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
Further reading
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- Evolutionary Biology
Lineages of rod-shaped bacteria such as Escherichia coli exhibit a temporal decline in elongation rate in a manner comparable to cellular or biological aging. The effect results from the production of asymmetrical daughters, one with a lower elongation rate, by the division of a mother cell. The slower daughter compared to the faster daughter, denoted respectively as the old and new daughters, has more aggregates of damaged proteins and fewer expressed gene products. We have examined further the degree of asymmetry by measuring the density of ribosomes between old and new daughters and between their poles. We found that ribosomes were denser in the new daughter and also in the new pole of the daughters. These ribosome patterns match the ones we previously found for expressed gene products. This outcome suggests that the asymmetry is not likely to result from properties unique to the gene expressed in our previous study, but rather from a more fundamental upstream process affecting the distribution of ribosomal abundance. Because damage aggregates and ribosomes are both more abundant at the poles of E. coli cells, we suggest that competition for space between the two could explain the reduced ribosomal density in old daughters. Using published values for aggregate sizes and the relationship between ribosomal number and elongation rates, we show that the aggregate volumes could in principle displace quantitatively the amount of ribosomes needed to reduce the elongation rate of the old daughters.
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- Evolutionary Biology
- Genetics and Genomics
Evolutionary arms races can arise at the contact surfaces between host and viral proteins, producing dynamic spaces in which genetic variants are continually pursued. However, the sampling of genetic variation must be balanced with the need to maintain protein function. A striking case is given by protein kinase R (PKR), a member of the mammalian innate immune system. PKR detects viral replication within the host cell and halts protein synthesis to prevent viral replication by phosphorylating eIF2α, a component of the translation initiation machinery. PKR is targeted by many viral antagonists, including poxvirus pseudosubstrate antagonists that mimic the natural substrate, eIF2α, and inhibit PKR activity. Remarkably, PKR has several rapidly evolving residues at this interface, suggesting it is engaging in an evolutionary arms race, despite the surface’s critical role in phosphorylating eIF2α. To systematically explore the evolutionary opportunities available at this dynamic interface, we generated and characterized a library of 426 SNP-accessible nonsynonymous variants of human PKR for their ability to escape inhibition by the model pseudosubstrate inhibitor K3, encoded by the vaccinia virus gene K3L. We identified key sites in the PKR kinase domain that harbor K3-resistant variants, as well as critical sites where variation leads to loss of function. We find K3-resistant variants are readily available throughout the interface and are enriched at sites under positive selection. Moreover, variants beneficial against K3 were also beneficial against an enhanced variant of K3, indicating resilience to viral adaptation. Overall, we find that the eIF2α-binding surface of PKR is highly malleable, potentiating its evolutionary ability to combat viral inhibition.
