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Meiotic Recombination. The Metabolic Pathways from DNA Double-Strand Breaks to Crossing Over and Chiasmata

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Abstract

The coupled phenomena of DNA repair and recombination serve as a molecular basis of the universal mechanism of meiosis, which was formed in the course of evolution of eukaryotic sexual reproduction. This review examines findings from the studies of chromosomal DNA metabolism pathways leading from initial molecular events to crossing over and then to chiasmata. The last are necessary for the homologous chromosome segregation during meiosis and transformation of diploid cells into haploid gametes or spores. The historical roots are described of the theory of homologous recombination based on the hypothesis of DNA double-strand breaks repair and the experimental discovery of the “core” protein set: SPO11, RAD51, ZMM complex and other proteins responsible for meiotic recombination in most eukaryotes. Attention is drawn to known exceptions to these patterns and possible ways to explain them. The theory of two types of crossing over, i.e., dependent and independent of its interference, is described. The current results of experimental studies on the role of meiosis-specific recombination proteins at all stages of meiosis are described. The hypotheses of crossing over homeostasis and the mechanism of its interference are considered.

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Notes

  1. In all organisms, except yeast, abbreviated designations of proteins are usually given in capital letters.

REFERENCES

  1. Keeney, S., Mechanism and control of meiotic recombination initiation, Curr. Top. Dev. Biol., 2001, vol. 52, pp. 1—53.

    Article  CAS  PubMed  Google Scholar 

  2. Marcon, E. and Moens, P.B., The evolution of meiosis: recruitment and modification of somatic DNA-repair proteins, BioEssay, 2005, vol. 27, pp. 795—808. https://doi.org/10.1002/bies.20264

    Article  CAS  Google Scholar 

  3. Loidl, J., Conservation and variability of meiosis across the eukaryotes, Annu. Rev. Genet., 2016, vol. 50, pp. 293—316. https://doi.org/10.1146/annurev-genet-120215-035100

    Article  CAS  PubMed  Google Scholar 

  4. Bogdanov, Yu.F., Dadashev, S.Ya., and Grishaeva, T.M., Comparative genomics and proteomics of Drosophila, Brenner’s nematode, and Arabidopsis: identification of functionally similar genes and proteins of meiotic chromosome synapsis, Russ. J. Genet., 2002, vol. 38, no. 8, pp. 908—917. https://doi.org/10.1023/A:1016883711260

    Article  CAS  Google Scholar 

  5. Bogdanov, Yu.F., Dadashev, S.Ya., and Grishaeva, T.M., In silico search for functionally similar proteins involved in meiosis and recombination in evolutionarily distant organisms, In Silico Biol., 2003, vol. 3, nos. 1—2, pp. 173—185.

    CAS  PubMed  Google Scholar 

  6. Bogdanov, Yu.F., Grishaeva, T.M., and Dadashev, S.Ya., Similarity of the domain structure of proteins as a basis for the evolutionarily conservation of meiosis, Int. Rev. Cytol., 2007, vol. 257, pp. 83—142. https://doi.org/10.1016/S0074-7696(07)57003-8

    Article  CAS  PubMed  Google Scholar 

  7. Youds, J.L. and Boulton, S.J., The choice in meiosis—defining the factors that influence crossover or non-crossover formation, J. Cell Sci., 2011, vol. 124, pp. 501—513. https://doi.org/10.1242/jcs.074427

    Article  CAS  PubMed  Google Scholar 

  8. Bogdanov, Yu.F., Variation and evolution of meiosis, Russ. J. Genet., 2003, vol. 39, no. 4, pp. 363–381. https://doi.org/10.1023/A:1023345311889

    Article  CAS  Google Scholar 

  9. Bogdanov, Yu.F., Noncanonical meiosis in the nematode Caenorhabditis elegans as a model for studying the molecular bases of the homologous chromosome synapsis, crossing over, and segregation, Russ. J. Genet., 2017, vol. 53, no. 12, pp. 1283—1298. https://doi.org/10.1134/S102279541712002X

    Article  CAS  Google Scholar 

  10. Grishaeva, T.M. and Bogdanov, Yu.F., The genetic control of meiosis in Drosophila,Russ. J. Genet., 2000, vol. 36, no. 10, pp. 1301—1321.

