Arribere JA, Bell RT, Fu BXH, Artiles KL, Hartman PS, Fire AZ. 2014. Efficient marker-free recovery of custom
genetic modifications with CRISPR/Cas9 in Caenorhabditis elegans. Genetics 198:837–846. DOI: https://doi.
org/10.1534/genetics.114.169730, PMID: 25161212
Baudat F, Manova K, Yuen JP, Jasin M, Keeney S. 2000. Chromosome synapsis defects and sexually dimorphic
meiotic progression in mice lacking Spo11. Molecular Cell 6:989–998. DOI: https://doi.org/10.1016/s1097-
2765(00)00098-8, PMID: 11106739
Bhalla N, Dernburg AF. 2005. A conserved checkpoint monitors meiotic chromosome synapsis in Caenorhabditis
elegans. Science 310:1683–1686. DOI: https://doi.org/10.1126/science.1117468, PMID: 16339446
Blitzblau HG, Hochwagen A. 2013. ATR/Mec1 prevents lethal meiotic recombination initiation on partially
replicated chromosomes in budding yeast. eLife 2:e00844. DOI: https://doi.org/10.7554/eLife.00844, PMID:
24137535
Bradley RK, Roberts A, Smoot M, Juvekar S, Do J, Dewey C, Holmes I, Pachter L. 2009. Fast statistical
alignment. PLOS Computational Biology 5:e1000392. DOI: https://doi.org/10.1371/journal.pcbi.1000392,
PMID: 19478997
Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71–94. DOI: https://doi.org/10.1093/
genetics/77.1.71, PMID: 4366476
Burel JM, Besson S, Blackburn C, Carroll M, Ferguson RK, Flynn H, Gillen K, Leigh R, Li S, Lindner D, Linkert M,
Moore WJ, Ramalingam B, Rozbicki E, Tarkowska A, Walczysko P, Allan C, Moore J, Swedlow JR. 2015.
Publishing and sharing multi-dimensional image data with OMERO. Mammalian Genome 26:441–447. DOI:
https://doi.org/10.1007/s00335-015-9587-6, PMID: 26223880
Carballo JA, Panizza S, Serrentino ME, Johnson AL, Geymonat M, Borde V, Klein F, Cha RS. 2013. Budding yeast
ATM/ATR control meiotic double-strand break (DSB) levels by down-regulating Rec114, an essential
component of the DSB-machinery. PLOS Genetics 9:e1003545. DOI: https://doi.org/10.1371/journal.pgen.
1003545
Carlton P. 2022. deltavisionquant. swh:1:rev:7faed1a32db1958b5677971c7ab5da823d04f1c9. Software
Heritage. https://archive.softwareheritage.org/swh:1:dir:638aa3f08201e88cfa7daeaecc6c67cd21f0e0d4;
origin=https://github.com/pmcarlton/deltavisionquant;visit=swh:1:snp:a6a10e0b064ebfc676ae3171ea036313
41860f27;anchor=swh:1:rev:7faed1a32db1958b5677971c7ab5da823d04f1c9
Chen H, Hughes DD, Chan TA, Sedat JW, Agard DA. 1996. IVE (Image Visualization Environment): a software
platform for all three-dimensional microscopy applications. Journal of Structural Biology 116:56–60. DOI:
https://doi.org/10.1006/jsbi.1996.0010, PMID: 8742723
Chin GM, Villeneuve AM. 2001. C. elegans mre-11 is required for meiotic recombination and DNA repair but is
dispensable for the meiotic G(2) DNA damage checkpoint. Genes & Development 15:522–534. DOI: https://
doi.org/10.1101/gad.864101, PMID: 11238374
Chuang CN, Cheng YH, Wang TF. 2012. Mek1 stabilizes Hop1-Thr318 phosphorylation to promote interhomolog
recombination and checkpoint responses during yeast meiosis. Nucleic Acids Research 40:11416–11427. DOI:
https://doi.org/10.1093/nar/gks920, PMID: 23047948
Claeys Bouuaert C, Pu S, Wang J, Oger C, Daccache D, Xie W, Patel DJ, Keeney S. 2021. DNA-driven
condensation assembles the meiotic DNA break machinery. Nature 592:144–149. DOI: https://doi.org/10.
