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

Rillo-Bohn, Regina; Adilardi, Renzo; Mitros, Therese; Avşaroğlu, Barış; Stevens, Lewis; Köhler, Simone; Bayes, Joshua; Wang, Clara; Lin, Sabrina; Baskevitch, K. Alienor; Rokhsar, Daniel S.; Dernburg, Abby F.

doi:10.7554/elife.70990

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

Journal Article · 23 August 2021 · eLife

DOI: https://doi.org/10.7554/elife.70990 · OSTI ID:1904089

Rillo-Bohn, Regina ^[1];

^[2]; Mitros, Therese ^[3]; Avşaroğlu, Barış ^[2];

^[4]; Köhler, Simone ^[2]; Bayes, Joshua ^[3]; Wang, Clara ^[2]; Lin, Sabrina ^[2]; Baskevitch, K. Alienor ^[2]; Rokhsar, Daniel S. ^[5];

^[6]

University of California, Berkeley, CA (United States); Howard Hughes Medical Institute; Howard Hughes Medical Institute, Chevy Chase, MD (United States); OSTI
University of California, Berkeley, CA (United States); Howard Hughes Medical Institute; Howard Hughes Medical Institute, Chevy Chase, MD (United States)
University of California, Berkeley, CA (United States)
University of California, Berkeley, CA (United States); Wellcome Sanger Institute, Cambridge (United Kingdom)
University of California, Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Okinawa Institute of Science and Technology Graduate University, Onna (Japan); Chan Zuckerberg Biohub, San Francisco, CA (United States)
University of California, Berkeley, CA (United States); Howard Hughes Medical Institute; Howard Hughes Medical Institute, Chevy Chase, MD (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); California Institute for Quantitative Biosciences, Berkeley, CA (United States)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: Helen Hay Whitney Foundation; Howard Hughes Medical Institute; Miller Institute for Basic Research in Science; National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1904089

Journal Information:: eLife, Journal Name: eLife Vol. 10; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

References (108)

