Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis
Autoři:
Jia-Chi Ku aff001; Arnaud Ronceret aff002; Inna Golubovskaya aff002; Ding Hua Lee aff001; Chiting Wang aff001; Ljudmilla Timofejeva aff002; Yu-Hsin Kao aff001; Ana Karen Gomez Angoa aff003; Karl Kremling aff002; Rosalind Williams-Carrier aff005; Robert Meeley aff006; Alice Barkan aff005; W. Zacheus Cande aff002; Chung-Ju Rachel Wang aff001
Působiště autorů:
Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan
aff001; Department of Molecular and Cell Biology and Plant and Microbial Biology, University of California, Berkeley, CA, United States of America
aff002; Instituto de Biotecnología / UNAM Cuernavaca, Morelos Mexico
aff003; N.I. Vavilov Institute of Plant Industry, St. Petersburg, Russia
aff004; Institute of Molecular Biology, University of Oregon, Eugene, OR, United States of America
aff005; Corteva Agriscience, Johnston, Iowa, United States of America
aff006
Vyšlo v časopise:
Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1007881
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1007881
Souhrn
Meiotic double-strand breaks (DSBs) are generated by the evolutionarily conserved SPO11 complex in the context of chromatin loops that are organized along axial elements (AEs) of chromosomes. However, how DSBs are formed with respect to chromosome axes and the SPO11 complex remains unclear in plants. Here, we confirm that DSB and bivalent formation are defective in maize spo11-1 mutants. Super-resolution microscopy demonstrates dynamic localization of SPO11-1 during recombination initiation, with variable numbers of SPO11-1 foci being distributed in nuclei but similar numbers of SPO11-1 foci being found on AEs. Notably, cytological analysis of spo11-1 meiocytes revealed an aberrant AE structure. At leptotene, AEs of wild-type and spo11-1 meiocytes were similarly curly and discontinuous. However, during early zygotene, wild-type AEs become uniform and exhibit shortened axes, whereas the elongated and curly AEs persisted in spo11-1 mutants, suggesting that loss of SPO11-1 compromised AE structural maturation. Our results reveal an interesting relationship between SPO11-1 loading onto AEs and the conformational remodeling of AEs during recombination initiation.
Klíčová slova:
Anthers – Homologous recombination – Chromatin – Chromosome mapping – Chromosome structure and function – Maize – Meiosis – Synapsis
Zdroje
1. Lam I, Keeney S. Mechanism and regulation of meiotic recombination initiation. Cold Spring Harb Perspect Biol. 2014;7(1):a016634. Epub 2014/10/18. doi: 10.1101/cshperspect.a016634 25324213; PubMed Central PMCID: PMC4292169.
2. Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P. An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature. 1997;386(6623):414–7. Epub 1997/03/27. doi: 10.1038/386414a0 9121560.
3. Neale MJ, Pan J, Keeney S. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature. 2005;436(7053):1053–7. Epub 2005/08/19. doi: 10.1038/nature03872 16107854; PubMed Central PMCID: PMC1262668.
4. Gray S, Cohen PE. Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation. Annu Rev Genet. 2016;50:175–210. Epub 2016/09/21. doi: 10.1146/annurev-genet-120215-035111 27648641; PubMed Central PMCID: PMC5319444.
5. Keeney S, Giroux CN, Kleckner N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell. 1997;88(3):375–84. Epub 1997/02/07. doi: 10.1016/s0092-8674(00)81876-0 9039264.
6. Baudat F, Manova K, Yuen JP, Jasin M, Keeney S. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell. 2000;6(5):989–98. Epub 2000/12/07. doi: 10.1016/s1097-2765(00)00098-8 11106739.
7. Grelon M, Vezon D, Gendrot G, Pelletier G. AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J. 2001;20(3):589–600. Epub 2001/02/07. doi: 10.1093/emboj/20.3.589 11157765; PubMed Central PMCID: PMC133473.
