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Genome-enabled insights into the biology of thrips as crop pests.
BMC Biol. 2020 10 19; 18(1):142.BB

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.

Links

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Authors+Show Affiliations

Rotenberg D
Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, 27695, USA. drotenb@ncsu.edu.
Baumann AA
Virology Section, College of Veterinary Medicine, University of Tennessee, A239 VTH, 2407 River Drive, Knoxville, TN, 37996, USA.
Ben-Mahmoud S
Department of Entomology and Nematology, University of California Davis, Davis, CA, 95616, USA.
Christiaens O
Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Coupure Links 653, 9000, Ghent, Belgium.
Dermauw W
Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Coupure Links 653, 9000, Ghent, Belgium.
Ioannidis P
Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, Vassilika Vouton, 70013, Heraklion, Greece. Department of Genetic Medicine and Development, University of Geneva Medical School, and Swiss Institute of Bioinformatics, Geneva, Switzerland.
Jacobs CGC
Institute of Biology, Leiden University, 2333 BE, Leiden, The Netherlands.
Vargas Jentzsch IM
Institute for Zoology: Developmental Biology, University of Cologne, 50674, Cologne, Germany.
Oliver JE
Department of Plant Pathology, University of Georgia - Tifton Campus, Tifton, GA, 31793-5737, USA.
Poelchau MF
National Agricultural Library, USDA-ARS, Beltsville, MD, 20705, USA.
Rajarapu SP
Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, 27695, USA.
Schneweis DJ
Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA.
Snoeck S
Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Coupure Links 653, 9000, Ghent, Belgium. Department of Biology, University of Washington, Seattle, WA, 98105, USA.
Taning CNT
Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Coupure Links 653, 9000, Ghent, Belgium.
Wei D
Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Coupure Links 653, 9000, Ghent, Belgium. Chongqing Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing, China. International Joint Laboratory of China-Belgium on Sustainable Crop Pest Control, Academy of Agricultural Sciences, Southwest University, Chongqing, China and Ghent University, Ghent, Belgium.
Widana Gamage SMK
Department of Botany, University of Ruhuna, Matara, Sri Lanka.
Hughes DST
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Murali SC
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Bailey ST
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.
Bejerman NE
IPAVE-CIAP-INTA, 5020, Cordoba, Argentina.
Holmes CJ
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.
Jennings EC
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.
Rosendale AJ
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA. Department of Biology, Mount St. Joseph University, Cincinnati, OH, 45233, USA.
Rosselot A
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.
Hervey K
Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA.
Schneweis BA
Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA.
Cheng S
Department of Biology, University of Rochester, Rochester, NY, 14627, USA.
Childers C
National Agricultural Library, USDA-ARS, Beltsville, MD, 20705, USA.
Simão FA
Department of Genetic Medicine and Development, University of Geneva Medical School, and Swiss Institute of Bioinformatics, Geneva, Switzerland.
Dietzgen RG
Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St. Lucia, QLD, 4072, Australia.
Chao H
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Dinh H
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Doddapaneni HV
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Dugan S
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Han Y
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Lee SL
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Muzny DM
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Qu J
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Worley KC
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Benoit JB
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.
Friedrich M
Department of Biological Sciences, Wayne State University, Detroit, MI, 48202, USA.
Jones JW
Department of Biological Sciences, Wayne State University, Detroit, MI, 48202, USA.
Panfilio KA
Institute for Zoology: Developmental Biology, University of Cologne, 50674, Cologne, Germany. School of Life Sciences, University of Warwick, Gibbet Hill Campus, Coventry, CV4 7AL, UK.
Park Y
Department of Entomology, Kansas State University, Manhattan, KS, 66506, USA.
Robertson HM
Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA.
Smagghe G
Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Coupure Links 653, 9000, Ghent, Belgium. Chongqing Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing, China. International Joint Laboratory of China-Belgium on Sustainable Crop Pest Control, Academy of Agricultural Sciences, Southwest University, Chongqing, China and Ghent University, Ghent, Belgium.
Ullman DE
Department of Entomology and Nematology, University of California Davis, Davis, CA, 95616, USA.
van der Zee M
Institute of Biology, Leiden University, 2333 BE, Leiden, The Netherlands.
Van Leeuwen T
Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Coupure Links 653, 9000, Ghent, Belgium.
Veenstra JA
INCIA UMR 5287 CNRS, University of Bordeaux, Pessac, France.
Waterhouse RM
Department of Ecology and Evolution, Swiss Institute of Bioinformatics, University of Lausanne, 1015, Lausanne, Switzerland.
Weirauch MT
Center for Autoimmune Genomics and Etiology, Divisions of Biomedical Informatics and Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, 45229, USA. Department of Pediatrics, University of Cincinnati, College of Medicine, Cincinnati, OH, 45229, USA.
Werren JH
Department of Biology, University of Rochester, Rochester, NY, 14627, USA.
Whitfield AE
Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, 27695, USA.
Zdobnov EM
Department of Genetic Medicine and Development, University of Geneva Medical School, and Swiss Institute of Bioinformatics, Geneva, Switzerland.
Gibbs RA
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Richards S
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

