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Genome-enabled insights into the biology of thrips as crop pests

BACKGROUND: The western flower thrips, Frankliniella occidentalis (Pergande), is a globally invasive pest and plant virus vector on a wide array of food, fiber, and ornamental crops. The underlying genetic mechanisms of the processes governing thrips pest and vector biology, feeding behaviors, ecolo...

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Autores principales: Rotenberg, Dorith, Baumann, Aaron A., Ben-Mahmoud, Sulley, Christiaens, Olivier, Dermauw, Wannes, Ioannidis, Panagiotis, Jacobs, Chris G. C., Vargas Jentzsch, Iris M., Oliver, Jonathan E., Poelchau, Monica F., Rajarapu, Swapna Priya, Schneweis, Derek J., Snoeck, Simon, Taning, Clauvis N. T., Wei, Dong, Widana Gamage, Shirani M. K., Hughes, Daniel S. T., Murali, Shwetha C., Bailey, Samuel T., Bejerman, Nicolas E., Holmes, Christopher J., Jennings, Emily C., Rosendale, Andrew J., Rosselot, Andrew, Hervey, Kaylee, Schneweis, Brandi A., Cheng, Sammy, Childers, Christopher, Simão, Felipe A., Dietzgen, Ralf G., Chao, Hsu, Dinh, Huyen, Doddapaneni, Harsha Vardhan, Dugan, Shannon, Han, Yi, Lee, Sandra L., Muzny, Donna M., Qu, Jiaxin, Worley, Kim C., Benoit, Joshua B., Friedrich, Markus, Jones, Jeffery W., Panfilio, Kristen A., Park, Yoonseong, Robertson, Hugh M., Smagghe, Guy, Ullman, Diane E., van der Zee, Maurijn, Van Leeuwen, Thomas, Veenstra, Jan A., Waterhouse, Robert M., Weirauch, Matthew T., Werren, John H., Whitfield, Anna E., Zdobnov, Evgeny M., Gibbs, Richard A., Richards, Stephen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7570057/
https://www.ncbi.nlm.nih.gov/pubmed/33070780
http://dx.doi.org/10.1186/s12915-020-00862-9
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author Rotenberg, Dorith
Baumann, Aaron A.
Ben-Mahmoud, Sulley
Christiaens, Olivier
Dermauw, Wannes
Ioannidis, Panagiotis
Jacobs, Chris G. C.
Vargas Jentzsch, Iris M.
Oliver, Jonathan E.
Poelchau, Monica F.
Rajarapu, Swapna Priya
Schneweis, Derek J.
Snoeck, Simon
Taning, Clauvis N. T.
Wei, Dong
Widana Gamage, Shirani M. K.
Hughes, Daniel S. T.
Murali, Shwetha C.
Bailey, Samuel T.
Bejerman, Nicolas E.
Holmes, Christopher J.
Jennings, Emily C.
Rosendale, Andrew J.
Rosselot, Andrew
Hervey, Kaylee
Schneweis, Brandi A.
Cheng, Sammy
Childers, Christopher
Simão, Felipe A.
Dietzgen, Ralf G.
Chao, Hsu
Dinh, Huyen
Doddapaneni, Harsha Vardhan
Dugan, Shannon
Han, Yi
Lee, Sandra L.
Muzny, Donna M.
Qu, Jiaxin
Worley, Kim C.
Benoit, Joshua B.
Friedrich, Markus
Jones, Jeffery W.
Panfilio, Kristen A.
Park, Yoonseong
Robertson, Hugh M.
Smagghe, Guy
Ullman, Diane E.
van der Zee, Maurijn
Van Leeuwen, Thomas
Veenstra, Jan A.
Waterhouse, Robert M.
Weirauch, Matthew T.
Werren, John H.
Whitfield, Anna E.
Zdobnov, Evgeny M.
Gibbs, Richard A.
Richards, Stephen
author_facet Rotenberg, Dorith
Baumann, Aaron A.
Ben-Mahmoud, Sulley
Christiaens, Olivier
Dermauw, Wannes
Ioannidis, Panagiotis
Jacobs, Chris G. C.
Vargas Jentzsch, Iris M.
Oliver, Jonathan E.
Poelchau, Monica F.
Rajarapu, Swapna Priya
Schneweis, Derek J.
Snoeck, Simon
Taning, Clauvis N. T.
Wei, Dong
Widana Gamage, Shirani M. K.
Hughes, Daniel S. T.
Murali, Shwetha C.
Bailey, Samuel T.
Bejerman, Nicolas E.
Holmes, Christopher J.
Jennings, Emily C.
Rosendale, Andrew J.