8. Yu H, Wang M, Tang D, Wang K, Chen F, Gong Z, et al. OsSPO11-1 is essential for both homologous chromosome pairing and crossover formation in rice. Chromosoma. 2010;119(6):625–36. Epub 2010/07/14. doi: 10.1007/s00412-010-0284-7 20625906.
9. Wu H, Gao J, Sharif WD, Davidson MK, Wahls WP. Purification, folding, and characterization of Rec12 (Spo11) meiotic recombinase of fission yeast. Protein Expr Purif. 2004;38(1):136–44. Epub 2004/10/13. doi: 10.1016/j.pep.2004.07.012 15477092; PubMed Central PMCID: PMC3127416.
10. Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell. 1998;94(3):387–98. Epub 1998/08/26. doi: 10.1016/s0092-8674(00)81481-6 9708740.
11. Borde V, Goldman AS, Lichten M. Direct coupling between meiotic DNA replication and recombination initiation. Science. 2000;290(5492):806–9. Epub 2000/10/29. doi: 10.1126/science.290.5492.806 11052944.
12. Keeney S, Lange J, Mohibullah N. Self-organization of meiotic recombination initiation: general principles and molecular pathways. Annu Rev Genet. 2014;48:187–214. Epub 2014/11/26. doi: 10.1146/annurev-genet-120213-092304 25421598; PubMed Central PMCID: PMC4291115.
13. Garcia V, Gray S, Allison RM, Cooper TJ, Neale MJ. Tel1(ATM)-mediated interference suppresses clustered meiotic double-strand-break formation. Nature. 2015;520(7545):114–8. Epub 2014/12/30. doi: 10.1038/nature13993 25539084.
14. Thacker D, Mohibullah N, Zhu X, Keeney S. Homologue engagement controls meiotic DNA break number and distribution. Nature. 2014;510(7504):241–6. Epub 2014/04/11. doi: 10.1038/nature13120 24717437; PubMed Central PMCID: PMC4057310.
15. Lange J, Pan J, Cole F, Thelen MP, Jasin M, Keeney S. ATM controls meiotic double-strand-break formation. Nature. 2011;479(7372):237–40. Epub 2011/10/18. doi: 10.1038/nature10508 22002603; PubMed Central PMCID: PMC3213282.
16. van Heemst D, Heyting C. Sister chromatid cohesion and recombination in meiosis. Chromosoma. 2000;109(1–2):10–26. doi: 10.1007/s004120050408 10855491.
17. Zickler D, Kleckner N. Meiotic chromosomes: integrating structure and function. Annu Rev Genet. 1999;33:603–754. Epub 2000/02/26. doi: 10.1146/annurev.genet.33.1.603 10690419.
18. Li J, Hooker GW, Roeder GS. Saccharomyces cerevisiae Mer2, Mei4 and Rec114 form a complex required for meiotic double-strand break formation. Genetics. 2006;173(4):1969–81. Epub 2006/06/20. doi: 10.1534/genetics.106.058768 16783010; PubMed Central PMCID: PMC1569690.
19. Kee K, Protacio RU, Arora C, Keeney S. Spatial organization and dynamics of the association of Rec102 and Rec104 with meiotic chromosomes. EMBO J. 2004;23(8):1815–24. Epub 2004/03/27. doi: 10.1038/sj.emboj.7600184 15044957; PubMed Central PMCID: PMC394238.
20. Kim KP, Weiner BM, Zhang L, Jordan A, Dekker J, Kleckner N. Sister Cohesion and Structural Axis Components Mediate Homolog Bias of Meiotic Recombination. Cell. 2010;143(6):924–37. doi: 10.1016/j.cell.2010.11.015 21145459
21. Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, Shirahige K, et al. Spo11-Accessory Proteins Link Double-Strand Break Sites to the Chromosome Axis in Early Meiotic Recombination. Cell. 2011;146(3):372–83. doi: 10.1016/j.cell.2011.07.003 21816273
22. Sommermeyer V, Beneut C, Chaplais E, Serrentino ME, Borde V. Spp1, a member of the Set1 Complex, promotes meiotic DSB formation in promoters by tethering histone H3K4 methylation sites to chromosome axes. Mol Cell. 2013;49(1):43–54. Epub 2012/12/19. doi: 10.1016/j.molcel.2012.11.008 23246437.