    CAS  Google Scholar 

  11. Grishaeva, T.M. and Bogdanov, Yu.F., Peculiarities of meiosis in Drosophila: a classical object of genetics has nonstandard meiosis, Biol. Bull. Rev., 2018, vol. 138, no. 1, pp. 68—82. https://doi.org/10.1134/S2079086418040047

    Article  Google Scholar 

  12. Simanovskii, S.A. and Bogdanov, Yu.F., Genetic control of meiosis in plants, Russ. J. Genet., 2018, vol. 54, no. 4, pp. 389—402. https://doi.org/10.1134/S1022795418030122

    Article  Google Scholar 

  13. Turner, J.M., Meiosis 2007—where have we got to and where are we going?, Chromosome Res., 2007, vol. 15, pp. 517—521. https://doi.org/10.1007/s10577-007-1152-z

    Article  CAS  PubMed  Google Scholar 

  14. Harigaya, Y. and Yamamoto, M., Molecular mechanisms underlying the mitosis—meiosis decision, Chromosome Res., 2007, vol. 15, pp. 523—537. https://doi.org/10.1007/s10577-007-1151-0

    Article  CAS  PubMed  Google Scholar 

  15. Matson, C.K., Murphy, M.W., Griswold, M.D., et al., The mammalian doublesex homolog DMRT1 is a transcriptional gatekeeper that controls the mitosis versus meiosis decision in male germ cells, Dev. Cell, 2010, vol. 19, pp. 612—624. https://doi.org/10.1016/j.devcel.2010.09.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Schwacha, A. and Kleckner, N., Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis, Cell, 1994, vol. 76, pp. 51—63.

    Article  CAS  PubMed  Google Scholar 

  17. Schwacha, A. and Kleckner, N., Identification of double Holliday junctions as intermediates in meiotic recombination, Cell, 1995, vol. 83, pp. 783—791.

    Article  CAS  PubMed  Google Scholar 

  18. Gray, S. and Cohen, P.E., Control of meiotic crossovers: from double-strand break formation to designation, Annu. Rev. Genet., 2016, vol. 50, pp. 175—210. https://doi.org/10.1146/annurev-genet-120215-035111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Allers, T. and Lichten, M., Differential timing and control of noncrossover and crossover recombination during meiosis, Cell, 2001, vol. 106, pp. 47—57. https://doi.org/10.1016/S0092-8674(01)00416-0

    Article  CAS  PubMed  Google Scholar 

  20. Zickler, D. and Kleckner, N., Recombination, pairing, and synapsis of homologs during meiosis, Cold Spring Harbor Perspect. Biol., 2015, vol. 7. pii: a016626. https://doi.org/10.1101/cshperspect.a016626

    Article  CAS  Google Scholar 

  21. Taylor, J.H., Woods, P.S., and Hughes, W.I., The organization and duplication of chromosomes as revealed by autoradiographic studies using tritium-labeled thymidine, Proc. Natl. Acad. Sci. U.S.A., 1957, vol. 43, pp. 122—128.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Jones, G.H., The control of chiasma distribution, Symp. Soc. Exp. Biol., 1984, vol. 38, pp. 293—320.

    CAS  PubMed  Google Scholar 

  23. Zakharov, A.F. and Egolina, N.A., Differential spiralization along mammalian chromosomes: 1. BrdU-revealed differentiation in Chinese hamster chromosomes, Chromosoma (Berlin), 1972, vol. 38, pp. 341—365.

    Article  CAS  PubMed  Google Scholar 

  24. Perry, P. and Wolff, S., New Giemsa method for the differential staining of sister chromatids, Nature, 1974, vol. 251, pp. 156—158.

    Article  CAS  PubMed  Google Scholar 

  25. Holliday, R., A mechanism for gene conversion in fungi, Genet. Res., 1964, vol. 78, pp. 282—304.

    Article  Google Scholar 

  26. Stahl, F.W., The Holliday junction on its thirtieth anniversary, Genetics, 1994, vol. 138, pp. 241—246.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Szostak, J.W., Orr-Weaver, T.L., Rothstein, R.J., and Stahl, F.W., Double-strand-break repair model for recombination, Cell, 1983, vol. 33, pp. 25—35.

