BMC Biology (Oct 2020)
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. Bejerman,
- Christopher 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
Affiliations
- Dorith Rotenberg
- Department of Entomology and Plant Pathology, North Carolina State University
- Aaron A. Baumann
- Virology Section, College of Veterinary Medicine, University of Tennessee
- Sulley Ben-Mahmoud
- Department of Entomology and Nematology, University of California Davis
- Olivier Christiaens
- Laboratory of Agrozoology, Department of Plants and Crops, Ghent University
- Wannes Dermauw
- Laboratory of Agrozoology, Department of Plants and Crops, Ghent University
- Panagiotis Ioannidis
- Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas
- Chris G. C. Jacobs
- Institute of Biology, Leiden University
- Iris M. Vargas Jentzsch
- Institute for Zoology: Developmental Biology, University of Cologne
- Jonathan E. Oliver
- Department of Plant Pathology, University of Georgia - Tifton Campus
- Monica F. Poelchau
- National Agricultural Library, USDA-ARS
- Swapna Priya Rajarapu
- Department of Entomology and Plant Pathology, North Carolina State University
- Derek J. Schneweis
- Department of Plant Pathology, Kansas State University
- Simon Snoeck
- Laboratory of Agrozoology, Department of Plants and Crops, Ghent University
- Clauvis N. T. Taning
- Laboratory of Agrozoology, Department of Plants and Crops, Ghent University
- Dong Wei
- Laboratory of Agrozoology, Department of Plants and Crops, Ghent University
- Shirani M. K. Widana Gamage
- Department of Botany, University of Ruhuna
- Daniel S. T. Hughes
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Shwetha C. Murali
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Samuel T. Bailey
- Department of Biological Sciences, University of Cincinnati
- Nicolas E. Bejerman
- IPAVE-CIAP-INTA
- Christopher J. Holmes
- Department of Biological Sciences, University of Cincinnati
- Emily C. Jennings
- Department of Biological Sciences, University of Cincinnati
- Andrew J. Rosendale
- Department of Biological Sciences, University of Cincinnati
- Andrew Rosselot
- Department of Biological Sciences, University of Cincinnati
- Kaylee Hervey
- Department of Plant Pathology, Kansas State University
- Brandi A. Schneweis
- Department of Plant Pathology, Kansas State University
- Sammy Cheng
- Department of Biology, University of Rochester
- Christopher Childers
- National Agricultural Library, USDA-ARS
- Felipe A. Simão
- Department of Genetic Medicine and Development, University of Geneva Medical School, and Swiss Institute of Bioinformatics
- Ralf G. Dietzgen
- Queensland Alliance for Agriculture and Food Innovation, The University of Queensland
- Hsu Chao
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Huyen Dinh
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Harsha Vardhan Doddapaneni
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Shannon Dugan
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Yi Han
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Sandra L. Lee
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Donna M. Muzny
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Jiaxin Qu
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Kim C. Worley
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Joshua B. Benoit
- Department of Biological Sciences, University of Cincinnati
- Markus Friedrich
- Department of Biological Sciences, Wayne State University
- Jeffery W. Jones
- Department of Biological Sciences, Wayne State University
- Kristen A. Panfilio
- Institute for Zoology: Developmental Biology, University of Cologne
- Yoonseong Park
- Department of Entomology, Kansas State University
- Hugh M. Robertson
- Department of Entomology, University of Illinois at Urbana-Champaign
- Guy Smagghe
- Laboratory of Agrozoology, Department of Plants and Crops, Ghent University
- Diane E. Ullman
- Department of Entomology and Nematology, University of California Davis
- Maurijn van der Zee
- Institute of Biology, Leiden University
- Thomas Van Leeuwen
- Laboratory of Agrozoology, Department of Plants and Crops, Ghent University
- Jan A. Veenstra
- INCIA UMR 5287 CNRS, University of Bordeaux
- Robert M. Waterhouse
- Department of Ecology and Evolution, Swiss Institute of Bioinformatics, University of Lausanne
- Matthew T. Weirauch
- Center for Autoimmune Genomics and Etiology, Divisions of Biomedical Informatics and Developmental Biology, Cincinnati Children’s Hospital Medical Center
- John H. Werren
- Department of Biology, University of Rochester
- Anna E. Whitfield
- Department of Entomology and Plant Pathology, North Carolina State University
- Evgeny M. Zdobnov
- Department of Genetic Medicine and Development, University of Geneva Medical School, and Swiss Institute of Bioinformatics
- Richard A. Gibbs
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Stephen Richards
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- DOI
- https://doi.org/10.1186/s12915-020-00862-9
- Journal volume & issue
-
Vol. 18,
no. 1
pp. 1 – 37
Abstract
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.
Keywords
- Thysanoptera
- Western flower thrips
- Hemipteroid assemblage
- Insect genomics
- Tospovirus
- Salivary glands