MeSH

AnimalsCrops, AgriculturalFeeding BehaviorFood ChainGenome, InsectImmunity, InnateLife History TraitsPerceptionPhylogenyReproductionThysanopteraTranscriptome

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

33070780

Citation

Rotenberg, Dorith, et al. "Genome-enabled Insights Into the Biology of Thrips as Crop Pests." BMC Biology, vol. 18, no. 1, 2020, p. 142.
Rotenberg D, Baumann AA, Ben-Mahmoud S, et al. Genome-enabled insights into the biology of thrips as crop pests. BMC Biol. 2020;18(1):142.
Rotenberg, D., Baumann, A. A., Ben-Mahmoud, S., Christiaens, O., Dermauw, W., Ioannidis, P., Jacobs, C. G. C., Vargas Jentzsch, I. M., Oliver, J. E., Poelchau, M. F., Rajarapu, S. P., Schneweis, D. J., Snoeck, S., Taning, C. N. T., Wei, D., Widana Gamage, S. M. K., Hughes, D. S. T., Murali, S. C., Bailey, S. T., ... Richards, S. (2020). Genome-enabled insights into the biology of thrips as crop pests. BMC Biology, 18(1), 142. https://doi.org/10.1186/s12915-020-00862-9
Rotenberg D, et al. Genome-enabled Insights Into the Biology of Thrips as Crop Pests. BMC Biol. 2020 10 19;18(1):142. PubMed PMID: 33070780.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Genome-enabled insights into the biology of thrips as crop pests. AU - Rotenberg,Dorith, AU - Baumann,Aaron A, AU - Ben-Mahmoud,Sulley, AU - Christiaens,Olivier, AU - Dermauw,Wannes, AU - Ioannidis,Panagiotis, AU - Jacobs,Chris G C, AU - Vargas Jentzsch,Iris M, AU - Oliver,Jonathan E, AU - Poelchau,Monica F, AU - Rajarapu,Swapna Priya, AU - Schneweis,Derek J, AU - Snoeck,Simon, AU - Taning,Clauvis N T, AU - Wei,Dong, AU - Widana Gamage,Shirani M K, AU - Hughes,Daniel S T, AU - Murali,Shwetha C, AU - Bailey,Samuel T, AU - Bejerman,Nicolas E, AU - Holmes,Christopher J, AU - Jennings,Emily C, AU - Rosendale,Andrew J, AU - Rosselot,Andrew, AU - Hervey,Kaylee, AU - Schneweis,Brandi A, AU - Cheng,Sammy, AU - Childers,Christopher, AU - Simão,Felipe A, AU - Dietzgen,Ralf G, AU - Chao,Hsu, AU - Dinh,Huyen, AU - Doddapaneni,Harsha Vardhan, AU - Dugan,Shannon, AU - Han,Yi, AU - Lee,Sandra L, AU - Muzny,Donna M, AU - Qu,Jiaxin, AU - Worley,Kim C, AU - Benoit,Joshua B, AU - Friedrich,Markus, AU - Jones,Jeffery W, AU - Panfilio,Kristen A, AU - Park,Yoonseong, AU - Robertson,Hugh M, AU - Smagghe,Guy, AU - Ullman,Diane E, AU - van der Zee,Maurijn, AU - Van Leeuwen,Thomas, AU - Veenstra,Jan A, AU - Waterhouse,Robert M, AU - Weirauch,Matthew T, AU - Werren,John H, AU - Whitfield,Anna E, AU - Zdobnov,Evgeny M, AU - Gibbs,Richard A, AU - Richards,Stephen, Y1 - 2020/10/19/ PY - 2020/02/18/received PY - 2020/09/02/accepted PY - 2020/10/19/entrez PY - 2020/10/20/pubmed PY - 2021/7/10/medline KW - Chemosensory receptors KW - Detoxification KW - Hemipteroid assemblage KW - Innate immunity KW - Insect genomics KW - Opsins KW - Salivary glands KW - Thysanoptera KW - Tospovirus KW - Western flower thrips SP - 142 EP - 142 JF - BMC biology JO - BMC Biol VL - 18 IS - 1 N2 - 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. SN - 1741-7007 UR - https://www.unboundmedicine.com/medline/citation/33070780/Genome_enabled_insights_into_the_biology_of_thrips_as_crop_pests_ DB - PRIME DP - Unbound Medicine ER -