Genome streamlining in a minute herbivore that manipulates its host plant
- University of Utah, United States
- Ghent University, Belgium
- University of Amsterdam, Netherlands
- University of Utah School of Medicine, United States
- 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.
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Aculops lycopersici Transcriptome or gene expressionNCBI Bioproject, PRJNA588365.
Article and author information
Author details
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.
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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Genome streamlining in a minute herbivore that manipulates its host plant
eLife 9:e56689.
https://doi.org/10.7554/eLife.56689
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Gene duplication drives evolution by providing raw material for proteins with novel functions. An influential hypothesis by Ohno (1970) posits that gene duplication helps genes tolerate new mutations and thus facilitates the evolution of new phenotypes. Competing hypotheses argue that deleterious mutations will usually inactivate gene duplicates too rapidly for Ohno’s hypothesis to work. We experimentally tested Ohno’s hypothesis by evolving one or exactly two copies of a gene encoding a fluorescent protein in Escherichia coli through several rounds of mutation and selection. We analyzed the genotypic and phenotypic evolutionary dynamics of the evolving populations through high-throughput DNA sequencing, biochemical assays, and engineering of selected variants. In support of Ohno’s hypothesis, populations carrying two gene copies displayed higher mutational robustness than those carrying a single gene copy. Consequently, the double-copy populations experienced relaxed purifying selection, evolved higher phenotypic and genetic diversity, carried more mutations and accumulated combinations of key beneficial mutations earlier. However, their phenotypic evolution was not accelerated, possibly because one gene copy rapidly became inactivated by deleterious mutations. Our work provides an experimental platform to test models of evolution by gene duplication, and it supports alternatives to Ohno’s hypothesis that point to the importance of gene dosage.