1038/s41586-021-03374-w, PMID: 33731927
Couteau F, Zetka M. 2011. DNA damage during meiosis induces chromatin remodeling and synaptonemal
complex disassembly. Developmental Cell 20:353–363. DOI: https://doi.org/10.1016/j.devcel.2011.01.015,
PMID: 21397846
Dainat J, Hereñú D, Pucholt P. 2020. NBISweden/AGAT: AGAT-v0.5.1. v0.5.1. Zenodo. https://doi.org/10.5281/
zenodo.4205393DOI: https://doi.org/doi:10.5281/ZENODO.3552717
Davis P, Zarowiecki M, Arnaboldi V, Becerra A, Cain S, Chan J, Chen WJ, Cho J, da Veiga Beltrame E,
Diamantakis S, Gao S, Grigoriadis D, Grove CA, Harris TW, Kishore R, Le T, Lee RYN, Luypaert M, Müller HM,
Nakamura C, et al. 2022. WormBase in 2022-data, processes, and tools for analyzing Caenorhabditis elegans.
Genetics 220:iyac003. DOI: https://doi.org/10.1093/genetics/iyac003, PMID: 35134929
Dereli I, Stanzione M, Olmeda F, Papanikos F, Baumann M, Demir S, Carofiglio F, Lange J, de Massy B,
Baarends WM, Turner J, Rulands S, Tóth A. 2021. Four-pronged negative feedback of DSB machinery in meiotic
Guo et al. eLife 2022;11:e77956. DOI: https://doi.org/10.7554/eLife.77956
26 of 30
A Self-archived copy in
Kyoto University Research Information Repository
https://repository.kulib.kyoto-u.ac.jp
Cell Biology | Genetics and Genomics
Research article
DNA-break control in mice. Nucleic Acids Research 49:2609–2628. DOI: https://doi.org/10.1093/nar/gkab082,
PMID: 33619545
Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM. 1998. Meiotic recombination in
C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell
94:387–398. DOI: https://doi.org/10.1016/s0092-8674(00)81481-6, PMID: 9708740
Duursma AM, Driscoll R, Elias JE, Cimprich KA. 2013. A role for the MRN complex in ATR activation via TOPBP1
recruitment. Molecular Cell 50:116–122. DOI: https://doi.org/10.1016/j.molcel.2013.03.006, PMID: 23582259
Eaton JW, Bateman D, Hauberg S, Wehbring R. 2020. GNU Octave version 5.2.0 manual: a high-level interactive
language for numerical computations. GNU Octave.
Emms DM, Kelly S. 2019. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome
Biology 20:238. DOI: https://doi.org/10.1186/s13059-019-1832-y, PMID: 31727128
Emms D. 2022. OrthoFinder: phylogenetic orthology inference for comparative genomics. 3.0. GitHub. https://
github.com/davidemms/OrthoFinder
Falk JE, Chan AC, Hoffmann E, Hochwagen A. 2010. A Mec1- and PP4-dependent checkpoint couples
centromere pairing to meiotic recombination. Developmental Cell 19:599–611. DOI: https://doi.org/10.1016/j.
devcel.2010.09.006, PMID: 20951350
Garcia V, Gray S, Allison RM, Cooper TJ, Neale MJ. 2015. Tel1(ATM)-mediated interference suppresses clustered
meiotic double-strand-break formation. Nature 520:114–118. DOI: https://doi.org/10.1038/nature13993,
PMID: 25539084
Garcia-Muse T, Boulton SJ. 2005. Distinct modes of ATR activation after replication stress and DNA double-
strand breaks in Caenorhabditis elegans. The EMBO Journal 24:4345–4355. DOI: https://doi.org/10.1038/sj.
emboj.7600896, PMID: 16319925
Goodyer W, Kaitna S, Couteau F, Ward JD, Boulton SJ, Zetka M. 2008. HTP-3 links DSB formation with homolog
pairing and crossing over during C. elegans meiosis. Developmental Cell 14:263–274. DOI: https://doi.org/10.
