The genome of Tetranychus urticae reveals herbivorous pest adaptations

Journal name:
Nature
Volume:
479,
Pages:
487–492
Date published:
DOI:
doi:10.1038/nature10640
Received
Accepted
Published online

Abstract

The spider mite Tetranychus urticae is a cosmopolitan agricultural pest with an extensive host plant range and an extreme record of pesticide resistance. Here we present the completely sequenced and annotated spider mite genome, representing the first complete chelicerate genome. At 90megabases T. urticae has the smallest sequenced arthropod genome. Compared with other arthropods, the spider mite genome shows unique changes in the hormonal environment and organization of the Hox complex, and also reveals evolutionary innovation of silk production. We find strong signatures of polyphagy and detoxification in gene families associated with feeding on different hosts and in new gene families acquired by lateral gene transfer. Deep transcriptome analysis of mites feeding on different plants shows how this pest responds to a changing host environment. The T. urticae genome thus offers new insights into arthropod evolution and plant–herbivore interactions, and provides unique opportunities for developing novel plant protection strategies.

At a glance

Figures

  1. Gene family history.
    Figure 1: Gene family history.

    At each time point (grey circles), the number of gains (+) and losses (−) of gene families is indicated as inferred by DOLLOP (black) and CAFÉ (red) programs. The inferred ancestral number of gene families, according to DOLLOP, is shown in green boxes.

  2. Gene expression changes when mites are shifted from P. vulgaris (bean) to A. thaliana or to S. lycopersicum (tomato).
    Figure 2: Gene expression changes when mites are shifted from P. vulgaris (bean) to A. thaliana or to S. lycopersicum (tomato).

    a, A phylogeny of the cytochrome P450 (CYP) genes and heat map of the response of CYP genes to host transfer. Two-thirds of the genes that are tandemly duplicated or that form clusters (indicated by black vertical lines) are co-regulated. b, Global changes in gene expression after host shift. c, Fold changes of important gene family members in digestion and detoxification are colour coded. The analysis of differential expression (b and c) is with a 5% false discovery rate as assessed with RNA-seq data collected in biological triplicate (fold changes between mean values are plotted).

  3. Maximum likelihood phylogeny of the fungal and arthropod carotenoid cyclase/synthase (CS) fusion proteins.
    Figure 3: Maximum likelihood phylogeny of the fungal and arthropod carotenoid cyclase/synthase (CS) fusion proteins.

    The out-group comprises chimaeric assemblies (CSchim) of the closest bacterial sequences of cyclases and synthases. The T. urticae and Acyrthosiphon pisum sequences form a monophyletic group closely related to the zygomycete sequences. Evidence for a single lateral gene transfer event is also shown by the common intron positions in the cyclase/synthase (orange) and desaturase (green) genes (upper right panel). Two clusters of carotenoid biosynthesis genes are found in T. urticae: a tail-to-tail arrangement on scaffold 1 as seen in zygomycetes and aphids, and a more complex head-to-head (re)arrangement on scaffold 11 (bottom right).

  4. Comparative organization of Hox clusters and expression pattern of the T. urticae engrailed gene.
    Figure 4: Comparative organization of Hox clusters and expression pattern of the T. urticae engrailed gene.

    a, T. urticae, T. castaneum and D. melanogaster Hox clusters. Gene sizes and intergenic distances are shown to scale. Dashed lines represent breaks in the cluster >1Mb. In T. urticae, fushi tarazu and Antennapedia are present in duplicate whereas abdominal-A and Hox3/zerknullt are missing (red asterisk). b, Variable pressure scanning electron microscopy (SEM) image of adult T. urticae with two main body regions indicated: P, prosoma; O, opisthosoma. c, T. urticae engrailed (en) expression pattern. en transcripts are detected in five prosomal stripes that correspond to future pedipalpal (Pp), four walking leg (L1–L4) and two opisthosomal (O1 and O2) segments. Scale bars: b, 0.125mm; c, 40 μm.

