Analysis of meiosis in Pristionchus pacificus reveals plasticity in homolog pairing and synapsis in the nematode lineage
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 shar...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2021-08-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/70990 |
| _version_ | 1811253619847069696 |
|---|---|
| author | Regina Rillo-Bohn Renzo Adilardi Therese Mitros Barış Avşaroğlu Lewis Stevens Simone Köhler Joshua Bayes Clara Wang Sabrina Lin K Alienor Baskevitch Daniel S Rokhsar Abby F Dernburg |
| author_facet | Regina Rillo-Bohn Renzo Adilardi Therese Mitros Barış Avşaroğlu Lewis Stevens Simone Köhler Joshua Bayes Clara Wang Sabrina Lin K Alienor Baskevitch Daniel S Rokhsar Abby F Dernburg |
| author_sort | Regina Rillo-Bohn |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-12T16:54:14Z |
| format | Article |
| id | doaj.art-f03a33e1be724ed2b2fbe6044a015c9a |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T16:54:14Z |
| publishDate | 2021-08-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-f03a33e1be724ed2b2fbe6044a015c9a2022-12-22T03:24:18ZengeLife Sciences Publications LtdeLife2050-084X2021-08-011010.7554/eLife.70990Analysis of meiosis in Pristionchus pacificus reveals plasticity in homolog pairing and synapsis in the nematode lineageRegina Rillo-Bohn0Renzo Adilardi1https://orcid.org/0000-0001-7279-3853Therese Mitros2Barış Avşaroğlu3Lewis Stevens4https://orcid.org/0000-0002-6075-8273Simone Köhler5Joshua Bayes6Clara Wang7Sabrina Lin8K Alienor Baskevitch9Daniel S Rokhsar10Abby F Dernburg11https://orcid.org/0000-0001-8037-1079Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States; Howard Hughes Medical Institute, Chevy Chase, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States; Howard Hughes Medical Institute, Chevy Chase, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States; Howard Hughes Medical Institute, Chevy Chase, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States; Darwin Tree of Life Project, Wellcome Sanger Institute, Cambridge, United KingdomDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States; Howard Hughes Medical Institute, Chevy Chase, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States; Howard Hughes Medical Institute, Chevy Chase, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States; Howard Hughes Medical Institute, Chevy Chase, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States; Howard Hughes Medical Institute, Chevy Chase, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States; Department of Energy Joint Genome Institute, Berkeley, United States; Okinawa Institute of Science and Technology Graduate University, Onna, Japan; Chan Zuckerberg Biohub, San Francisco, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States; Howard Hughes Medical Institute, Chevy Chase, United States; Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, United States; California Institute for Quantitative Biosciences, Berkeley, United StatesMeiosis 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.https://elifesciences.org/articles/70990pristionchus pacificusmeiosismeiotic recombinationchromosome pairingcomparative cell biology |
| spellingShingle | Regina Rillo-Bohn Renzo Adilardi Therese Mitros Barış Avşaroğlu Lewis Stevens Simone Köhler Joshua Bayes Clara Wang Sabrina Lin K Alienor Baskevitch Daniel S Rokhsar Abby F Dernburg Analysis of meiosis in Pristionchus pacificus reveals plasticity in homolog pairing and synapsis in the nematode lineage eLife pristionchus pacificus meiosis meiotic recombination chromosome pairing comparative cell biology |
| title | Analysis of meiosis in Pristionchus pacificus reveals plasticity in homolog pairing and synapsis in the nematode lineage |
| title_full | Analysis of meiosis in Pristionchus pacificus reveals plasticity in homolog pairing and synapsis in the nematode lineage |
| title_fullStr | Analysis of meiosis in Pristionchus pacificus reveals plasticity in homolog pairing and synapsis in the nematode lineage |
| title_full_unstemmed | Analysis of meiosis in Pristionchus pacificus reveals plasticity in homolog pairing and synapsis in the nematode lineage |
| title_short | Analysis of meiosis in Pristionchus pacificus reveals plasticity in homolog pairing and synapsis in the nematode lineage |
| title_sort | analysis of meiosis in pristionchus pacificus reveals plasticity in homolog pairing and synapsis in the nematode lineage |
| topic | pristionchus pacificus meiosis meiotic recombination chromosome pairing comparative cell biology |
| url | https://elifesciences.org/articles/70990 |
| work_keys_str_mv | AT reginarillobohn analysisofmeiosisinpristionchuspacificusrevealsplasticityinhomologpairingandsynapsisinthenematodelineage AT renzoadilardi analysisofmeiosisinpristionchuspacificusrevealsplasticityinhomologpairingandsynapsisinthenematodelineage AT theresemitros analysisofmeiosisinpristionchuspacificusrevealsplasticityinhomologpairingandsynapsisinthenematodelineage AT barısavsaroglu analysisofmeiosisinpristionchuspacificusrevealsplasticityinhomologpairingandsynapsisinthenematodelineage AT lewisstevens analysisofmeiosisinpristionchuspacificusrevealsplasticityinhomologpairingandsynapsisinthenematodelineage AT simonekohler analysisofmeiosisinpristionchuspacificusrevealsplasticityinhomologpairingandsynapsisinthenematodelineage AT joshuabayes analysisofmeiosisinpristionchuspacificusrevealsplasticityinhomologpairingandsynapsisinthenematodelineage AT clarawang analysisofmeiosisinpristionchuspacificusrevealsplasticityinhomologpairingandsynapsisinthenematodelineage AT sabrinalin analysisofmeiosisinpristionchuspacificusrevealsplasticityinhomologpairingandsynapsisinthenematodelineage AT kalienorbaskevitch analysisofmeiosisinpristionchuspacificusrevealsplasticityinhomologpairingandsynapsisinthenematodelineage AT danielsrokhsar analysisofmeiosisinpristionchuspacificusrevealsplasticityinhomologpairingandsynapsisinthenematodelineage AT abbyfdernburg analysisofmeiosisinpristionchuspacificusrevealsplasticityinhomologpairingandsynapsisinthenematodelineage |