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
The majority of highly polymorphic genes are related to immune functions and with over 100 alleles within a population, genes of the major histocompatibility complex (MHC) are the most polymorphic loci in vertebrates. How such extraordinary polymorphism arose and is maintained is controversial. One possibility is heterozygote advantage (HA), which can in principle maintain any number of alleles, but biologically explicit models based on this mechanism have so far failed to reliably predict the coexistence of significantly more than 10 alleles. We here present an eco-evolutionary model showing that evolution can result in the emergence and maintenance of more than 100 alleles under HA if the following two assumptions are fulfilled: first, pathogens are lethal in the absence of an appropriate immune defence; second, the effect of pathogens depends on host condition, with hosts in poorer condition being affected more strongly. Thus, our results show that HA can be a more potent force in explaining the extraordinary polymorphism found at MHC loci than currently recognised.
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- Computational and Systems Biology
- Evolutionary Biology
As pathogens spread in a population of hosts, immunity is built up, and the pool of susceptible individuals are depleted. This generates selective pressure, to which many human RNA viruses, such as influenza virus or SARS-CoV-2, respond with rapid antigenic evolution and frequent emergence of immune evasive variants. However, the host’s immune systems adapt, and older immune responses wane, such that escape variants only enjoy a growth advantage for a limited time. If variant growth dynamics and reshaping of host-immunity operate on comparable time scales, viral adaptation is determined by eco-evolutionary interactions that are not captured by models of rapid evolution in a fixed environment. Here, we use a Susceptible/Infected model to describe the interaction between an evolving viral population in a dynamic but immunologically diverse host population. We show that depending on strain cross-immunity, heterogeneity of the host population, and durability of immune responses, escape variants initially grow exponentially, but lose their growth advantage before reaching high frequencies. Their subsequent dynamics follows an anomalous random walk determined by future escape variants and results in variant trajectories that are unpredictable. This model can explain the apparent contradiction between the clearly adaptive nature of antigenic evolution and the quasi-neutral dynamics of high-frequency variants observed for influenza viruses.