Transgenesis by microparticle bombardment for live imaging of fluorescent proteins in Pristionchus pacificus germline and early embryos Namai, Satoshi; Sugimoto, Asako Development Genes and Evolution, Vol. 228, Issue 1 https://doi.org/10.1007/s00427-018-0605-z	journal	January 2018
DMC1: A meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression Bishop, Douglas K.; Park, Demian; Xu, Liuzhong Cell, Vol. 69, Issue 3 https://doi.org/10.1016/0092-8674(92)90446-j	journal	May 1992
Chromosome pairing and synapsis during Caenorhabditis elegans meiosis Rog, Ofer; Dernburg, Abby F. Current Opinion in Cell Biology, Vol. 25, Issue 3 https://doi.org/10.1016/j.ceb.2013.03.003	journal	June 2013
Chromosome Sites Play Dual Roles to Establish Homologous Synapsis during Meiosis in C. elegans MacQueen, Amy J.; Phillips, Carolyn M.; Bhalla, Needhi Cell, Vol. 123, Issue 6 https://doi.org/10.1016/j.cell.2005.09.034	journal	December 2005
Cytoskeletal Forces Span the Nuclear Envelope to Coordinate Meiotic Chromosome Pairing and Synapsis Sato, Aya; Isaac, Berith; Phillips, Carolyn M. Cell, Vol. 139, Issue 5 https://doi.org/10.1016/j.cell.2009.10.039	journal	November 2009
Meiotic Chromosome Homology Search Involves Modifications of the Nuclear Envelope Protein Matefin/SUN-1 Penkner, Alexandra M.; Fridkin, Alexandra; Gloggnitzer, Jiradet Cell, Vol. 139, Issue 5 https://doi.org/10.1016/j.cell.2009.10.045	journal	November 2009
A Family of Zinc-Finger Proteins Is Required for Chromosome-Specific Pairing and Synapsis during Meiosis in C. elegans Phillips, Carolyn M.; Dernburg, Abby F. Developmental Cell, Vol. 11, Issue 6 https://doi.org/10.1016/j.devcel.2006.09.020	journal	December 2006
Polo Kinases Establish Links between Meiotic Chromosomes and Cytoskeletal Forces Essential for Homolog Pairing Labella, Sara; Woglar, Alexander; Jantsch, Verena Developmental Cell, Vol. 21, Issue 5 https://doi.org/10.1016/j.devcel.2011.07.011	journal	November 2011
The Chromosome Axis Mediates Feedback Control of CHK-2 to Ensure Crossover Formation in C. elegans Kim, Yumi; Kostow, Nora; Dernburg, Abby F. Developmental Cell, Vol. 35, Issue 2 https://doi.org/10.1016/j.devcel.2015.09.021	journal	October 2015
Meiosis-Specific DNA Double-Strand Breaks Are Catalyzed by Spo11, a Member of a Widely Conserved Protein Family Keeney, Scott; Giroux, Craig N.; Kleckner, Nancy Cell, Vol. 88, Issue 3 https://doi.org/10.1016/s0092-8674(00)81876-0	journal	February 1997
Meiotic Prophase Arrest with Failure of Chromosome Synapsis in Mice Deficient for Dmc1 , a Germline-Specific RecA Homolog Pittman, Douglas L.; Cobb, John; Schimenti, Kerry J. Molecular Cell, Vol. 1, Issue 5 https://doi.org/10.1016/s1097-2765(00)80069-6	journal	April 1998
Recombination activities of HsDmc1 protein, the meiotic human homolog of RecA protein Li, Zhufang; Golub, Efim I.; Gupta, Ravindra Proceedings of the National Academy of Sciences, Vol. 94, Issue 21 https://doi.org/10.1073/pnas.94.21.11221	journal	October 1997
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
Roles for Caenorhabditis elegans rad-51 in Meiosis and in Resistance to Ionizing Radiation During Development Rinaldo, Cinzia; Bazzicalupo, Paolo; Ederle, Sara Genetics, Vol. 160, Issue 2 https://doi.org/10.1093/genetics/160.2.471	journal	February 2002
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans MacQueen, A. J. Genes & Development, Vol. 16, Issue 18 https://doi.org/10.1101/gad.1011602	journal	September 2002
Roles for two RecA homologs in promoting meiotic chromosome synapsis. Rockmill, B.; Sym, M.; Scherthan, H. Genes & Development, Vol. 9, Issue 21 https://doi.org/10.1101/gad.9.21.2684	journal	November 1995
Random Chromosome Segregation without Meiotic Arrest in Both Male and Female Meiocytes of a dmc1 Mutant of Arabidopsis Couteau, Florence; Belzile, François; Horlow, Christine The Plant Cell, Vol. 11, Issue 9 https://doi.org/10.1105/tpc.11.9.1623	journal	September 1999