    Article  CAS  PubMed  Google Scholar 

  28. Kohl, K.P. and Sekelsky, J., Meiotic and mitotic recombination in meiosis, Genetics, 2013, vol. 194, pp. 327—334. https://doi.org/10.1534/genetics.113.150581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Pochart, P., Woltering, D., and Hollingsworth, N.M., Conserved properties between functionally distinct MutS homologs in yeast, J. Biol. Chem., 1997, vol. 272, pp. 30345—30349.

    Article  CAS  PubMed  Google Scholar 

  30. Ross-Macdonald, P. and Roeder, G.S., Mutation of a meiosis-specific MutS homolog decreases crossing over but not mismatch correction, Cell, 1994, vol. 79, pp. 1069—1080.

    Article  CAS  PubMed  Google Scholar 

  31. Hollingsworth, N.M., Ponte, L., and Halsey, C., MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair, Genes Dev., 1995, vol. 9, pp. 1728—1739.

    Article  CAS  PubMed  Google Scholar 

  32. Zalevsky, J., MacQueen, A.J., Duffy, J.B., et al., Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast, Genetics, 1999, vol. 153, pp. 1271—1283.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Kelly, K.O., Dernburg, A.F., Stanfield, G.M., and Villeneuve, A.M., Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis, Genetics, 2000, vol. 156, pp. 617—630.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Kohl, K.P., Jones, C.D., and Sekelsky, J., Evolution of an MCM complex in flies that promotes meiotic crossovers by blocking BLM helicase, Science, 2012, vol. 338, pp. 1363—1365. https://doi.org/10.1126/science.1228190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Villeneuve, A.M. and Hillers, K.J., Whence meiosis?, Cell, 2001, vol. 106, pp. 647—650.

    Article  CAS  PubMed  Google Scholar 

  36. Boddy, M.N., Gaillard, P.H., McDonald, W.H., et al., Mus81-Eme1 are essential components of a Holliday junction resolvase, Cell, 2001, vol. 107, pp. 537—548.

    Article  CAS  PubMed  Google Scholar 

  37. Smith, G.R., Boddy, M.N., Shanahan, P., and Russell, P., Fission yeast Mus81-Emel Holliday junction resolvase is required for meiotic crossing over but not for gene conversion, Genetics, 2003, vol. 165, pp. 2289—2293.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Argueso, J.L., Wanat, J., Gemici, Z., and Alani, E., Competing crossover pathways act during meiosis in Saccharomyces cerevisiae,Genetics, 2004, vol. 168, pp. 1805—1816. https://doi.org/10.1534/genetics.104.032912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. de los Santos, T., Hunter, N., Lee, C., et al., The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast, Genetics, 2003, vol. 164, pp. 81—94.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Berchowitz, L.E., Francis, K.E., Bey, A.L., and Copenhaver, G.P., The role of AtMUS81 in interference-insensitive crossovers in A. thaliana,PLoS Genet., 2007, vol. 3. e132. https://doi.org/10.1371/journal.pgen.0030132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Munz, P., An analysis of interference in the fission yeast Schizosaccharomyces pombe,Genetics, 1994, vol. 137, pp. 701—707.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Sekelsky, J., Brodsky, M.H., and Burtis, K.C., DNA repair in Drosophila: insights from the Drosophila genome sequence, J. Cell Biol., 2000, vol. 150, pp. F31—F36.

    Article  CAS  PubMed  Google Scholar 

  43. Keeney, S., Giroux, C.N., and Kleckner, N., Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family, Cell, 1997, vol. 88, pp. 375—384.

    Article  CAS  PubMed  Google Scholar 

  44. Romanienko, P.J. and Camerini-Otero, R.D., The mouse Spo11 gene is required for meiotic chromosome synapsis, Mol. Cell, 2000, vol. 6, pp. 975—987.