23. Acquaviva L, Szekvolgyi L, Dichtl B, Dichtl BS, de La Roche Saint Andre C, Nicolas A, et al. The COMPASS subunit Spp1 links histone methylation to initiation of meiotic recombination. Science. 2013;339(6116):215–8. Epub 2012/11/20. doi: 10.1126/science.1225739 23160953.
24. Li XC, Bolcun-Filas E, Schimenti JC. Genetic evidence that synaptonemal complex axial elements govern recombination pathway choice in mice. Genetics. 2011;189(1):71–82. Epub 2011/07/14. doi: 10.1534/genetics.111.130674 21750255; PubMed Central PMCID: PMC3176111.
25. Page SL, Hawley RS. The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol. 2004;20:525–58. Epub 2004/10/12. doi: 10.1146/annurev.cellbio.19.111301.155141 15473851.
26. Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N, Belcram K, et al. AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci. 2005;118(20):4621–32.
27. Golubovskaya IN, Hamant O, Timofejeva L, Wang C-JR, Braun D, Meeley R, et al. Alleles of afd1 dissect REC8 functions during meiotic prophase I. J Cell Sci. 2006;119(16):3306–15. doi: 10.1242/jcs.03054 16868028
28. Armstrong SJ, Caryl AP, Jones GH, Franklin FC. Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci. 2002;115(Pt 18):3645–55. Epub 2002/08/21. doi: 10.1242/jcs.00048 12186950.
29. Nonomura K, Nakano M, Eiguchi M, Suzuki T, Kurata N. PAIR2 is essential for homologous chromosome synapsis in rice meiosis I. J Cell Sci. 2006;119(Pt 2):217–25. Epub 2006/01/18. doi: 10.1242/jcs.02736 16410547.
30. Hollingsworth NM, Byers B. HOP1: a yeast meiotic pairing gene. Genetics. 1989;121(3):445–62. 2653960; PubMed Central PMCID: PMC1203632.
31. Osman K, Yang J, Roitinger E, Lambing C, Heckmann S, Howell E, et al. Affinity proteomics reveals extensive phosphorylation of the Brassica chromosome axis protein ASY1 and a network of associated proteins at prophase I of meiosis. Plant J. 2018;93(1):17–33. Epub 2017/10/28. doi: 10.1111/tpj.13752 29078019; PubMed Central PMCID: PMC5767750.
32. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, Boonsanay V, et al. Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet. 2009;5(10):e1000702. Epub 2009/10/24. doi: 10.1371/journal.pgen.1000702 19851446; PubMed Central PMCID: PMC2758600.
33. Golubovskaya IN, Wang CJ, Timofejeva L, Cande WZ. Maize meiotic mutants with improper or non-homologous synapsis due to problems in pairing or synaptonemal complex formation. J Exp Bot. 2011;62(5):1533–44. Epub 2010/10/12. doi: 10.1093/jxb/erq292 20926553; PubMed Central PMCID: PMC3107535.
34. West AM, Rosenberg SC, Ur SN, Lehmer MK, Ye Q, Hagemann G, et al. A conserved filamentous assembly underlies the structure of the meiotic chromosome axis. Elife. 2019;8. Epub 2019/01/19. doi: 10.7554/eLife.40372 30657449; PubMed Central PMCID: PMC6349405.
35. Woltering D, Baumgartner B, Bagchi S, Larkin B, Loidl J, de los Santos T, et al. Meiotic segregation, synapsis, and recombination checkpoint functions require physical interaction between the chromosomal proteins Red1p and Hop1p. Mol Cell Biol. 2000;20(18):6646–58. Epub 2000/08/25. doi: 10.1128/mcb.20.18.6646-6658.2000 10958662; PubMed Central PMCID: PMC86166.
