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
In all organisms, except yeast, abbreviated designations of proteins are usually given in capital letters.
REFERENCES
Keeney, S., Mechanism and control of meiotic recombination initiation, Curr. Top. Dev. Biol., 2001, vol. 52, pp. 1—53.
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
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
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
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.
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
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
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
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
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.
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
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
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
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
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
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.
Schwacha, A. and Kleckner, N., Identification of double Holliday junctions as intermediates in meiotic recombination, Cell, 1995, vol. 83, pp. 783—791.
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
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
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
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.
Jones, G.H., The control of chiasma distribution, Symp. Soc. Exp. Biol., 1984, vol. 38, pp. 293—320.
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.
Perry, P. and Wolff, S., New Giemsa method for the differential staining of sister chromatids, Nature, 1974, vol. 251, pp. 156—158.
Holliday, R., A mechanism for gene conversion in fungi, Genet. Res., 1964, vol. 78, pp. 282—304.
Stahl, F.W., The Holliday junction on its thirtieth anniversary, Genetics, 1994, vol. 138, pp. 241—246.
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.
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
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.
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.
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.
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.
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.
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
Villeneuve, A.M. and Hillers, K.J., Whence meiosis?, Cell, 2001, vol. 106, pp. 647—650.
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.
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.
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
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.
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
Munz, P., An analysis of interference in the fission yeast Schizosaccharomyces pombe,Genetics, 1994, vol. 137, pp. 701—707.
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.
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.
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.
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
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
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
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
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
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
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.
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
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.
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
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
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
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.
Zickler, D. and Kleckner, N., The leptotene to zygotene transition of meiosis, Annu. Rev. Genet., 1998, vol. 32, pp. 619—697.
Moses, M.J., Microspreading and synaptonemal complex in cytogenetic study, Chromosomes Today, 1977, vol. 6, pp. 71—82.
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.
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.
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
Agarwal, S. and Roeder, G.S., Zip3 provides a link between recombination enzymes and synaptonemal complex proteins, Cell, 2000, vol. 102, pp. 245—255.
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
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.
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.
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.
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
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
Muller, H., The mechanism of crossing-over, Am. Nat., 1916, vol. 50, pp. 193—221.
Forejt, J., X-inactivation and its role in mail sterility, Chromosomes Today, 1984, vol. 8, pp. 17—22.
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.
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.
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
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
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
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.
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.
Auger, D.L. and Sheridan, W.F., Negative crossover interference in maize translocation heterozygotes, Genetics, 2001, vol. 159, pp. 1717—1726.
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
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
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.
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
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
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.
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
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.
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.
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
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
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
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
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
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
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
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
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
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
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
King, J.S. and Mortimer, R.K., A polymerization model of chiasma interference and corresponding computer simulation, Genetics, 1990, vol. 126, pp. 1127—1138.
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.
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
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
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
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.
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.
Holm, P.B. and Rasmussen, S.W., Three-dimensional reconstruction of meiotic chromosomes in human spermatogenesis, Chromosomes Today, 1978, vol. 6, pp. 83—93.
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.
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.
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.
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
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
Zickler, D. and Kleckner, N., Meiotic chromosomes: integrating structure and function, Annu. Rev. Genet., 1999, vol. 33, pp. 603—754.
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.
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
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
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
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
Prokof’eva-Bel’govskaya, A.A., Geterokhromaticheskie raiony khromosom (Heterochromatic Regions of Chromosomes), Moscow: Nauka, 1986.
Elgin, S.C. and Grewal, S.I., Heterochromatin: silence is golden, Curr. Biol., 2003, vol. 13, p. R896.
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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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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DOI: https://doi.org/10.1134/S1022795420020039