Rosselot, Andrew
Hervey, Kaylee
Schneweis, Brandi A.
Cheng, Sammy
Childers, Christopher
Simão, Felipe A.
Dietzgen, Ralf G.
Chao, Hsu
Dinh, Huyen
Doddapaneni, Harsha Vardhan
Dugan, Shannon
Han, Yi
Lee, Sandra L.
Muzny, Donna M.
Qu, Jiaxin
Worley, Kim C.
Benoit, Joshua B.
Friedrich, Markus
Jones, Jeffery W.
Panfilio, Kristen A.
Park, Yoonseong
Robertson, Hugh M.
Smagghe, Guy
Ullman, Diane E.
van der Zee, Maurijn
Van Leeuwen, Thomas
Veenstra, Jan A.
Waterhouse, Robert M.
Weirauch, Matthew T.
Werren, John H.
Whitfield, Anna E.
Zdobnov, Evgeny M.
Gibbs, Richard A.
Richards, Stephen
author_sort Rotenberg, Dorith
collection PubMed
description BACKGROUND: The western flower thrips, Frankliniella occidentalis (Pergande), is a globally invasive pest and plant virus vector on a wide array of food, fiber, and ornamental crops. The underlying genetic mechanisms of the processes governing thrips pest and vector biology, feeding behaviors, ecology, and insecticide resistance are largely unknown. To address this gap, we present the F. occidentalis draft genome assembly and official gene set. RESULTS: We report on the first genome sequence for any member of the insect order Thysanoptera. Benchmarking Universal Single-Copy Ortholog (BUSCO) assessments of the genome assembly (size = 415.8 Mb, scaffold N50 = 948.9 kb) revealed a relatively complete and well-annotated assembly in comparison to other insect genomes. The genome is unusually GC-rich (50%) compared to other insect genomes to date. The official gene set (OGS v1.0) contains 16,859 genes, of which ~ 10% were manually verified and corrected by our consortium. We focused on manual annotation, phylogenetic, and expression evidence analyses for gene sets centered on primary themes in the life histories and activities of plant-colonizing insects. Highlights include the following: (1) divergent clades and large expansions in genes associated with environmental sensing (chemosensory receptors) and detoxification (CYP4, CYP6, and CCE enzymes) of substances encountered in agricultural environments; (2) a comprehensive set of salivary gland genes supported by enriched expression; (3) apparent absence of members of the IMD innate immune defense pathway; and (4) developmental- and sex-specific expression analyses of genes associated with progression from larvae to adulthood through neometaboly, a distinct form of maturation differing from either incomplete or complete metamorphosis in the Insecta. CONCLUSIONS: Analysis of the F. occidentalis genome offers insights into the polyphagous behavior of this insect pest that finds, colonizes, and survives on a widely diverse array of plants. The genomic resources presented here enable a more complete analysis of insect evolution and biology, providing a missing taxon for contemporary insect genomics-based analyses. Our study also offers a genomic benchmark for molecular and evolutionary investigations of other Thysanoptera species.
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spelling pubmed-75700572020-10-20 Genome-enabled insights into the biology of thrips as crop pests Rotenberg, Dorith Baumann, Aaron A. Ben-Mahmoud, Sulley Christiaens, Olivier Dermauw, Wannes Ioannidis, Panagiotis Jacobs, Chris G. C. Vargas Jentzsch, Iris M. Oliver, Jonathan E. Poelchau, Monica F. Rajarapu, Swapna Priya Schneweis, Derek J. Snoeck, Simon Taning, Clauvis N. T. Wei, Dong Widana Gamage, Shirani M. K. Hughes, Daniel S. T. Murali, Shwetha C. Bailey, Samuel T. Bejerman, Nicolas E. Holmes, Christopher J. Jennings, Emily C. Rosendale, Andrew J. Rosselot, Andrew Hervey, Kaylee Schneweis, Brandi A. Cheng, Sammy Childers, Christopher Simão, Felipe A. Dietzgen, Ralf G. Chao, Hsu Dinh, Huyen Doddapaneni, Harsha Vardhan Dugan, Shannon Han, Yi Lee, Sandra L. Muzny, Donna M. Qu, Jiaxin Worley, Kim C. Benoit, Joshua B. Friedrich, Markus Jones, Jeffery W. Panfilio, Kristen A. Park, Yoonseong Robertson, Hugh M. Smagghe, Guy Ullman, Diane E. van der Zee, Maurijn Van Leeuwen, Thomas Veenstra, Jan A. Waterhouse, Robert M. Weirauch, Matthew T. Werren, John H. Whitfield, Anna E. Zdobnov, Evgeny M. Gibbs, Richard A. Richards, Stephen BMC Biol Research Article BACKGROUND: The western flower thrips, Frankliniella