1016/j.devcel.2007.11.016, PMID: 18267094
Han X, Gomes JE, Birmingham CL, Pintard L, Sugimoto A, Mains PE. 2009. The role of protein phosphatase 4 in
regulating microtubule severing in the Caenorhabditis elegans embryo. Genetics 181:933–943. DOI: https://
doi.org/10.1534/genetics.108.096016, PMID: 19087961
Hayashi M, Chin GM, Villeneuve AM. 2007. C. elegans germ cells switch between distinct modes of double-
strand break repair during meiotic prophase progression. PLOS Genetics 3:e191. DOI: https://doi.org/10.1371/
journal.pgen.0030191, PMID: 17983271
Hinman AW, Yeh HY, Roelens B, Yamaya K, Woglar A, Bourbon HMG, Chi P, Villeneuve AM. 2021.
Caenorhabditis elegans DSB-3 reveals conservation and divergence among protein complexes promoting
meiotic double-strand breaks. PNAS 118:e2109306118. DOI: https://doi.org/10.1073/pnas.2109306118, PMID:
34389685
Howe KL, Bolt BJ, Shafie M, Kersey P, Berriman M. 2017. WormBase ParaSite - a comprehensive resource for
helminth genomics. Molecular and Biochemical Parasitology 215:2–10. DOI: https://doi.org/10.1016/j.
molbiopara.2016.11.005, PMID: 27899279
Huerta-Cepas J, Serra F, Bork P. 2016. Ete 3: Reconstruction, analysis, and visualization of phylogenomic data.
Molecular Biology and Evolution 33:1635–1638. DOI: https://doi.org/10.1093/molbev/msw046, PMID:
26921390
Hustedt N, Seeber A, Sack R, Tsai-Pflugfelder M, Bhullar B, Vlaming H, van Leeuwen F, Guénolé A,
van Attikum H, Srivas R, Ideker T, Shimada K, Gasser SM. 2015. Yeast PP4 interacts with ATR homolog
Ddc2-Mec1 and regulates checkpoint signaling. Molecular Cell 57:273–289. DOI: https://doi.org/10.1016/j.
molcel.2014.11.016, PMID: 25533186
Johnson D, Crawford M, Cooper T, Claeys Bouuaert C, Keeney S, Llorente B, Garcia V, Neale MJ. 2021.
Concerted cutting by Spo11 illuminates meiotic DNA break mechanics. Nature 594:572–576. DOI: https://doi.
org/10.1038/s41586-021-03389-3, PMID: 34108687
Jones MR, Huang JC, Chua SY, Baillie DL, Rose AM. 2012. The atm-1 gene is required for genome stability in
Caenorhabditis elegans. Molecular Genetics and Genomics 287:325–335. DOI: https://doi.org/10.1007/
s00438-012-0681-0, PMID: 22350747
Joyce EF, Pedersen M, Tiong S, White-Brown SK, Paul A, Campbell SD, McKim KS. 2011. Drosophila ATM and
ATR have distinct activities in the regulation of meiotic DNA damage and repair. The Journal of Cell Biology
195:359–367. DOI: https://doi.org/10.1083/jcb.201104121, PMID: 22024169
Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A,
Potapenko A, Bridgland A, Meyer C, Kohl SAA, Ballard AJ, Cowie A, Romera-Paredes B, Nikolov S, Jain R,
Adler J, Back T, et al. 2021. Highly accurate protein structure prediction with AlphaFold. Nature 596:583–589.