Meiotic recombination modulates the structure and dynamics of the synaptonemal complex during C. elegans meiosis Pattabiraman, Divya; Roelens, Baptiste; Woglar, Alexander PLOS Genetics, Vol. 13, Issue 3 https://doi.org/10.1371/journal.pgen.1006670	journal	March 2017
SYP-3 Restricts Synaptonemal Complex Assembly to Bridge Paired Chromosome Axes During Meiosis in Caenorhabditis elegans Smolikov, Sarit; Eizinger, Andreas; Schild-Prufert, Kristina Genetics, Vol. 176, Issue 4 https://doi.org/10.1534/genetics.107.072413	journal	June 2007
Pristionchus pacificus: a well-rounded nematode Hong, Ray L.; Sommer, Ralf J. BioEssays, Vol. 28, Issue 6 https://doi.org/10.1002/bies.20404	journal	January 2006
Centromere organization in meiotic chromosomes of Parascaris univalens Goday, C.; Pimpinelli, S. Chromosoma, Vol. 98, Issue 3 https://doi.org/10.1007/BF00329679	journal	September 1989
Segregation of holocentric chromosomes at meiosis in the nematode,Caenorhabditis elegans Albertson, Donna G.; Thomson, J. Nichol Chromosome Research, Vol. 1, Issue 1 https://doi.org/10.1007/BF00710603	journal	May 1993
Gene inactivation using the CRISPR/Cas9 system in the nematode Pristionchus pacificus Witte, Hanh; Moreno, Eduardo; Rödelsperger, Christian Development Genes and Evolution, Vol. 225, Issue 1 https://doi.org/10.1007/s00427-014-0486-8	journal	December 2014
Transgenesis by microparticle bombardment for live imaging of fluorescent proteins in Pristionchus pacificus germline and early embryos Namai, Satoshi; Sugimoto, Asako Development Genes and Evolution, Vol. 228, Issue 1 https://doi.org/10.1007/s00427-018-0605-z	journal	January 2018
An integrated physical and genetic map of the nematode Pristionchus pacificus Srinivasan, J.; Sinz, W.; Jesse, T. Molecular Genetics and Genomics, Vol. 269, Issue 5 https://doi.org/10.1007/s00438-003-0881-8	journal	July 2003
Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis Melters, Daniël P.; Paliulis, Leocadia V.; Korf, Ian F. Chromosome Research, Vol. 20, Issue 5 https://doi.org/10.1007/s10577-012-9292-1	journal	July 2012
DMC1: A meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression Bishop, Douglas K.; Park, Demian; Xu, Liuzhong Cell, Vol. 69, Issue 3 https://doi.org/10.1016/0092-8674(92)90446-J	journal	May 1992
Meiosis-Specific DNA Double-Strand Breaks Are Catalyzed by Spo11, a Member of a Widely Conserved Protein Family Keeney, Scott; Giroux, Craig N.; Kleckner, Nancy Cell, Vol. 88, Issue 3 https://doi.org/10.1016/S0092-8674(00)81876-0	journal	February 1997
The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair Aravind, L.; Koonin, Eugene V. Trends in Biochemical Sciences, Vol. 23, Issue 8 https://doi.org/10.1016/S0968-0004(98)01257-2	journal	August 1998
Meiotic Prophase Arrest with Failure of Chromosome Synapsis in Mice Deficient for Dmc1 , a Germline-Specific RecA Homolog Pittman, Douglas L.; Cobb, John; Schimenti, Kerry J. Molecular Cell, Vol. 1, Issue 5 https://doi.org/10.1016/S1097-2765(00)80069-6	journal	April 1998
The Mouse RecA-like Gene Dmc1 Is Required for Homologous Chromosome Synapsis during Meiosis Yoshida, Kayo; Kondoh, Gen; Matsuda, Yoichi Molecular Cell, Vol. 1, Issue 5 https://doi.org/10.1016/S1097-2765(00)80070-2	journal	April 1998
Chromosome pairing and synapsis during Caenorhabditis elegans meiosis Rog, Ofer; Dernburg, Abby F. Current Opinion in Cell Biology, Vol. 25, Issue 3 https://doi.org/10.1016/j.ceb.2013.03.003	journal	June 2013
Chromosome Sites Play Dual Roles to Establish Homologous Synapsis during Meiosis in C. elegans MacQueen, Amy J.; Phillips, Carolyn M.; Bhalla, Needhi Cell, Vol. 123, Issue 6 https://doi.org/10.1016/j.cell.2005.09.034	journal	December 2005
HIM-8 Binds to the X Chromosome Pairing Center and Mediates Chromosome-Specific Meiotic Synapsis Phillips, Carolyn M.; Wong, Chihunt; Bhalla, Needhi Cell, Vol. 123, Issue 6 https://doi.org/10.1016/j.cell.2005.09.035	journal	December 2005
