Genome streamlining in a minute herbivore that manipulates its host plant

Author:

Greenhalgh Robert1ORCID,Dermauw Wannes2ORCID,Glas Joris J3ORCID,Rombauts Stephane45ORCID,Wybouw Nicky2ORCID,Thomas Jainy6,Alba Juan M3ORCID,Pritham Ellen J6,Legarrea Saioa3ORCID,Feyereisen René27ORCID,Van de Peer Yves458ORCID,Van Leeuwen Thomas2ORCID,Clark Richard M19ORCID,Kant Merijn R3ORCID

Affiliation:

1. School of Biological Sciences, University of Utah, Salt Lake City, United States

2. Laboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium

3. Department of Evolutionary and Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands

4. Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium

5. Center for Plant Systems Biology, VIB, Ghent, Belgium

6. Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, United States

7. Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark

8. Centre for Microbial Ecology and Genomics, Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria, South Africa

9. Henry Eyring Center for Cell and Genome Science, University of Utah, Salt Lake City, United States

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.

Funder

Netherlands Organisation for Scientific Research

National Science Foundation

Horizon 2020 - Research and Innovation Framework Programme

Research Foundation Flanders

National Institutes of Health

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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