    Article  CAS  PubMed  Google Scholar 

  45. Grelon, M., Vezon, D., Gendrot, G., and Pelletier, G., AtSPO11-1 is necessary for efficient meiotic recombination in plants, EMBO J., 2001, vol. 20, pp. 589—600. https://doi.org/10.1093/emboj/20.3.589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Phadnis, N., Hyppa, R.W., and Smith, G.R., New and old ways to control meiotic recombination, Trends Genet., 2011, vol. 27, pp. 411—421. https://doi.org/10.1016/j.tig.2011.06.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Mézard, C., Jahns, M.T., and Grelon, M., Where to cross? New insights into the location of meiotic crossovers, Trends Genet., 2015, vol. 31, pp. 393—401. https://doi.org/10.1016/j.tig.2015.03.008

    Article  CAS  PubMed  Google Scholar 

  48. Székvőlgyi, L., Ohta, K., and Nicokas, A., Initiation of meiotic homologous recombination: flexibility, impact of histone modifications, and chromatin remodeling, Cold Spring Harbor Perspect. Biol., 2015, vol. 7. a016527. https://doi.org/10.1101/cshperspect.a016527

    Article  CAS  Google Scholar 

  49. Mehrotra, S. and McKim, K.S., Temporal analysis of meiotic DNA double-strand break formation and repair in Drosophila females, PLoS Genet., 2006, vol. 2. e200. https://doi.org/10.1371/journal.pgen.0020200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lambing, C., Tock, A.J., Choi, K., et al., REC8-cohesin, chromatin and transcription orchestrate meiotic recombination in the Arabidopsis genome, bioRxiv, 2019. https://doi.org/10.1101/512400

  51. Hunter, N. and Kleckner, N., The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination, Cell, 2001, vol. 106, pp. 59—70.

    Article  CAS  PubMed  Google Scholar 

  52. Fowler, K.R., Gutierrez-Velasco, S., Martín-Castellanos, C., and Smith, G.R., Protein determinants of meiotic DNA break hot spots, Mol. Cell., 2013, vol. 49, pp. 983—996. https://doi.org/10.1016/j.molcel.2013.01.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Börner, G.V., Kleckner, N., and Hunter, N., Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis, Cell, 2004, vol. 117, pp. 29—45.

    Article  PubMed  Google Scholar 

  54. Kleckner, N., Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex, Chromosoma, 2006, vol. 115, pp. 175—193. https://doi.org/10.1007/s00412-006-0055-7

    Article  PubMed  Google Scholar 

  55. Shinohara, A. and Shinohara, M., Roles of RecA homologues Rad51 and Dmc1 during meiotic recombination, Cytogenet. Genome Res., 2004, vol. 107, pp. 201—207. https://doi.org/10.1159/000080598

    Article  CAS  PubMed  Google Scholar 

  56. West, S.C., Molecular views of recombination proteins and their control, Nature Rev., 2003, vol. 4, pp. 435—445. https://doi.org/10.1038/nrm1127

    Article  CAS  Google Scholar 

  57. Blat, Y., Protacio, R.U., Hunter, N., and Kleckner, N., Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation, Cell, 2002, vol. 111, pp. 791—802.

    Article  CAS  PubMed  Google Scholar 

  58. Zickler, D. and Kleckner, N., The leptotene to zygotene transition of meiosis, Annu. Rev. Genet., 1998, vol. 32, pp. 619—697.

    Article  CAS  PubMed  Google Scholar 

  59. Moses, M.J., Microspreading and synaptonemal complex in cytogenetic study, Chromosomes Today, 1977, vol. 6, pp. 71—82.

    Google Scholar 

  60. Bogdanov, Yu.F. and Kolomiets, O.L., Sinaptonemnyi kompleks—indikator dinamiki meioza i izmenchivosti khromosom (Synaptonemal Complex—an Indicator of Meiosis Dynamics and Chromosome Variation), Moscow: KMK, 2007.

  61. Bishop, D.K. and Zickler, D., Early decision; meiotic cross-over interference prior to stable strand exchange and synapsis, Cell, 2004, vol. 117, pp. 9—15.