Cytoskeletal Forces Span the Nuclear Envelope to Coordinate Meiotic Chromosome Pairing and Synapsis Sato, Aya; Isaac, Berith; Phillips, Carolyn M. Cell, Vol. 139, Issue 5 https://doi.org/10.1016/j.cell.2009.10.039	journal	November 2009
Meiotic Chromosome Homology Search Involves Modifications of the Nuclear Envelope Protein Matefin/SUN-1 Penkner, Alexandra M.; Fridkin, Alexandra; Gloggnitzer, Jiradet Cell, Vol. 139, Issue 5 https://doi.org/10.1016/j.cell.2009.10.045	journal	November 2009
Single-Molecule Sequencing Reveals the Chromosome-Scale Genomic Architecture of the Nematode Model Organism Pristionchus pacificus Rödelsperger, Christian; Meyer, Jan M.; Prabh, Neel Cell Reports, Vol. 21, Issue 3 https://doi.org/10.1016/j.celrep.2017.09.077	journal	October 2017
A Family of Zinc-Finger Proteins Is Required for Chromosome-Specific Pairing and Synapsis during Meiosis in C. elegans Phillips, Carolyn M.; Dernburg, Abby F. Developmental Cell, Vol. 11, Issue 6 https://doi.org/10.1016/j.devcel.2006.09.020	journal	December 2006
The Nuclear Envelope Protein Matefin/SUN-1 Is Required for Homologous Pairing in C. elegans Meiosis Penkner, Alexandra; Tang, Lois; Novatchkova, Maria Developmental Cell, Vol. 12, Issue 6 https://doi.org/10.1016/j.devcel.2007.05.004	journal	June 2007
Polo Kinases Establish Links between Meiotic Chromosomes and Cytoskeletal Forces Essential for Homolog Pairing Labella, Sara; Woglar, Alexander; Jantsch, Verena Developmental Cell, Vol. 21, Issue 5 https://doi.org/10.1016/j.devcel.2011.07.011	journal	November 2011
Pairing Centers Recruit a Polo-like Kinase to Orchestrate Meiotic Chromosome Dynamics in C. elegans Harper, Nicola C.; Rillo, Regina; Jover-Gil, Sara Developmental Cell, Vol. 21, Issue 5 https://doi.org/10.1016/j.devcel.2011.09.001	journal	November 2011
HORMA Domains at the Heart of Meiotic Chromosome Dynamics Vader, Gerben; Musacchio, Andrea Developmental Cell, Vol. 31, Issue 4 https://doi.org/10.1016/j.devcel.2014.11.009	journal	November 2014
The Chromosome Axis Mediates Feedback Control of CHK-2 to Ensure Crossover Formation in C. elegans Kim, Yumi; Kostow, Nora; Dernburg, Abby F. Developmental Cell, Vol. 35, Issue 2 https://doi.org/10.1016/j.devcel.2015.09.021	journal	October 2015
WormBase ParaSite − a comprehensive resource for helminth genomics Howe, Kevin L.; Bolt, Bruce J.; Shafie, Myriam Molecular and Biochemical Parasitology, Vol. 215 https://doi.org/10.1016/j.molbiopara.2016.11.005	journal	July 2017
Meiotic recombination and the crossover assurance checkpoint in Caenorhabditis elegans Yu, Zhouliang; Kim, Yumi; Dernburg, Abby F. Seminars in Cell & Developmental Biology, Vol. 54 https://doi.org/10.1016/j.semcdb.2016.03.014	journal	June 2016
Gonadogenesis in Pristionchus pacificus and organ evolution: development, adult morphology and cell–cell interactions in the hermaphrodite gonad Rudel, David; Riebesell, Metta; Sommer, Ralf J. Developmental Biology, Vol. 277, Issue 1 https://doi.org/10.1016/j.ydbio.2004.09.021	journal	January 2005
Whence Meiosis? Villeneuve, Anne M.; Hillers, Kenneth J. Cell, Vol. 106, Issue 6 https://doi.org/10.1016/s0092-8674(01)00500-1	journal	September 2001
An atypical topoisomerase II from archaea with implications for meiotic recombination Bergerat, Agnès; de Massy, Bernard; Gadelle, Danielle Nature, Vol. 386, Issue 6623 https://doi.org/10.1038/386414a0	journal	March 1997
Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription Zhang, Feng; Cong, Le; Lodato, Simona Nature Biotechnology, Vol. 29, Issue 2 https://doi.org/10.1038/nbt.1775	journal	January 2011
Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in C. elegans Phillips, Carolyn M.; Meng, Xiangdong; Zhang, Lei Nature Cell Biology, Vol. 11, Issue 8 https://doi.org/10.1038/ncb1904	journal	July 2009
Microtubule-driven nuclear rotations promote meiotic chromosome dynamics Christophorou, Nicolas; Rubin, Thomas; Bonnet, Isabelle Nature Cell Biology, Vol. 17, Issue 11 https://doi.org/10.1038/ncb3249	journal	October 2015