DOI: https://doi.org/10.1038/s41586-021-03819-2, PMID: 34265844
Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M,
Welchman DP, Zipperlen P, Ahringer J. 2003. Systematic functional analysis of the Caenorhabditis elegans
genome using RNAi. Nature 421:231–237. DOI: https://doi.org/10.1038/nature01278, PMID: 12529635
Kar FM, Hochwagen A. 2021. Phospho-Regulation of Meiotic Prophase. Frontiers in Cell and Developmental
Biology 9:667073. DOI: https://doi.org/10.3389/fcell.2021.667073, PMID: 33928091
Karman Z, Rethi-Nagy Z, Abraham E, Fabri-Ordogh L, Csonka A, Vilmos P, Debski J, Dadlez M, Glover DM,
Lipinszki Z. 2020. Novel perspectives of target-binding by the evolutionarily conserved PP4 phosphatase. Open
Biology 10:200343. DOI: https://doi.org/10.1098/rsob.200343, PMID: 33352067
Guo et al. eLife 2022;11:e77956. DOI: https://doi.org/10.7554/eLife.77956
27 of 30
A Self-archived copy in
Kyoto University Research Information Repository
https://repository.kulib.kyoto-u.ac.jp
Cell Biology | Genetics and Genomics
Research article
Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in
performance and usability. Molecular Biology and Evolution 30:772–780. DOI: https://doi.org/10.1093/molbev/
mst010, PMID: 23329690
Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, Keeney S. 2013. Numerical constraints and feedback control of
double-strand breaks in mouse meiosis. Genes & Development 27:873–886. DOI: https://doi.org/10.1101/gad.
213652.113, PMID: 23599345
Keeney S, Giroux CN, Kleckner N. 1997. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a
member of a widely conserved protein family. Cell 88:375–384. DOI: https://doi.org/10.1016/s0092-8674(00)
81876-0, PMID: 9039264
Keogh MC, Kim JA, Downey M, Fillingham J, Chowdhury D, Harrison JC, Onishi M, Datta N, Galicia S, Emili A,
Lieberman J, Shen X, Buratowski S, Haber JE, Durocher D, Greenblatt JF, Krogan NJ. 2006. A phosphatase
complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature 439:497–
501. DOI: https://doi.org/10.1038/nature04384, PMID: 16299494
Kim JA, Hicks WM, Li J, Tay SY, Haber JE. 2011. Protein phosphatases pph3, ptc2, and ptc3 play redundant roles
in DNA double-strand break repair by homologous recombination. Molecular and Cellular Biology 31:507–516.
DOI: https://doi.org/10.1128/MCB.01168-10, PMID: 21135129
Kim S, Peterson SE, Jasin M, Keeney S. 2016. Mechanisms of germ line genome instability. Seminars in Cell &
Developmental Biology 54:177–187. DOI: https://doi.org/10.1016/j.semcdb.2016.02.019, PMID: 26880205
Kleckner N. 1996. Meiosis: how could it work? PNAS 93:8167. DOI: https://doi.org/10.1073/pnas.93.16.8167
Kumar R, Ghyselinck N, Ishiguro KI, Watanabe Y, Kouznetsova A, Höög C, Strong E, Schimenti J, Daniel K,
Toth A, Massy B. 2015. MEI4 – a central player in the regulation of meiotic DNA double-strand break formation
in the mouse. Journal of Cell Science 128:1800–1811. DOI: https://doi.org/10.1242/jcs.165464
Kumar R, Oliver C, Brun C, Juarez-Martinez AB, Tarabay Y, Kadlec J, Massy B. 2018. Mouse REC114 is essential
for meiotic DNA double-strand break formation and forms a complex with MEI4. Life Sci Alliance
1:e201800259. DOI: https://doi.org/10.26508/lsa.201800259
Lange J, Pan J, Cole F, Thelen MP, Jasin M, Keeney S. 2011. ATM controls meiotic double-strand-break
formation. Nature 479:237–240. DOI: https://doi.org/10.1038/nature10508, PMID: 22002603
Lee JH, Paull TT. 2004. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science
304:93–96. DOI: https://doi.org/10.1126/science.1091496, PMID: 15064416
Lee DH, Pan Y, Kanner S, Sung P, Borowiec JA, Chowdhury D. 2010. A PP4 phosphatase complex
dephosphorylates RPA2 to facilitate DNA repair via homologous recombination. Nature Structural & Molecular
Biology 17:365–372. DOI: https://doi.org/10.1038/nsmb.1769, PMID: 20154705
Letunic I, Bork P. 2016. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of
phylogenetic and other trees. Nucleic Acids Research 44:W242–W245. DOI: https://doi.org/10.1093/nar/
gkw290, PMID: 27095192
Li J, Hooker GW, Roeder GS. 2006. Saccharomyces cerevisiae Mer2, Mei4 and Rec114 form a complex required
for meiotic double-strand break formation. Genetics 173:1969–1981. DOI: https://doi.org/10.1534/genetics.
