Mathieu, Kronforst, Marcus R, Mullen, Sean P, Reed, Robert D, Scherer, Steven E, Richards, Stephen, Mallet, James, McMillan, W Owen, and Jiggins, Chris D

Subjects
Adaptation, Physiological, Animals, Bombyx, Butterflies, Chromosomes, Insect, Evolution, Molecular, Gene Flow, Genes, Homeobox, Genes, Insect, Genome, Insect, Genomics, Hybridization, Genetic, Molecular Mimicry, Molecular Sequence Data, Phylogeny, Pigmentation, Sequence Analysis, DNA, Species Specificity, Synteny, Wings, Animal, Heliconius Genome Consortium, General Science & Technology
Abstract

The evolutionary importance of hybridization and introgression has long been debated. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12,669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.

Published
2012

21. Downregulation of a transcription factor associated with resistance to Bt toxin Vip3Aa in the invasive fall armyworm.

Author

Minghui Jin, Yinxue Shan, Yan Peng, Wenhui Wang, Huihui Zhang, Kaiyu Liu, Heckel, David G., Kongming Wu, Tabashnik, Bruce E., and Yutao Xiao

Subjects
FALL armyworm, TRANSCRIPTION factors, GENE expression, RNA interference, GENOME-wide association studies, NATURAL products
Abstract

Transgenic crops producing insecticidal proteins from Bacillus thuringiensis (Bt) have revolutionized control of some major pests. However, more than 25 cases of field-evolved practical resistance have reduced the efficacy of transgenic crops producing crystalline (Cry) Bt proteins, spurring adoption of alternatives including crops producing the Bt vegetative insecticidal protein Vip3Aa. Although practical resistance to Vip3Aa has not been reported yet, better understanding of the genetic basis of resistance to Vip3Aa is urgently needed to proactively monitor, delay, and counter pest resistance. This is especially important for fall armyworm (Spodoptera frugiperda), which has evolved practical resistance to Cry proteins and is one of the world's most damaging pests. Here, we report the identification of an association between downregulation of the transcription factor gene SfMyb and resistance to Vip3Aa in S. frugiperda. Results from a genome-wide association study, fine-scale mapping, and RNA-Seq identified this gene as a compelling candidate for contributing to the 206-fold resistance to Vip3Aa in a laboratory-selected strain. Experimental reduction of SfMyb expression in a susceptible strain using RNA interference (RNAi) or CRISPR/Cas9 gene editing decreased susceptibility to Vip3Aa, confirming that reduced expression of this gene can cause resistance to Vip3Aa. Relative to the wild-type promoter for SfMyb, the promoter in the resistant strain has deletions and lower activity. Data from yeast one-hybrid assays, genomics, RNA-Seq, RNAi, and proteomics identified genes that are strong candidates for mediating the effects of SfMyb on Vip3Aa resistance. The results reported here may facilitate progress in understanding and managing pest resistance to Vip3Aa. [ABSTRACT FROM AUTHOR]

Published
2023
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30. Towards evolutionary predictions: Current promises and challenges

Author

Wortel, Meike T., primary, Agashe, Deepa, additional, Bailey, Susan F., additional, Bank, Claudia, additional, Bisschop, Karen, additional, Blankers, Thomas, additional, Cairns, Johannes, additional, Colizzi, Enrico Sandro, additional, Cusseddu, Davide, additional, Desai, Michael M., additional, van Dijk, Bram, additional, Egas, Martijn, additional, Ellers, Jacintha, additional, Groot, Astrid T., additional, Heckel, David G., additional, Johnson, Marcelle L., additional, Kraaijeveld, Ken, additional, Krug, Joachim, additional, Laan, Liedewij, additional, Lässig, Michael, additional, Lind, Peter A., additional, Meijer, Jeroen, additional, Noble, Luke M., additional, Okasha, Samir, additional, Rainey, Paul B., additional, Rozen, Daniel E., additional, Shitut, Shraddha, additional, Tans, Sander J., additional, Tenaillon, Olivier, additional, Teotónio, Henrique, additional, de Visser, J. Arjan G. M., additional, Visser, Marcel E., additional, Vroomans, Renske M. A., additional, Werner, Gijsbert D. A., additional, Wertheim, Bregje, additional, and Pennings, Pleuni S., additional

Published
2022
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35. The butterfly plant arms-race escalated by gene and genome duplications

Author

Edger, Patrick P., Heidel-Fischer, Hanna M., Bekaert, Michaël, Rota, Jadranka, Glöckner, Gernot, Platts, Adrian E., Heckel, David G., Der, Joshua P., Wafula, Eric K., Tang, Michelle, Hofberger, Johannes A., Smithson, Ann, Hall, Jocelyn C., Blanchette, Matthieu, Bureau, Thomas E., Wright, Stephen I., dePamphilis, Claude W., Schranz, M. Eric, Barker, Michael S., Conant, Gavin C., Wahlberg, Niklas, Vogel, Heiko, Pires, J. Chris, and Wheat, Christopher W.

Published
2015

41. Comparative genomics of the mimicry switch in Papilio dardanus

Author

Timmermans, Martijn J. T. N., Baxter, Simon W., Clark, Rebecca, Heckel, David G., Vogel, Heiko, Collins, Steve, Papanicolaou, Alexie, Fukova, Iva, Joron, Mathieu, Thompson, Martin J., Jiggins, Chris D., ffrench-Constant, Richard H., and Vogler, Alfried P.

Published
2014

44. Phenalenone-type phytoalexins mediate resistance of banana plants (Musa spp.) to the burrowing nematode Radopholus similis

Author

Hölscher, Dirk, Dhakshinamoorthy, Suganthagunthalam, Alexandrov, Theodore, Becker, Michael, Bretschneider, Tom, Buerkert, Andreas, Crecelius, Anna C., Waele, Dirk De, Elsen, Annemie, Heckel, David G., Heklau, Heike, Hertweck, Christian, Kai, Marco, Knop, Katrin, Krafft, Christoph, Maddula, Ravi K., Matthäus, Christian, Popp, Jürgen, Schneider, Bernd, Schubert, Ulrich S., Sikora, Richard A., Svatoš, Aleš, and Swennen, Rony L.

Published
2014

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