The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism Dieterich, Christoph; Clifton, Sandra W.; Schuster, Lisa N. Nature Genetics, Vol. 40, Issue 10 https://doi.org/10.1038/ng.227	journal	September 2008
Fiji: an open-source platform for biological-image analysis Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2019	journal	June 2012
ModelFinder: fast model selection for accurate phylogenetic estimates Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F. Nature Methods, Vol. 14, Issue 6 https://doi.org/10.1038/nmeth.4285	journal	May 2017
Spatiotemporal regulation of Aurora B recruitment ensures release of cohesion during C. elegans oocyte meiosis Ferrandiz, Nuria; Barroso, Consuelo; Telecan, Oana Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03229-5	journal	February 2018
Sex chromosome evolution in parasitic nematodes of humans Foster, Jeremy M.; Grote, Alexandra; Mattick, John Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15654-6	journal	April 2020
Here, There, and Everywhere Dernburg, Abby F. Journal of Cell Biology, Vol. 153, Issue 6 https://doi.org/10.1083/jcb.153.6.f33	journal	June 2001
Identification of novel synaptonemal complex components in C. elegans Hurlock, Matthew E.; Čavka, Ivana; Kursel, Lisa E. Journal of Cell Biology, Vol. 219, Issue 5 https://doi.org/10.1083/jcb.201910043	journal	March 2020
MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization Katoh, Kazutaka; Rozewicki, John; Yamada, Kazunori D. Briefings in Bioinformatics, Vol. 20, Issue 4 https://doi.org/10.1093/bib/bbx108	journal	September 2017
Jalview Version 2--a multiple sequence alignment editor and analysis workbench Waterhouse, A. M.; Procter, J. B.; Martin, D. M. A. Bioinformatics, Vol. 25, Issue 9 https://doi.org/10.1093/bioinformatics/btp033	journal	January 2009
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs Simão, Felipe A.; Waterhouse, Robert M.; Ioannidis, Panagiotis Bioinformatics, Vol. 31, Issue 19 https://doi.org/10.1093/bioinformatics/btv351	journal	June 2015
AtSPO11-1 is necessary for efficient meiotic recombination in plants Grelon, M. The EMBO Journal, Vol. 20, Issue 3 https://doi.org/10.1093/emboj/20.3.589	journal	February 2001
A telomere-to-telomere assembly ofOscheius tipulaeand the evolution of rhabditid nematode chromosomes Gonzalez de la Rosa, Pablo Manuel; Thomson, Marian; Trivedi, Urmi G3 Genes\|Genomes\|Genetics, Vol. 11, Issue 1 https://doi.org/10.1093/g3journal/jkaa020	journal	December 2020
A Genome Resequencing-Based Genetic Map Reveals the Recombination Landscape of an Outbred Parasitic Nematode in the Presence of Polyploidy and Polyandry Doyle, Stephen R.; Laing, Roz; Bartley, David J. Genome Biology and Evolution, Vol. 10, Issue 2 https://doi.org/10.1093/gbe/evx269	journal	December 2017
HOP1: a yeast meiotic pairing gene. Hollingsworth, N. M.; Byers, B. Genetics, Vol. 121, Issue 3 https://doi.org/10.1093/genetics/121.3.445	journal	March 1989
Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans. Barnes, T. M.; Kohara, Y.; Coulson, A. Genetics, Vol. 141, Issue 1 https://doi.org/10.1093/genetics/141.1.159	journal	September 1995
Roles for Caenorhabditis elegans rad-51 in Meiosis and in Resistance to Ionizing Radiation During Development Rinaldo, Cinzia; Bazzicalupo, Paolo; Ederle, Sara Genetics, Vol. 160, Issue 2 https://doi.org/10.1093/genetics/160.2.471	journal	February 2002
A Bacterial Artificial Chromosome-Based Genetic Linkage Map of the Nematode Pristionchus pacificus Srinivasan, Jagan; Sinz, Waltraud; Lanz, Christa Genetics, Vol. 162, Issue 1 https://doi.org/10.1093/genetics/162.1.129	journal	September 2002
THE GENETICS OF CAENORHABDITIS ELEGANS Brenner, S. Genetics, Vol. 77, Issue 1 https://doi.org/10.1093/genetics/77.1.71	journal	May 1974
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
