Genome streamlining in a minute herbivore that manipulates its host plant

  1. Robert Greenhalgh
  2. Wannes Dermauw  Is a corresponding author
  3. Joris J Glas
  4. Stephane Rombauts
  5. Nicky Wybouw
  6. Jainy Thomas
  7. Juan M Alba
  8. Ellen J Pritham
  9. Saioa Legarrea
  10. René Feyereisen
  11. Yves Van de Peer
  12. Thomas Van Leeuwen
  13. Richard M Clark  Is a corresponding author
  14. Merijn R Kant  Is a corresponding author
  1. University of Utah, United States
  2. Ghent University, Belgium
  3. University of Amsterdam, Netherlands
  4. University of Utah School of Medicine, United States
  5. University of Copenhagen, Denmark

Abstract

The tomato russet mite, Aculops lycopersici, is among the smallest animals on earth. It is a worldwide pest on tomato and can potently suppress the host's natural resistance. We sequenced its genome, the first of an eriophyoid, and explored whether there are genomic features associated with the mite's minute size and lifestyle. At only 32.5 Mb, the genome is the smallest yet reported for any arthropod and, reminiscent of microbial eukaryotes, exceptionally streamlined. It has few transposable elements, tiny intergenic regions, and is remarkably intron-poor, as more than 80% of coding genes are intronless. Furthermore, in accordance with ecological specialization theory, this defense-suppressing herbivore has extremely reduced environmental response gene families such as those involved in chemoreception and detoxification. Other losses associate with this species' highly derived body plan. Our findings accelerate the understanding of evolutionary forces underpinning metazoan life at the limits of small physical and genome size.

Data availability

The genomic and 454 transcriptomic datasets generated by this project are available under BioProject accessions PRJNA588358 and PRJNA588365, respectively; the Illumina transcriptome data are available under BioProject accession PRJNA588358. This Whole Genome Shotgun project has been deposited at DDBJ/ENA/GenBank under the accession WNKI00000000. The version described in this paper is version WNKI01000000. Additional datasets are hosted by the Online Resource for Community Annotation of Eukaryotes (ORCAE) at https://bioinformatics.psb.ugent.be/orcae/, where the annotation can be viewed and de novo transcriptomes (Illumina and 454) can be downloaded.

The following data sets were generated

Article and author information

Author details

  1. Robert Greenhalgh

    School of Biological Sciences, University of Utah, Salt Lake City, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2816-3154
  2. Wannes Dermauw

    Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
    For correspondence
    wannes.dermauw@ugent.be
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4612-8969
  3. Joris J Glas

    Evolutionary and Population Biology, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    No competing interests declared.
  4. Stephane Rombauts

    Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium
    Competing interests
    No competing interests declared.
  5. Nicky Wybouw

    Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
    Competing interests
    No competing interests declared.
  6. Jainy Thomas

    Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, United States
    Competing interests
    No competing interests declared.
  7. Juan M Alba

    Evolutionary and Population Biology, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4822-9827
  8. Ellen J Pritham

    Human Genetics, University of Utah, Salt Lake City, United States
    Competing interests
    No competing interests declared.
  9. Saioa Legarrea

    Evolutionary and Population Biology, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9127-2794
  10. René Feyereisen

    University of Copenhagen, Copenhagen, Denmark
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9560-571X
  11. Yves Van de Peer

    Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4327-3730
  12. Thomas Van Leeuwen

    Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    No competing interests declared.
  13. Richard M Clark

    Department of Biology, University of Utah, Salt Lake City, United States
    For correspondence
    clark@biology.utah.edu
    Competing interests
    No competing interests declared.
  14. Merijn R Kant

    Evolutionary and Population Biology, University of Amsterdam, Amsterdam, Netherlands
    For correspondence
    M.Kant@uva.nl
    Competing interests
    Merijn R Kant, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2524-8195

Funding

Netherlands Organization for Scientific Research (STW-VIDI/13492,STW-GAP/13550)

  • Merijn R Kant

USA National Science Foundation (1457346)

  • Richard M Clark

European Union Horizon 2020 research and innovation program (772026-POLYADAPT)

  • Thomas Van Leeuwen

Research Foundation Flanders (1274917N)

  • Wannes Dermauw

National Institutes of Health (T32GM007464)

  • Robert Greenhalgh

Research Foundation Flanders (12T9818N)

  • Nicky Wybouw

European Union Horizon 2020 research and innovation program (773902-SuperPests)

  • Thomas Van Leeuwen

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Detlef Weigel, Max Planck Institute for Developmental Biology, Germany

Version history

  1. Received: June 4, 2020
  2. Accepted: October 22, 2020
  3. Accepted Manuscript published: October 23, 2020 (version 1)
  4. Version of Record published: December 15, 2020 (version 2)

Copyright

© 2020, Greenhalgh et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Robert Greenhalgh
  2. Wannes Dermauw
  3. Joris J Glas
  4. Stephane Rombauts
  5. Nicky Wybouw
  6. Jainy Thomas
  7. Juan M Alba
  8. Ellen J Pritham
  9. Saioa Legarrea
  10. René Feyereisen
  11. Yves Van de Peer
  12. Thomas Van Leeuwen
  13. Richard M Clark
  14. Merijn R Kant
(2020)
Genome streamlining in a minute herbivore that manipulates its host plant
eLife 9:e56689.
https://doi.org/10.7554/eLife.56689

Share this article

https://doi.org/10.7554/eLife.56689

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