  5. T. urticae silk structure and dimensions.
    Figure 5: T. urticae silk structure and dimensions.

    a, Spider mite colony on a bean plant forming characteristic silk webbing. b, SEM image of the spider mite larval silk filament (top), and atomic force microscopy (AFM) image of two larval spider mite silk filaments (bottom). c, Height profile of the adult spider mite silk filament obtained from the AFM image. Scale bars: a, 0.75 cm; b, 1μm.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Gene Expression Omnibus

Sequence Read Archive

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Author information

  1. These authors contributed equally to this work.

    • Miodrag Grbić,
    • Thomas Van Leeuwen &
    • Richard M. Clark

Affiliations

  1. Department of Biology, The University of Western Ontario, London N6A 5B7, Canada

    • Miodrag Grbić,
    • Vojislava Grbić,
    • Marc Cazaux,
    • Marie Navarro,
    • Vladimir Zhurov,
    • Gustavo Acevedo &
    • Anica Bjelica
  2. Instituto de Ciencias de la Vid y el Vino (CSIC, UR, Gobiernode La Rioja), 26006 Logroño, Spain

    • Miodrag Grbić &
    • Vojislava Grbić
  3. Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium

    • Thomas Van Leeuwen,
    • Wannes Dermauw,
    • Guy Smagghe,
    • Masatoshi Iga,
    • Olivier Christiaens &
    • Luc Tirry
  4. Department of Biology, University of Utah, Salt Lake City, Utah 84112, USA

    • Richard M. Clark &
    • Edward J. Osborne
  5. Department of Plant Systems Biology, VIB, Technologiepark 927, B-9052 Ghent, Belgium

    • Stephane Rombauts,
    • Pierre Rouzé,
    • Phuong Cao Thi Ngoc,
    • Jeffrey A. Fawcett,
    • Eric Bonnet,
    • Cindy Martens,
    • Guy Baele &
    • Yves Van de Peer
  6. Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, B-9052 Ghent, Belgium

    • Stephane Rombauts,
    • Pierre Rouzé,
    • Phuong Cao Thi Ngoc,
    • Jeffrey A. Fawcett,
    • Eric Bonnet,
    • Cindy Martens,
    • Guy Baele &
    • Yves Van de Peer
  7. Department of Environmental Biology, Centro de Investigaciones Biológicas, CSIC, 28040 Madrid, Spain

    • Félix Ortego &
    • Pedro Hernández-Crespo
  8. Centro de Biotecnología y Genómica de Plantas,UPM-INIA, 28223 Madrid, Spain

    • Isabel Diaz &
    • Manuel Martinez
  9. INRA, UMR CBGP (INRA/IRD/Cirad/Montpellier SupAgro), Campus international de Baillarguet, 34988 Montferrier-sur-Lez, France

    • Maria Navajas
  10. Instituto Gulbenkian de Ciência, 2781-901 Oeiras, Portugal

    • Élio Sucena
  11. Universidade de Lisboa, Faculdade de Ciências, Departamento de Biologia Animal, 1749-016 Lisbon, Portugal

    • Élio Sucena
  12. Universidade de Lisboa, Faculdade de Ciências, Centro de Biologia Ambiental, 1749-016 Lisbon, Portugal

    • Sara Magalhães
  13. Department of Molecular and Cellular Biology, University of Arizona, Tucson, Arizona 85721, USA

    • Lisa Nagy &
    • Ryan M. Pace
  14. Johns Hopkins University School of Medicine, Department of Molecular Biology & Genetics, Baltimore, Maryland 21205, USA

    • Sergej Djuranović
  15. Institut de Neurosciences Cognitives et Intégratives d’Aquitaine Université de Bordeaux 1, 33405 Talence, France

    • Jan A. Veenstra
  16. Centro Interdisciplinario de Neurociencia de Valparaíso, Facultad de Ciencias, Universidad de Valparaíso, Valparaíso 2360102, Chile

    • John Ewer &
    • Rodrigo Mancilla Villalobos
  17. Department of Physics and Astronomy, The University of Western Ontario, N6A 5B7 London, Canada