Tandem repeats finder: a program to analyze DNA sequences Benson, G. Nucleic Acids Research, Vol. 27, Issue 2 https://doi.org/10.1093/nar/27.2.573	journal	January 1999
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw290	journal	April 2016
Shugoshin protects cohesin complexes at centromeres Watanabe, Yoshinori; Kitajima, Tomoya S. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 360, Issue 1455 https://doi.org/10.1098/rstb.2004.1607	journal	March 2005
Origins of Eukaryotic Sexual Reproduction Goodenough, U.; Heitman, J. Cold Spring Harbor Perspectives in Biology, Vol. 6, Issue 3 https://doi.org/10.1101/cshperspect.a016154	journal	March 2014
Meiotic Recombination: The Essence of Heredity Hunter, Neil Cold Spring Harbor Perspectives in Biology https://doi.org/10.1101/cshperspect.a016618	journal	October 2015
Recombination, Pairing, and Synapsis of Homologs during Meiosis Zickler, Denise; Kleckner, Nancy Cold Spring Harbor Perspectives in Biology, Vol. 7, Issue 6 https://doi.org/10.1101/cshperspect.a016626	journal	May 2015
Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans MacQueen, A. J. Genes & Development, Vol. 16, Issue 18 https://doi.org/10.1101/gad.1011602	journal	September 2002
Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion Martinez-Perez, Enrique; Schvarzstein, Mara; Barroso, Consuelo Genes & Development, Vol. 22, Issue 20 https://doi.org/10.1101/gad.1694108	journal	October 2008
Defining the influence of Rad51 and Dmc1 lineage-specific amino acids on genetic recombination Steinfeld, Justin B.; Beláň, Ondrej; Kwon, Youngho Genes & Development, Vol. 33, Issue 17-18 https://doi.org/10.1101/gad.328062.119	journal	August 2019
Roles for two RecA homologs in promoting meiotic chromosome synapsis. Rockmill, B.; Sym, M.; Scherthan, H. Genes & Development, Vol. 9, Issue 21 https://doi.org/10.1101/gad.9.21.2684	journal	November 1995
Young genes have distinct gene structure, epigenetic profiles, and transcriptional regulation Werner, Michael S.; Sieriebriennikov, Bogdan; Prabh, Neel Genome Research, Vol. 28, Issue 11 https://doi.org/10.1101/gr.234872.118	journal	September 2018
Efficient Architecture-Aware Acceleration of BWA-MEM for Multicore Systems Vasimuddin, Md.; Misra, Sanchit; Li, Heng 2019 IEEE International Parallel and Distributed Processing Symposium (IPDPS) https://doi.org/10.1109/IPDPS.2019.00041	conference	May 2019
OneMap: software for genetic mapping in outcrossing species: OneMap Margarido, G. R. A.; Souza, A. P.; Garcia, A. A. F. Hereditas, Vol. 144, Issue 3 https://doi.org/10.1111/j.2007.0018-0661.02000.x	journal	June 2007
Rad51 Is an Accessory Factor for Dmc1-Mediated Joint Molecule Formation During Meiosis Cloud, V.; Chan, Y. -L.; Grubb, J. Science, Vol. 337, Issue 6099 https://doi.org/10.1126/science.1219379	journal	September 2012
RAD-51-Dependent and -Independent Roles of a Caenorhabditis elegans BRCA2-Related Protein during DNA Double-Strand Break Repair Martin, Julie S.; Winkelmann, Nicole; Petalcorin, Mark I. R. Molecular and Cellular Biology, Vol. 25, Issue 8 https://doi.org/10.1128/MCB.25.8.3127-3139.2005	journal	April 2005
The Molecular Control of Meiotic Chromosomal Behavior: Events in Early Meiotic Prophase in Drosophila Oocytes Lake, Cathleen M.; Hawley, R. Scott Annual Review of Physiology, Vol. 74, Issue 1 https://doi.org/10.1146/annurev-physiol-020911-153342	journal	March 2012
Meiotic Chromosomes: Integrating Structure and Function Zickler, D.; Kleckner, N. Annual Review of Genetics, Vol. 33, Issue 1 https://doi.org/10.1146/annurev.genet.33.1.603	journal	December 1999
BLAST+: architecture and applications Camacho, Christiam; Coulouris, George; Avagyan, Vahram BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-421	journal	January 2009
ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees Zhang, Chao; Rabiee, Maryam; Sayyari, Erfan BMC Bioinformatics, Vol. 19, Issue S6 https://doi.org/10.1186/s12859-018-2129-y	journal	May 2018
OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy Emms, David M.; Kelly, Steven Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0721-2	journal	August 2015
X-chromosome silencing in the germline of C. elegans Kelly, William G.; Schaner, Christine E.; Dernburg, Abby F. Development, Vol. 129, Issue 2 https://doi.org/10.1242/dev.129.2.479	journal	January 2002
LAB-1 Targets PP1 and Restricts Aurora B Kinase upon Entrance into Meiosis to Promote Sister Chromatid Cohesion Tzur, Yonatan B.; Egydio de Carvalho, Carlos; Nadarajan, Saravanapriah PLoS Biology, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pbio.1001378	journal	August 2012
C. elegans Germ Cells Switch between Distinct Modes of Double-Strand Break Repair During Meiotic Prophase Progression Hayashi, Michiko; Chin, Gregory M.; Villeneuve, Anne M. PLoS Genetics, Vol. 3, Issue 11 https://doi.org/10.1371/journal.pgen.0030191	journal	November 2007
Recombinational Landscape and Population Genomics of Caenorhabditis elegans Rockman, Matthew V.; Kruglyak, Leonid PLoS Genetics, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pgen.1000419	journal	March 2009
Spermatogenesis-Specific Features of the Meiotic Program in Caenorhabditis elegans Shakes, Diane C.; Wu, Jui-ching; Sadler, Penny L. PLoS Genetics, Vol. 5, Issue 8 https://doi.org/10.1371/journal.pgen.1000611	journal	August 2009
Meiotic Recombination in Arabidopsis Is Catalysed by DMC1, with RAD51 Playing a Supporting Role Da Ines, Olivier; Degroote, Fabienne; Goubely, Chantal PLoS Genetics, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pgen.1003787	journal	September 2013
Synaptonemal Complex Components Promote Centromere Pairing in Pre-meiotic Germ Cells Christophorou, Nicolas; Rubin, Thomas; Huynh, Jean-René PLoS Genetics, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pgen.1004012	journal	December 2013
Transition from a meiotic to a somatic-like DNA damage response during the pachytene stage in mouse meiosis Enguita-Marruedo, Andrea; Martín-Ruiz, Marta; García, Eva PLOS Genetics, Vol. 15, Issue 1 https://doi.org/10.1371/journal.pgen.1007439	journal	January 2019
Excess crossovers impede faithful meiotic chromosome segregation in C. elegans Hollis, Jeremy A.; Glover, Marissa L.; Schlientz, Aleesa J. PLOS Genetics, Vol. 16, Issue 9 https://doi.org/10.1371/journal.pgen.1009001	journal	September 2020
Chromosome-Wide Evolution and Sex Determination in the Three-Sexed Nematode Auanema rhodensis Tandonnet, Sophie; Koutsovoulos, Georgios D.; Adams, Sally G3 Genes\|Genomes\|Genetics, Vol. 9, Issue 4 https://doi.org/10.1534/g3.119.0011	journal	April 2019
Meiotic and Mitotic Recombination in Meiosis Kohl, Kathryn P.; Sekelsky, Jeff Genetics, Vol. 194, Issue 2 https://doi.org/10.1534/genetics.113.150581	journal	June 2013
Precise and Heritable Genome Editing in Evolutionarily Diverse Nematodes Using TALENs and CRISPR/Cas9 to Engineer Insertions and Deletions Lo, Te-Wen; Pickle, Catherine S.; Lin, Steven Genetics, Vol. 195, Issue 2 https://doi.org/10.1534/genetics.113.155382	journal	August 2013
Random Chromosome Segregation without Meiotic Arrest in Both Male and Female Meiocytes of a dmc1 Mutant of Arabidopsis Couteau, Florence; Belzile, Francois; Horlow, Christine The Plant Cell, Vol. 11, Issue 9 https://doi.org/10.2307/3871042	journal	September 1999
Meiosis in male Drosophila McKee, Bruce D.; Yan, Rihui; Tsai, Jui-He Spermatogenesis, Vol. 2, Issue 3 https://doi.org/10.4161/spmg.21800	journal	July 2012
Divergent kleisin subunits of cohesin specify mechanisms to tether and release meiotic chromosomes Severson, Aaron F.; Meyer, Barbara J. eLife, Vol. 3 https://doi.org/10.7554/eLife.03467	journal	August 2014
Polo-like kinase-dependent phosphorylation of the synaptonemal complex protein SYP-4 regulates double-strand break formation through a negative feedback loop. Nadarajan, Saravanapriah; Lambert, Talley J.; Altendorfer, Elisabeth eLife, Vol. 6 https://doi.org/10.7554/eLife.23437	journal	March 2017