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.

Metrics

  • 1,663
    views
  • 235
    downloads
  • 25
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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
(2021)
Analysis of meiosis in Pristionchus pacificus reveals plasticity in homolog pairing and synapsis in the nematode lineage
eLife 10:e70990.
https://doi.org/10.7554/eLife.70990

Share this article

https://doi.org/10.7554/eLife.70990

Further reading

    1. Cell Biology
    2. Physics of Living Systems
    David Trombley McSwiggen, Helen Liu ... Hilary P Beck
    Research Article

    The regulation of cell physiology depends largely upon interactions of functionally distinct proteins and cellular components. These interactions may be transient or long-lived, but often affect protein motion. Measurement of protein dynamics within a cellular environment, particularly while perturbing protein function with small molecules, may enable dissection of key interactions and facilitate drug discovery; however, current approaches are limited by throughput with respect to data acquisition and analysis. As a result, studies using super-resolution imaging are typically drawing conclusions from tens of cells and a few experimental conditions tested. We addressed these limitations by developing a high-throughput single-molecule tracking (htSMT) platform for pharmacologic dissection of protein dynamics in living cells at an unprecedented scale (capable of imaging >106 cells/day and screening >104 compounds). We applied htSMT to measure the cellular dynamics of fluorescently tagged estrogen receptor (ER) and screened a diverse library to identify small molecules that perturbed ER function in real time. With this one experimental modality, we determined the potency, pathway selectivity, target engagement, and mechanism of action for identified hits. Kinetic htSMT experiments were capable of distinguishing between on-target and on-pathway modulators of ER signaling. Integrated pathway analysis recapitulated the network of known ER interaction partners and suggested potentially novel, kinase-mediated regulatory mechanisms. The sensitivity of htSMT revealed a new correlation between ER dynamics and the ability of ER antagonists to suppress cancer cell growth. Therefore, measuring protein motion at scale is a powerful method to investigate dynamic interactions among proteins and may facilitate the identification and characterization of novel therapeutics.

    1. Cell Biology
    2. Neuroscience
    Jiayao Zhang, Juan Li ... Weicai Liu
    Research Article

    It has been well validated that chronic psychological stress leads to bone loss, but the underlying mechanism remains unclarified. In this study, we established and analyzed the chronic unpredictable mild stress (CUMS) mice to investigate the miRNA-related pathogenic mechanism involved in psychological stress-induced osteoporosis. Our result found that these CUMS mice exhibited osteoporosis phenotype that is mainly attributed to the abnormal activities of osteoclasts. Subsequently, miRNA sequencing and other analysis showed that miR-335-3p, which is normally highly expressed in the brain, was significantly downregulated in the nucleus ambiguous, serum, and bone of the CUMS mice. Additionally, in vitro studies detected that miR-335-3p is important for osteoclast differentiation, with its direct targeting site in Fos. Further studies demonstrated FOS was upregulated in CUMS osteoclast, and the inhibition of FOS suppressed the accelerated osteoclastic differentiation, as well as the expression of osteoclastic genes, such as Nfatc1, Acp5, and Mmp9, in miR-335-3p-restrained osteoclasts. In conclusion, this work indicated that psychological stress may downregulate the miR-335-3p expression, which resulted in the accumulation of FOS and the upregulation of NFACT1 signaling pathway in osteoclasts, leading to its accelerated differentiation and abnormal activity. These results decipher a previously unrecognized paradigm that miRNA can act as a link between psychological stress and bone metabolism.