1. Evolutionary Biology
  2. Microbiology and Infectious Disease
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A unique chromatin profile defines adaptive genomic regions in a fungal plant pathogen

  1. David E Cook  Is a corresponding author
  2. H Martin Kramer
  3. David E Torres
  4. Michael F Seidl
  5. Bart PHJ Thomma  Is a corresponding author
  1. Kansas State University, United States
  2. Wageningen University, Netherlands
Research Article
  • Cited 5
  • Views 1,172
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Cite this article as: eLife 2020;9:e62208 doi: 10.7554/eLife.62208

Abstract

Genomes store information at scales beyond the linear nucleotide sequence, which impacts genome function at the level of an individual, while influences on populations and long-term genome function remains unclear. Here, we addressed how physical and chemical DNA characteristics influence genome evolution in the plant pathogenic fungus Verticillium dahliae. We identified incomplete DNA methylation of repetitive elements, associated with specific genomic compartments originally defined as Lineage-Specific (LS) regions that contain genes involved in host adaptation. Further chromatin characterization revealed associations with features such as H3 Lys-27 methylated histones (H3K27me3) and accessible DNA. Machine learning trained on chromatin data identified twice as much LS DNA as previously recognized, which was validated through orthogonal analysis, and we propose to refer to this DNA as adaptive genomic regions. Our results provide evidence that specific chromatin profiles define adaptive genomic regions, and highlight how different epigenetic factors contribute to the organization of these regions.

Data availability

The sequencing data for this project are accessible from the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) under BioProject PRJNA592220.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. David E Cook

    Department of Plant Pathology, Kansas State University, Manhattan, United States
    For correspondence
    decook@ksu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2719-4701
  2. H Martin Kramer

    Laboratory of Phytopathology, Wageningen University, Wageningen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. David E Torres

    Laboratory of Phytopathology, Wageningen University, Wageningen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Michael F Seidl

    Laboratory of Phytopathology, Wageningen University, Wageningen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Bart PHJ Thomma

    Laboratory of Phytopathology, Wageningen University, Wageningen, Netherlands
    For correspondence
    bart.thomma@wur.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4125-4181

Funding

Nederlandse Organisatie voor Wetenschappelijk Onderzoek

  • Michael F Seidl
  • Bart PHJ Thomma

European Molecular Biology Organization (Postdoctoral fellowship EMBO, ALTF 969-2013)

  • David E Cook

Human Frontier Science Program (Postdoctoral Fellowship HFSP, LT000627/2014-L)

  • David E Cook

Deutsche Forschungsgemeinschaft

  • Bart PHJ Thomma

Conacyt

  • David E Torres

United States Department of Agriculture

  • David E Cook

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

Publication history

  1. Received: August 18, 2020
  2. Accepted: December 17, 2020
  3. Accepted Manuscript published: December 18, 2020 (version 1)
  4. Version of Record published: January 4, 2021 (version 2)

Copyright

© 2020, Cook 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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Further reading

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    1. Developmental Biology
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    Eukaryotic life cycles alternate between haploid and diploid phases and in phylogenetically diverse unicellular eukaryotes, expression of paralogous homeodomain genes in gametes primes the haploid-to-diploid transition. In the unicellular chlorophyte alga Chlamydomonas, KNOX and BELL TALE-homeodomain genes mediate this transition. We demonstrate that in the liverwort Marchantia polymorpha, paternal (sperm) expression of three of five phylogenetically diverse BELL genes, MpBELL234, and maternal (egg) expression of both MpKNOX1 and MpBELL34 mediate the haploid-to-diploid transition. Loss-of-function alleles of MpKNOX1 result in zygotic arrest, whereas a loss of either maternal or paternal MpBELL234 results in variable zygotic and early embryonic arrest. Expression of MpKNOX1 and MpBELL34 during diploid sporophyte development is consistent with a later role for these genes in patterning the sporophyte. These results indicate that the ancestral mechanism to activate diploid gene expression was retained in early diverging land plants and subsequently co-opted during evolution of the diploid sporophyte body.