106.058768, PMID: 16783010
Li W, Yanowitz JL. 2019. Atm and atr influence meiotic crossover formation through antagonistic and overlapping
functions in Caenorhabditis elegans Genetics 212:431–443. DOI: https://doi.org/10.1534/genetics.119.302193,
PMID: 31015193
Liu H, Gordon SG, Rog O. 2021. Heterologous synapsis in C. elegans is regulated by meiotic double-strand
breaks and crossovers. Chromosoma 130:237–250. DOI: https://doi.org/10.1007/s00412-021-00763-y, PMID:
34608541
Lukaszewicz A, Lange J, Keeney S, Jasin M. 2018. Control of meiotic double-strand-break formation by ATM:
local and global views. Cell Cycle 17:1155–1172. DOI: https://doi.org/10.1080/15384101.2018.1464847, PMID:
29963942
Lukaszewicz A, Lange J, Keeney S, Jasin M. 2021. De novo deletions and duplications at recombination
hotspots in mouse germlines. Cell 184:5970-5984.. DOI: https://doi.org/10.1016/j.cell.2021.10.025, PMID:
34793701
Machovina TS, Mainpal R, Daryabeigi A, McGovern O, Paouneskou D, Labella S, Zetka M, Jantsch V,
Yanowitz JL. 2016. A surveillance system ensures crossover formation in C. elegans. Current Biology 26:2873–
2884. DOI: https://doi.org/10.1016/j.cub.2016.09.007, PMID: 27720619
MacQueen AJ, Villeneuve AM. 2001. Nuclear reorganization and homologous chromosome pairing during
meiotic prophase require C. elegans chk-2. Genes & Development 15:1674–1687. DOI: https://doi.org/10.
1101/gad.902601, PMID: 11445542
MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, Dernburg AF. 2005. Chromosome sites play dual
roles to establish homologous synapsis during meiosis in C. elegans. Cell 123:1037–1050. DOI: https://doi.org/
10.1016/j.cell.2005.09.034, PMID: 16360034
Maleki S, Neale MJ, Arora C, Henderson KA, Keeney S. 2007. Interactions between Mei4, Rec114, and other
proteins required for meiotic DNA double-strand break formation in Saccharomyces cerevisiae. Chromosoma
116:471–486. DOI: https://doi.org/10.1007/s00412-007-0111-y, PMID: 17558514
Malone RE, Bullard S, Hermiston M, Rieger R, Cool M, Galbraith A. 1991. Isolation of mutants defective in early
steps of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics 128:79–88. DOI: https://doi.
org/10.1093/genetics/128.1.79, PMID: 2060778
Guo et al. eLife 2022;11:e77956. DOI: https://doi.org/10.7554/eLife.77956
28 of 30
A Self-archived copy in
Kyoto University Research Information Repository
https://repository.kulib.kyoto-u.ac.jp
Cell Biology | Genetics and Genomics
Research article
McKim KS, Green-Marroquin BL, Sekelsky JJ, Chin G, Steinberg C, Khodosh R, Hawley RS. 1998. Meiotic
synapsis in the absence of recombination. Science 279:876–878. DOI: https://doi.org/10.1126/science.279.