    Article  CAS  PubMed  Google Scholar 

  62. Lynn, A., Soucek, R., and Börner, G.V., ZMM proteins during meiosis: crossover artists at work, Chromosome Res., 2007, vol. 15, pp. 591—605. https://doi.org/10.1007/s10577-007-1150-1

    Article  CAS  PubMed  Google Scholar 

  63. Agarwal, S. and Roeder, G.S., Zip3 provides a link between recombination enzymes and synaptonemal complex proteins, Cell, 2000, vol. 102, pp. 245—255.

    Article  CAS  PubMed  Google Scholar 

  64. Tsubouchi, T., Zhao, H., and Roeder, G.S., The meiosis-specific Zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with Zip2, Dev. Cell, 2006, vol. 10, pp. 809—819. https://doi.org/10.1016/j.devcel.2006.04.003

    Article  CAS  PubMed  Google Scholar 

  65. Paquis-Flucklinger, V., Santucci-Darmanin, S., Paul, R., et al., Cloning and expression analysis of a meiosis-specific MutS homolog: the human MSH4 gene, Genomics, 1997, vol. 44, pp. 188—194.

    Article  CAS  PubMed  Google Scholar 

  66. Bocker, T., Barusevicius, A., Snowden, T., et al., Hmsh5: a human MutS homologue that forms a novel heterodimer with hMSH4 and is expressed during spermatogenesis, Cancer Res., 1999, vol. 59, pp. 816—822.

    CAS  PubMed  Google Scholar 

  67. Santucci-Darmanin, S., Walpita, D., Lespinasse, F., et al., MSH4 acts in conjunction with MLH1 during mammalian meiosis, FASEB J., 2000, vol. 14, pp. 1539—1547.

    Article  CAS  PubMed  Google Scholar 

  68. Grishaeva, T.M. and Bogdanov, Yu.F., Evolutionary conservation of recombination proteins and variability of meiosis-specific proteins of chromosomes, Russ. J. Genet., 2017, vol. 53, no. 5, pp. 542—550. https://doi.org/10.1134/S1022795417040081

    Article  CAS  Google Scholar 

  69. Grishaeva, T.M. and Bogdanov, Yu.F., Conservation of meiosis-specific nuclear proteins in eukaryotes: a comparative approach, Nucleus, 2018, vol. 61, no. 3, pp. 175—182. https://doi.org/10.1007/s13237-018-0253-8

    Article  Google Scholar 

  70. Muller, H., The mechanism of crossing-over, Am. Nat., 1916, vol. 50, pp. 193—221.

    Article  Google Scholar 

  71. Forejt, J., X-inactivation and its role in mail sterility, Chromosomes Today, 1984, vol. 8, pp. 17—22.

    Google Scholar 

  72. Rodionov, A.V., Chelysheva, L.A., Solovei, I.V., and Miakoshina, Y.U., Chiasma distribution in the lampbrush chromosomes of the chicken Gallus gallus domesticus: hotspots of recombination and their possible role in the proper disjunction of homologous chromosomes at the first meiotic division, Russ. J. Genet., 1992, vol. 28, no. 7, pp. 151—160.

    CAS  Google Scholar 

  73. Rodionov, A.V., Micro vs. macro: review of structure and functions of avian micro- and macro-chromosomes, Russ. J. Genet., 1996, vol. 32, no. 5, pp. 517—527.

    CAS  Google Scholar 

  74. Chen, S.Y., Tsubouchi, T., Rockmill, B., et al., Global analysis of the meiotic crossover landscape, Dev. Cell, 2008, vol. 15, pp. 401—415. https://doi.org/10.1016/j.devcel.2008.07.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. de Boer, E. and Heyting, C., The diverse roles of transverse filaments of synaptonemal complexes in meiosis, Chromosoma, 2006, vol. 115, pp. 220—234. https://doi.org/10.1007/s00412-006-0057-5

    Article  PubMed  Google Scholar 

  76. Shinohara, M., Oh, S.D., Hunter, N., and Shinohara, A., Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis, Nat. Genet., 2008, vol. 40, pp. 299—309. https://doi.org/10.1038/ng.83

    Article  CAS  PubMed  Google Scholar 

  77. Tung, K.S. and Roeder, G.S., Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae,Genetics, 1998, vol. 149, pp. 817—832.