    • Jeffrey L. Hutter &
    • Stephen D. Hudson
  18. Instituto de Catálisis y Petroleoquímica CSIC, Madrid, Spain; IMDEA Nanociencias, Facultad de Ciencias, Universidad Autonoma de Madrid, 28050 Madrid, Spain

    • Marisela Velez
  19. School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332, USA

    • Soojin V. Yi &
    • Jia Zeng
  20. Department of Biology, University of Texas at Arlington, Arlington, Texas 76019, USA

    • Andre Pires-daSilva
  21. Universite de Toulouse, UPS, Centre de Biologie du Developpement, Universite Paul Sabatier, 31062 Toulouse, France; Centre National de la Recherche Scientifique, UMR5547, Centre de Biologie du Developpement, 31062 Toulouse, France

    • Fernando Roch
  22. Westfälische Wilhelms University, Institute for Evolution and Biodiversity, Evolutionary Bioinformatics Group, Hüfferstrasse 1, D-48149 Münster, Germany

    • Lothar Wissler
  23. CMPG, Department of Microbial and Molecular Systems, K.U. Leuven, B-3001 Leuven, Belgium

    • Aminael Sanchez-Rodriguez
  24. UPMC Univ Paris 06, UMR CNRS 7622, Equipe Biogenèse des signaux hormonaux, Case 29, 75005 Paris, France

    • Catherine Blais
  25. Research Group EnVOC, Department of Sustainable Organic Chemistry and Technology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium

    • Kristof Demeestere
  26. Max Planck Institute for Developmental Biology, D-72076 Tübingen, Germany

    • Stefan R. Henz
  27. Department of Integrative Biology, University of Guelph, N1G 2W1 Guelph, Canada

    • T. Ryan Gregory
  28. Boyce Thompson Institute for Plant Research, Ithaca, New York 14853, USA

    • Johannes Mathieu
  29. Southern Crop Protection and Food Research Centre, Agriculture and Agri-Food Canada, N5V 4T3 London, Canada

    • Lou Verdon
  30. Fasteris SA, CH-1228 Plan-les-Ouates, Switzerland

    • Laurent Farinelli
  31. HudsonAlpha Institute for Biotechnology Huntsville, Alabama 35806, USA

    • Jeremy Schmutz
  32. DOE Joint Genome Institute, Walnut Creek, California 94598, USA

    • Jeremy Schmutz &
    • Erika Lindquist
  33. UMR 1301, INRA, CNRS and Université de Nice Sophia Antipolis, 06903 Sophia Antipolis, France

    • René Feyereisen
  34. Present addresses: Institut Curie, 26 rue d’Ulm, Paris 75248, France; INSERM, U900, Paris 75248, France ; Mines ParisTech, Fontainebleau 77300, France (E.B.); Graduate University for Advanced Studies, Hayama, Kanagawa 240-0193, Japan (J.A.F.).

    • Jeffrey A. Fawcett &
    • Eric Bonnet

Contributions

M.G. wrote the genome sequencing proposal. M.G. and V.G. generated DNA and RNA for sequencing. M.G., T.V.L., R.M.C., V.G., R.F. and Y.V.d.P. coordinated genome analysis and manuscript preparation. J.S. and E.L. coordinated genome assembly whereas P.R. and S.R. centralized and enabled the annotation process. All other authors are members of the spider mite genome sequencing consortium and contributed annotation, analyses or data to the genome project. M.G., T.V.L. and R.M.C. should be considered joint first authors. S.R., P.R. and V.G. should be considered joint second authors. M.G., R.F. and Y.V.d.P. should be considered joint corresponding authors.

Competing financial interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to:

Individual scaffolds of the T. urticae (London) genome are available through GenBank under accession numbers HE587301 to HE587940. The Illumina data for T. urticae strain Montpellier can be found in the Sequence Read Archive (SRA) database under accession numbers SRX030911 to SRX030913. RNA-seq data is available under Gene Expression Omnibus (GEO) super series number GSE32342.

Author details

Supplementary information

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    The file contains Supplementary Text, Supplementary Tables 1-12, Supplementary Figures 1-12 with legends and additional references (see Contents list for more details).

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