5352.876, PMID: 9452390
Menees TM, Roeder GS. 1989. MEI4, a yeast gene required for meiotic recombination. Genetics 123:675–682.
DOI: https://doi.org/10.1093/genetics/123.4.675, PMID: 2693205
Mets DG, Meyer BJ. 2009. Condensins regulate meiotic DNA break distribution, thus crossover frequency, by
controlling chromosome structure. Cell 139:73–86. DOI: https://doi.org/10.1016/j.cell.2009.07.035, PMID:
19781752
Mirdita M, Schütze K, Moriwaki Y, Heo L, Ovchinnikov S, Steinegger M. 2021. ColabFold - Making Protein
Folding Accessible to All. bioRxiv. DOI: https://doi.org/10.1101/2021.08.15.456425
Miyazaki T, Bressan DA, Shinohara M, Haber JE, Shinohara A. 2004. In vivo assembly and disassembly of Rad51
and Rad52 complexes during double-strand break repair. The EMBO Journal 23:939–949. DOI: https://doi.org/
10.1038/sj.emboj.7600091, PMID: 14765116
Mohibullah N, Keeney S. 2016. Numerical and spatial patterning of yeast meiotic DNA breaks by Tel1. Genome
Research 27:278–288. DOI: https://doi.org/10.1101/gr.213587.116
Molnar M, Parisi S, Kakihara Y, Nojima H, Yamamoto A, Hiraoka Y, Bozsik A, Sipiczki M, Kohli J. 2001.
Characterization of rec7, an early meiotic recombination gene in Schizosaccharomyces pombe. Genetics
157:519–532. DOI: https://doi.org/10.1093/genetics/157.2.519, PMID: 11156975
Nadarajan S, Lambert TJ, Altendorfer E, Gao J, Blower MD, Waters JC, Colaiácovo MP. 2017. Polo-like kinase-
dependent phosphorylation of the synaptonemal complex protein SYP-4 regulates double-strand break
formation through a negative feedback loop. eLife 6:e23437. DOI: https://doi.org/10.7554/eLife.23437, PMID:
28346135
Nageswaran DC, Kim J, Lambing C, Kim J, Park J, Kim EJ, Cho HS, Kim H, Byun D, Park YM, Kuo P, Lee S,
Tock AJ, Zhao X, Hwang I, Choi K, Henderson IR. 2021. High crossover rate1 encodes protein phosphatase x1
and restricts meiotic crossovers in arabidopsis. Nature Plants 7:452–467. DOI: https://doi.org/10.1038/
s41477-021-00889-y, PMID: 33846593
Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. 2015. IQ-TREE: a fast and effective stochastic algorithm for
estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32:268–274. DOI: https://doi.
org/10.1093/molbev/msu300, PMID: 25371430
Oates ME, Romero P, Ishida T, Ghalwash M, Mizianty MJ, Xue B, Dosztányi Z, Uversky VN, Obradovic Z,
Kurgan L, Dunker AK, Gough J. 2013. D2D2D. Nucleic Acids Research 41:D508–D516. DOI: https://doi.org/10.
1093/nar/gks1226, PMID: 23203878
Otsu N. 1975. A threshold selection method from gray-level histograms. Automatica 11:23–27. DOI: https://doi.
org/10.1109/TSMC.1979.4310076
Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, Shirahige K, Klein F. 2011. Spo11-accessory proteins
link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 146:372–383. DOI:
https://doi.org/10.1016/j.cell.2011.07.003, PMID: 21816273
Pattabiraman D, Roelens B, Woglar A, Villeneuve AM. 2017. Meiotic recombination modulates the structure and
dynamics of the synaptonemal complex during C. elegans meiosis. PLOS Genetics 13:e1006670. DOI: https://
doi.org/10.1371/journal.pgen.1006670, PMID: 28339470
Phillips CM, Dernburg AF. 2006. A family of zinc-finger proteins is required for chromosome-specific pairing and
synapsis during meiosis in C. elegans. Developmental Cell 11:817–829. DOI: https://doi.org/10.1016/j.devcel.
