Analysis of meiosis in Pristionchus pacificus reveals plasticity in homolog pairing and synapsis in the nematode lineage

  1. Regina Rillo-Bohn
  2. Renzo Adilardi
  3. Therese Mitros
  4. Barış Avşaroğlu
  5. Lewis Stevens
  6. Simone Koehler
  7. Joshua Bayes III
  8. Clara Wang
  9. Sabrina Lin
  10. Kayla Alienor Baskevitch
  11. Daniel S Rokhsar
  12. Abby F Dernburg  Is a corresponding author
  1. University of California, Davis, United States
  2. UC Berkeley and HHMI, United States
  3. University of California, Berkeley, United States
  4. Northwestern University, United States
  5. European Molecular Biology Laboratory, Germany
  6. University of California, Berkeley and HHMI, United States

Abstract

Meiosis is conserved across eukaryotes yet varies in the details of its execution. Here we describe a new comparative model system for molecular analysis of meiosis, the nematode Pristionchus pacificus, a distant relative of the widely studied model organism Caenorhabditis elegans. P. pacificus shares many anatomical and other features that facilitate analysis of meiosis in C. elegans. However, while C. elegans has lost the meiosis-specific recombinase Dmc1 and evolved a recombination-independent mechanism to synapse its chromosomes, P. pacificus expresses both DMC-1 and RAD-51. We find that SPO-11 and DMC-1 are required for stable homolog pairing, synapsis, and crossover formation, while RAD-51 is dispensable for these key meiotic processes. RAD-51 and DMC-1 localize sequentially to chromosomes during meiotic prophase and show nonoverlapping functions. We also present a new genetic map for P. pacificus that reveals a crossover landscape very similar to that of C. elegans, despite marked divergence in the regulation of synapsis and crossing-over between these lineages.

Data availability

Sequence data used to generate the recombination map for P. pacificus have been deposited at the NIH Sequence Read Archive under accession number PRJNA734516 and are available at https://www.ncbi.nlm.nih.gov/bioproject/PRJNA734516. These include sequence reads for three parental genomes and 93 hybrid progeny. Genotype calls are provided as Excel files in the Supplemental Data.

The following data sets were generated

Article and author information

Author details

  1. Regina Rillo-Bohn

    University of California, Davis, Davis, CA, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Renzo Adilardi

    Molecular and Cell Biology, UC Berkeley and HHMI, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Therese Mitros

    University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Barış Avşaroğlu

    Molecular and Cell Biology, UC Berkeley and HHMI, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Lewis Stevens

    Department of Molecular Biosciences, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6075-8273
  6. Simone Koehler

    European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Joshua Bayes III

    Molecular and Cell Biology, UC Berkeley and HHMI, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Clara Wang

    Molecular and Cell Biology, UC Berkeley and HHMI, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Sabrina Lin

    Molecular and Cell Biology, UC Berkeley and HHMI, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Kayla Alienor Baskevitch

    Molecular and Cell Biology, UC Berkeley and HHMI, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Daniel S Rokhsar

    University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Abby F Dernburg

    University of California, Berkeley and HHMI, Berkeley, United States
    For correspondence
    afdernburg@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8037-1079

Funding

Howard Hughes Medical Institute

  • Abby F Dernburg

Miller Institute for Basic Research

  • Abby F Dernburg

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2021, Rillo-Bohn 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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https://doi.org/10.7554/eLife.70990

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