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Borodin, P.M., Gorlov, I.P., Agulnik, A.I., et al., Chromosome pairing and recombination in mice heterozygous for different translocations in chromosomes 16 and 17, Chromosoma, 1991, vol. 101, pp. 252—258.

    Article  CAS  PubMed  Google Scholar 

  79. Auger, D.L. and Sheridan, W.F., Negative crossover interference in maize translocation heterozygotes, Genetics, 2001, vol. 159, pp. 1717—1726.

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Torgasheva, A.A., Rubtsov, N.B., and Borodin, P.M., Recombination and synaptic adjustment in oocytes of mice heterozygous for a large paracentric inversion, Chromosome Res., 2013, vol. 21, pp. 37—48. https://doi.org/10.1007/s10577-012-9336-6

    Article  CAS  PubMed  Google Scholar 

  81. Martini, E., Diaz, R.L., Hunter, N., and Keeney, S., Crossover homeostasis in yeast meiosis, Cell, 2006, vol. 126, pp. 285—295. https://doi.org/10.1016/j.cell.2006.05.044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Celerin, M., Merino, S.T., Stone, J.E., et al., Multiple roles of Spo11 in meiotic chromosome behavior, EMBO J., 2000, vol. 19, pp. 2739—2750.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Henderson, K.A. and Keeney, S., Tying synaptonemal complex initiation to the formation and programmed repair of DNA double strand breaks, Proc. Natl. Acad. Sci. U.S.A., 2004, vol. 101, pp. 4519—4524. https://doi.org/10.1073/pnas.0400843101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Bhuijan, H. and Schmekel, K., Meiotic chromosome synapsis in yeast can occur without spo11-induced DNA double-strand breaks, Genetics, 2004, vol. 168, pp. 775—783. https://doi.org/10.1534/genetics.104.029660

    Article  CAS  Google Scholar 

  85. Albini, S.M. and Jones, G.H., Synaptonemal complex spreading in Allium cepa and A. fistulosum: 1. The initiation and sequence of pairing, Chromosoma, 1987, vol. 95, pp. 324—338.

    Article  Google Scholar 

  86. Tessé, S., Storlazzi, A., Kleckner, N., et al., Localization and roles of SkiSp protein in Sordaria meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition, Proc. Natl. Acad. Sci. U.S.A., 2003, vol. 100, pp. 12865—12870. https://doi.org/10.1073/pnas.2034282100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Franklin, A.E., McElver, J., Sunjevaric, I., et al., Three-dimensional microscopy of the Rad51 recombination protein during meiotic prophase, Plant Cell, 1999, vol. 11, pp. 809—824.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Tarsounas, M., Morita, T., Pearlman, R.E., and Moens, P.B., RAD51 and DMC1 form mixed complexes associated with mouse meiotic chromosome cores and synaptonemal complexes, J. Cell Biol., 1999, vol. 147, pp. 207—220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Page, S.L. and Hawley, R.S., The genetics and molecular biology of the synaptonemal complex, Annu. Rev. Cell. Dev. Biol., 2004, vol. 20, pp. 525—558. https://doi.org/10.1146/annurev.cellbio.19.111301.155141