2006.09.020, PMID: 17141157
Phillips CM, McDonald KL, Dernburg AF. 2009. Cytological analysis of meiosis in Caenorhabditis elegans.
Methods in Molecular Biology 558:171–195. DOI: https://doi.org/10.1007/978-1-60761-103-5_11, PMID:
19685325
Raices M, Bowman R, Smolikove S, Yanowitz JL. 2021. Aging negatively impacts dna repair and bivalent
formation in the C. elegans germ line. Frontiers in Cell and Developmental Biology 9:695333. DOI: https://doi.
org/10.3389/fcell.2021.695333, PMID: 34422819
Roeder GS. 1995. Sex and the single cell: meiosis in yeast. PNAS 92:10450–10456. DOI: https://doi.org/10.
1073/pnas.92.23.10450
Roeder GS, Bailis JM. 2000. The pachytene checkpoint. Trends in Genetics 16:395–403. DOI: https://doi.org/10.
1016/s0168-9525(00)02080-1, PMID: 10973068
Roelens B, Schvarzstein M, Villeneuve AM. 2015. Manipulation of karyotype in Caenorhabditis elegans reveals
multiple inputs driving pairwise chromosome synapsis during meiosis. Genetics 201:1363–1379. DOI: https://
doi.org/10.1534/genetics.115.182279, PMID: 26500263
Romanienko PJ, Camerini-Otero RD. 2000. The mouse Spo11 gene is required for meiotic chromosome
synapsis. Molecular Cell 6:975–987. DOI: https://doi.org/10.1016/s1097-2765(00)00097-6, PMID: 11106738
Rosu S, Zawadzki KA, Stamper EL, Libuda DE, Reese AL, Dernburg AF, Villeneuve AM. 2013. The C. elegans
DSB-2 protein reveals a regulatory network that controls competence for meiotic DSB formation and promotes
crossover assurance. PLOS Genetics 9:e1003674. DOI: https://doi.org/10.1371/journal.pgen.1003674
Sato-Carlton A, Li X, Crawley O, Testori S, Martinez-Perez E, Sugimoto A, Carlton PM. 2014. Protein
phosphatase 4 promotes chromosome pairing and synapsis, and contributes to maintaining crossover
competence with increasing age. PLOS Genetics 10:e1004638. DOI: https://doi.org/10.1371/journal.pgen.
1004638, PMID: 25340746
Sato-Carlton A, Nakamura-Tabuchi C, Li X, Boog H, Lehmer MK, Rosenberg SC, Barroso C, Martinez-Perez E,
Corbett KD, Carlton PM. 2020. Phosphoregulation of HORMA domain protein HIM-3 promotes asymmetric
Guo et al. eLife 2022;11:e77956. DOI: https://doi.org/10.7554/eLife.77956
29 of 30
A Self-archived copy in
Kyoto University Research Information Repository
https://repository.kulib.kyoto-u.ac.jp
Cell Biology | Genetics and Genomics
Research article
synaptonemal complex disassembly in meiotic prophase in Caenorhabditis elegans. PLOS Genetics
16:e1008968. DOI: https://doi.org/10.1371/journal.pgen.1008968, PMID: 33175901
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S,
Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A. 2012. Fiji: an open-source
platform for biological-image analysis. Nature Methods 9:676–682. DOI: https://doi.org/10.1038/nmeth.2019,
PMID: 22743772
Stamper EL, Rodenbusch SE, Rosu S, Ahringer J, Villeneuve AM, Dernburg AF. 2013. Identification of DSB-1, a
protein required for initiation of meiotic recombination in Caenorhabditis elegans, illuminates a crossover
assurance checkpoint. PLOS Genetics 9:e1003679. DOI: https://doi.org/10.1371/journal.pgen.1003679, PMID:
23990794