occidentalis (Pergande), is a globally invasive pest and plant virus vector on a wide array of food, fiber, and ornamental crops. The underlying genetic mechanisms of the processes governing thrips pest and vector biology, feeding behaviors, ecology, and insecticide resistance are largely unknown. To address this gap, we present the F. occidentalis draft genome assembly and official gene set. RESULTS: We report on the first genome sequence for any member of the insect order Thysanoptera. Benchmarking Universal Single-Copy Ortholog (BUSCO) assessments of the genome assembly (size = 415.8 Mb, scaffold N50 = 948.9 kb) revealed a relatively complete and well-annotated assembly in comparison to other insect genomes. The genome is unusually GC-rich (50%) compared to other insect genomes to date. The official gene set (OGS v1.0) contains 16,859 genes, of which ~ 10% were manually verified and corrected by our consortium. We focused on manual annotation, phylogenetic, and expression evidence analyses for gene sets centered on primary themes in the life histories and activities of plant-colonizing insects. Highlights include the following: (1) divergent clades and large expansions in genes associated with environmental sensing (chemosensory receptors) and detoxification (CYP4, CYP6, and CCE enzymes) of substances encountered in agricultural environments; (2) a comprehensive set of salivary gland genes supported by enriched expression; (3) apparent absence of members of the IMD innate immune defense pathway; and (4) developmental- and sex-specific expression analyses of genes associated with progression from larvae to adulthood through neometaboly, a distinct form of maturation differing from either incomplete or complete metamorphosis in the Insecta. CONCLUSIONS: Analysis of the F. occidentalis genome offers insights into the polyphagous behavior of this insect pest that finds, colonizes, and survives on a widely diverse array of plants. The genomic resources presented here enable a more complete analysis of insect evolution and biology, providing a missing taxon for contemporary insect genomics-based analyses. Our study also offers a genomic benchmark for molecular and evolutionary investigations of other Thysanoptera species. BioMed Central 2020-10-19 /pmc/articles/PMC7570057/ /pubmed/33070780 http://dx.doi.org/10.1186/s12915-020-00862-9 Text en © The Author(s) 2020 Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Rotenberg, Dorith
Baumann, Aaron A.
Ben-Mahmoud, Sulley
Christiaens, Olivier
Dermauw, Wannes
Ioannidis, Panagiotis
Jacobs, Chris G. C.
Vargas Jentzsch, Iris M.
Oliver, Jonathan E.
Poelchau, Monica F.
Rajarapu, Swapna Priya
Schneweis, Derek J.
Snoeck, Simon
Taning, Clauvis N. T.
Wei, Dong
Widana Gamage, Shirani M. K.
Hughes, Daniel S. T.
Murali, Shwetha C.
Bailey, Samuel T.
Bejerman, Nicolas E.
Holmes, Christopher J.
Jennings, Emily C.
Rosendale, Andrew J.
Rosselot, Andrew
Hervey, Kaylee
Schneweis, Brandi A.
Cheng, Sammy
Childers, Christopher
Simão, Felipe A.
Dietzgen, Ralf G.
Chao, Hsu
Dinh, Huyen
Doddapaneni, Harsha Vardhan
Dugan, Shannon
Han, Yi
Lee, Sandra L.
Muzny, Donna M.
Qu, Jiaxin
Worley, Kim C.
Benoit, Joshua B.
Friedrich, Markus
Jones, Jeffery W.
Panfilio, Kristen A.
Park, Yoonseong
Robertson, Hugh M.
Smagghe, Guy
Ullman, Diane E.
van der Zee, Maurijn
Van Leeuwen, Thomas
Veenstra, Jan A.
Waterhouse, Robert M.
Weirauch, Matthew T.
Werren, John H.
Whitfield, Anna E.
Zdobnov, Evgeny M.
Gibbs, Richard A.
Richards, Stephen
Genome-enabled insights into the biology of thrips as crop pests
title Genome-enabled insights into the biology of thrips as crop pests
title_full Genome-enabled insights into the biology of thrips as crop pests
title_fullStr Genome-enabled insights into the biology of thrips as crop pests
title_full_unstemmed Genome-enabled insights into the biology of thrips as crop pests
title_short Genome-enabled insights into the biology of thrips as crop pests
title_sort genome-enabled insights into the biology of thrips as crop pests
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7570057/
https://www.ncbi.nlm.nih.gov/pubmed/33070780
http://dx.doi.org/10.1186/s12915-020-00862-9
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