    Article  CAS  PubMed  Google Scholar 

  90. Lorenz, A. and Whitby, M.C., How not to get cross(ed): a novel role for FANCM orthologs in meiotic recombination, Cell Cycle, 2012, vol. 11, pp. 3347—3348. https://doi.org/10.4161/cc.21844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Zakharyevich, K., Tang, S., Ma, Y., and Hunter, N., Delineation of joint molecule resolution pathways in meiosis identifies a cross-over-specific resolvase, Cell, 2012, vol. 149, pp. 334—347. https://doi.org/10.1016/j.cell.2012.03.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. De Muyt, A., Jessop, L., Kolar, E., et al., BLM helicase ortholog Sgsl is a central regulator of meiotic recombination intermediate metabolism, Mol. Cell, 2012, vol. 46, pp. 43—53. https://doi.org/10.1016/j.molcel.2012.02.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Youds, J.L., Mets, D.G., McIlwraith, M.J., et al., RTEL-1 enforces meiotic crossover interference and homeostasis, Science, 2010, vol. 327, pp. 1254—1258. https://doi.org/10.1126/science.1183112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Rosu, S., Libuda, D.E., and Villeneuve, A.M., Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number, Science, 2011, vol. 334, pp. 1286—1289. https://doi.org/10.1126/science.1212424 94a. Kauppi, L., Jasin, M., and Keeney, S., How much is enough? Control of DNA double-strand break numbers in mouse meiosis, Cell Cycle, 2013, vol. 12, pp. 2719—2720. https://doi.org/10.4161/cc.26079

  95. Baudat, F., Buard, J., Grey, C., et al., PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice, Science, 2010, vol. 327, pp. 836—840. https://doi.org/10.1126/science.1183439

    Article  CAS  PubMed  Google Scholar 

  96. Grey, C., Baudat, F., and de Massy, B., PRDM9, a driver of the genetic map, PLoS Genet., 2018, vol. 14. e1007479. https://doi.org/10.1371/journal.pgen.1007479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Kumar, R. and de Massy, B., Initiation of meiotic recombination in mammals, Genes, 2010, vol. 1, pp. 521—549. https://doi.org/10.3390/genes1030521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Cromie, G.A., Hyppa, R.W., Cam, H.P., et al., A discrete class of intergenic DNA dictates meiotic DNA break hotspots in fission yeast, PLoS Genet., 2007, vol. 3. e141. https://doi.org/10.1371/journal.pgen.0030141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Dadashev, S.Ya., Grishaeva, T.M., and Bogdanov, Yu.F., In silico identification and characterization of meiotic DNA: AluJb possibly participates in the attachment of chromatin loops to synaptonemal complex, Russ. J. Genet., 2005, vol. 41, no. 12, pp. 1419—1424. https://doi.org/10.1007/s11177-006-0016-5

    Article  CAS  Google Scholar 

  100. King, J.S. and Mortimer, R.K., A polymerization model of chiasma interference and corresponding computer simulation, Genetics, 1990, vol. 126, pp. 1127—1138.

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Kleckner, N., Zickler, D., Jones, G.H., et al., A mechanical basis for chromosome function, Proc. Natl. Acad. Sci. U.S.A., 2004, vol. 101, pp. 12592—12597.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Berchowitz, L.E., and Copenhaver, G.P., Genetic interference: don’t stand so close to me, Curr. Genomics, 2010, vol. 11, pp. 91—102. https://doi.org/10.2174/138920210790886835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Joshi, N., Barot, A., Jamison, C., and Börner, G.V., Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis, PLoS Genet., 2009, vol. 5. e1000557. https://doi.org/10.1371/journal.pgen.1000557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Herruzo, E., Ontoso, D., Gonzalez-Arranz, S., et al., The Pch2 AAA+ ATPase promotes phosphorylation of the Hop1 meiotic checkpoint adaptor in response to synaptonemal complex defects, Nucleic Acids Res., 2016, vol. 44, pp. 7722—7741. https://doi.org/10.1093/nar/gkw506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Goldman, A.S.H. and Hulten, M.A., Meiotic analysis of a human male 46,XY,t (15;20)(q11.2;q.11.2) translocation heterozygote: quadrivalent configuration, orientation and fires meiotic segregation, Chromosoma, 1993, vol. 102, pp. 102—111.

    Article  CAS  PubMed  Google Scholar 

  106. Carpenter, A.T.C., Electron microscopy of meiosis in Drosophila melanogaster females: 2. The recombination nodule—a recombination-associated structure at pachytene?, Proc. Natl. Acad. Sci. U.S.A., 1975, vol. 72, pp. 3186—3189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Holm, P.B. and Rasmussen, S.W., Three-dimensional reconstruction of meiotic chromosomes in human spermatogenesis, Chromosomes Today, 1978, vol. 6, pp. 83—93.

