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

Dorith Rotenberg, Aaron A. Baumann, Sulley Ben-Mahmoud, Olivier Christiaens, Wannes Dermauw, Panagiotis Ioannidis, Chris G.C. Jacobs, Iris M. Vargas Jentzsch, Jonathan E. Oliver, Monica F. Poelchau, Swapna Priya Rajarapu, Derek J. Schneweis, Simon Snoeck, Clauvis N.T. Taning, Dong Wei, Shirani M.K. Widana Gamage, Daniel S.T. Hughes, Shwetha C. Murali, Samuel T. Bailey, Nicolas E. BejermanChristopher J. Holmes, Emily C. Jennings, Andrew J. Rosendale, Andrew Rosselot, Kaylee Hervey, Brandi A. Schneweis, Sammy Cheng, Christopher Childers, Felipe A. Simão, Ralf G. Dietzgen, Hsu Chao, Huyen Dinh, Harsha Vardhan Doddapaneni, Shannon Dugan, Yi Han, Sandra L. Lee, Donna M. Muzny, Jiaxin Qu, Kim C. Worley, Joshua B. Benoit, Markus Friedrich, Jeffery W. Jones, Kristen A. Panfilio, Yoonseong Park, Hugh M. Robertson, Guy Smagghe, Diane E. Ullman, Maurijn van der Zee, Thomas Van Leeuwen, Jan A. Veenstra, Robert M. Waterhouse, Matthew T. Weirauch, John H. Werren, Anna E. Whitfield, Evgeny M. Zdobnov, Richard A. Gibbs, Stephen Richards

Research output: Contribution to journalArticlepeer-review

Abstract

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.

Original languageEnglish (US)
Article number142
JournalBMC biology
Volume18
Issue number1
DOIs
StatePublished - Dec 1 2020

Keywords

  • Chemosensory receptors
  • Detoxification
  • Hemipteroid assemblage
  • Innate immunity
  • Insect genomics
  • Opsins
  • Salivary glands
  • Thysanoptera
  • Tospovirus
  • Western flower thrips

ASJC Scopus subject areas

  • Biotechnology
  • Structural Biology
  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • Plant Science
  • Developmental Biology
  • Cell Biology

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