Steinegger M. 2022. ColabFold. v1.3.0. GitHub. https://github.com/sokrypton/ColabFold
Stevens L, Félix MA, Beltran T, Braendle C, Caurcel C, Fausett S, Fitch D, Frézal L, Gosse C, Kaur T, Kiontke K,
Newton MD, Noble LM, Richaud A, Rockman MV, Sudhaus W, Blaxter M. 2019. Comparative genomics of 10
new Caenorhabditis species. Evol Lett 3:217–236. DOI: https://doi.org/10.1002/evl3.110
Sumiyoshi E, Sugimoto A, Yamamoto M. 2002. Protein phosphatase 4 is required for centrosome maturation in
mitosis and sperm meiosis in C. elegans. Journal of Cell Science 115:1403–1410. DOI: https://doi.org/10.1242/
jcs.115.7.1403, PMID: 11896188
Tessé S, Storlazzi A, Kleckner N, Gargano S, Zickler D. 2003. Localization and roles of Ski8p protein in Sordaria
meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition. PNAS
100:12865–12870. DOI: https://doi.org/10.1073/pnas.2034282100, PMID: 14563920
Tessé S, Bourbon HM, Debuchy R, Budin K, Dubois E, Liangran Z, Antoine R, Piolot T, Kleckner N, Zickler D,
Espagne E. 2017. Asy2/Mer2: an evolutionarily conserved mediator of meiotic recombination, pairing, and
global chromosome compaction. Genes & Development 31:1880–1893. DOI: https://doi.org/10.1101/gad.
304543.117, PMID: 29021238
Ueki Y, Kruse T, Weisser MB, Sundell GN, Larsen MSY, Mendez BL, Jenkins NP, Garvanska DH, Cressey L,
Zhang G, Davey N, Montoya G, Ivarsson Y, Kettenbach AN, Nilsson J. 2019. A consensus binding motif for the
pp4 protein phosphatase. Molecular Cell 76:953–964. DOI: https://doi.org/10.1016/j.molcel.2019.08.029,
PMID: 31585692
UniProt Consortium. 2021. UniProt: the universal protein knowledgebase in 2021. Nucleic Acids Research
49:D480–D489. DOI: https://doi.org/10.1093/nar/gkaa1100
Uziel T, Lerenthal Y, Moyal L, Andegeko Y, Mittelman L, Shiloh Y. 2003. Requirement of the MRN complex for
ATM activation by DNA damage. The EMBO Journal 22:5612–5621. DOI: https://doi.org/10.1093/emboj/
cdg541, PMID: 14532133
Villoria MT, Gutiérrez-Escribano P, Alonso-Rodríguez E, Ramos F, Merino E, Campos A, Montoya A, Kramer H,
Aragón L, Clemente-Blanco A. 2019. PP4 phosphatase cooperates in recombinational DNA repair by
enhancing double-strand break end resection. Nucleic Acids Research 47:10706–10727. DOI: https://doi.org/
10.1093/nar/gkz794, PMID: 31544936
Yadav VK, Claeys Bouuaert C. 2021. Mechanism and control of meiotic dna double-strand break formation in S.
cerevisiae. Frontiers in Cell and Developmental Biology 9:642737. DOI: https://doi.org/10.3389/fcell.2021.
642737, PMID: 33748134
Zhang L, Kim KP, Kleckner NE, Storlazzi A. 2011. Meiotic double-strand breaks occur once per pair of (sister)
chromatids and, via Mec1/ATR and Tel1/ATM, once per quartet of chromatids. PNAS 108:20036–20041. DOI:
https://doi.org/10.1073/pnas.1117937108, PMID: 22123968
Zhang L, Ward JD, Cheng Z, Dernburg AF. 2015. The auxin-inducible degradation (AID) system enables versatile
conditional protein depletion in C. elegans. Development 142:4374–4384. DOI: https://doi.org/10.1242/dev.
129635, PMID: 26552885
Guo et al. eLife 2022;11:e77956. DOI: https://doi.org/10.7554/eLife.77956
30 of 30
...