    Google Scholar 

  108. Bishop, D.K., RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis, Cell, 1994, vol. 79, pp. 1081—1092.

    Article  CAS  PubMed  Google Scholar 

  109. Anderson, L.K., Reeves, A., Web, L.M., and Ashley, T., Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein, Genetics, 1999, vol. 151, pp. 1569—1579.

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Anderson, L.K., Doyle, G.G., Brigham, B., et al., High-resolution crossover maps for each bivalents of Zea mays using recombination nodules, Genetics, 2003, vol. 165, pp. 849—865.

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Lisachov, A.P., Zadesenets, K.S., Rubtsov, N.B., and Borodin, P.M., Sex chromosome synapsis and recombination in male guppies, Zebrafish, 2015, vol. 12, pp. 174—180. https://doi.org/10.1089/zeb.2014.1000

    Article  CAS  PubMed  Google Scholar 

  112. Spangenberg, V., Matveevsky, S., Bogdanov, Y., et al., Reticulate evolution of the rock lizards: meiotic chromosome dynamics and spermatogenesis in diploid and triploid males of the genus Darevskia,Genes, 2017, vol. 8, pp. 2—15. https://doi.org/10.3390/genes8060149

    Article  CAS  Google Scholar 

  113. Zickler, D. and Kleckner, N., Meiotic chromosomes: integrating structure and function, Annu. Rev. Genet., 1999, vol. 33, pp. 603—754.

    Article  CAS  PubMed  Google Scholar 

  114. Kundu, S.C. and Bogdanov, Yu.F., Ultrastructural studies of late meiotic prophase nuclei of spermatocytes in Ascaris sum,Chromosoma, 1979, vol. 70, no. 3, pp. 375—384.

    Article  Google Scholar 

  115. Revenkova, E. and Jessberger, R., Keeping sister chromatids together: cohesins in meiosis, Reproduction, 2005, vol. 130, pp. 783—790. https://doi.org/10.1530/rep.1.00864

    Article  CAS  PubMed  Google Scholar 

  116. Barbero, J.L., Cohesins: chromatin architects in chromosome segregation, control of gene expression and much more, Cell. Mol. Life Sci., 2009, vol. 66, pp. 2025—2035. https://doi.org/10.1007/s00018-009-0004-8

    Article  CAS  PubMed  Google Scholar 

  117. Gutierrez-Caballero, C., Cebollero, L.R., and Pendas, A.M., Shugoshins: from protectors of cohesion to versatile adaptors at the centromere, Trends Genet., 2012, vol. 28, pp. 351—360. https://doi.org/10.1016/j.tig.2012.03.003

    Article  CAS  PubMed  Google Scholar 

  118. West, A.M.V., Rosenberg, S.C., Ur, S.N., et al., A conserved filamentous assembly underlies the structure of the meiotic chromosome axis, eLife, 2019, vol. 8. e40372. https://doi.org/10.7554/eLife.40372

    Article  PubMed  PubMed Central  Google Scholar 

  119. Prokof’eva-Bel’govskaya, A.A., Geterokhromaticheskie raiony khromosom (Heterochromatic Regions of Chromosomes), Moscow: Nauka, 1986.

  120. Elgin, S.C. and Grewal, S.I., Heterochromatin: silence is golden, Curr. Biol., 2003, vol. 13, p. R896.

    Article  CAS  Google Scholar 

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ACKNOWLEDGMENTS

We thank P.M. Borodin, A.V. Rodionov, and A.A. Torgasheva for valuable comments and suggestions.

Funding

This study was supported by the Russian Foundation for Basic Research (grant no. 17-00-00430 (17-00-00429 KOMFI)) and the state contract with the Vavilov Institute of General Genetics, Russian Academy of Sciences (no. 0112-2019-0002).

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Correspondence to Yu. F. Bogdanov.

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The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

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Translated by N. Maleeva

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Bogdanov, Y.F., Grishaeva, T.M. Meiotic Recombination. The Metabolic Pathways from DNA Double-Strand Breaks to Crossing Over and Chiasmata. Russ J Genet 56, 159–176 (2020). https://doi.org/10.1134/S1022795420020039

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