36. Wang K, Wang M, Tang D, Shen Y, Qin B, Li M, et al. PAIR3, an axis-associated protein, is essential for the recruitment of recombination elements onto meiotic chromosomes in rice. Mol Biol Cell. 2011;22(1):12–9. Epub 2010/12/02. doi: 10.1091/mbc.E10-08-0667 21119003; PubMed Central PMCID: PMC3016970.
37. Lee DH, Kao YH, Ku JC, Lin CY, Meeley R, Jan YS, et al. The Axial Element Protein DESYNAPTIC2 Mediates Meiotic Double-Strand Break Formation and Synaptonemal Complex Assembly in Maize. Plant Cell. 2015;27(9):2516–29. Epub 2015/08/25. doi: 10.1105/tpc.15.00434 26296964; PubMed Central PMCID: PMC4815100.
38. Ferdous M, Higgins JD, Osman K, Lambing C, Roitinger E, Mechtler K, et al. Inter-homolog crossing-over and synapsis in Arabidopsis meiosis are dependent on the chromosome axis protein AtASY3. PLoS Genet. 2012;8(2):e1002507. Epub 2012/02/10. doi: 10.1371/journal.pgen.1002507 22319460; PubMed Central PMCID: PMC3271061.
39. Chambon A, West A, Vezon D, Horlow C, De Muyt A, Chelysheva L, et al. Identification of ASYNAPTIC4, a Component of the Meiotic Chromosome Axis. Plant Physiol. 2018;178(1):233–46. Epub 2018/07/14. doi: 10.1104/pp.17.01725 30002256; PubMed Central PMCID: PMC6130017.
40. de Massy B. Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu Rev Genet. 2013;47:563–99. Epub 2013/09/21. doi: 10.1146/annurev-genet-110711-155423 24050176.
41. Dawe RK, Sedat JW, Agard DA, Cande WZ. Meiotic chromosome pairing in maize is associated with a novel chromatin organization. Cell. 1994;76(5):901–12. Epub 1994/03/11. doi: 10.1016/0092-8674(94)90364-6 8124724.
42. Wang CJ, Carlton PM, Golubovskaya IN, Cande WZ. Interlock formation and coiling of meiotic chromosome axes during synapsis. Genetics. 2009;183(3):905–15. Epub 2009/09/16. doi: 10.1534/genetics.109.108688 19752214; PubMed Central PMCID: PMC2778986.
43. Phillips D, Nibau C, Wnetrzak J, Jenkins G. High resolution analysis of meiotic chromosome structure and behaviour in barley (Hordeum vulgare L.). PLoS One. 2012;7(6):e39539. Epub 2012/07/05. doi: 10.1371/journal.pone.0039539 22761818; PubMed Central PMCID: PMC3382580.
44. Higgins JD, Osman K, Jones GH, Franklin FC. Factors underlying restricted crossover localization in barley meiosis. Annu Rev Genet. 2014;48:29–47. Epub 2014/08/05. doi: 10.1146/annurev-genet-120213-092509 25089719.
45. Colas I, Shaw P, Prieto P, Wanous M, Spielmeyer W, Mago R, et al. Effective chromosome pairing requires chromatin remodeling at the onset of meiosis. Proc Natl Acad Sci U S A. 2008;105(16):6075–80. Epub 2008/04/18. doi: 10.1073/pnas.0801521105 18417451; PubMed Central PMCID: PMC2329686.
46. Ronceret A, Pawlowski WP. Chromosome dynamics in meiotic prophase I in plants. Cytogenet Genome Res. 2010;129(1–3):173–83. Epub 2010/06/17. doi: 10.1159/000313656 20551605.
47. Golubovskaya IN, Sheridan WF, Harper LC, Zacheus CW. Novel meiotic mutants of maize identified from Mu transposon and EMS mutant screens. Maize Genet Coop Newsl 2003 77:10–3.
48. Cande WZ, Golubovskaya I, Wang CJR, Harper L. Meiotic Genes and Meiosis in Maize. In: Bennetzen J, Hake S, editors. Handbook of Maize. New York: Springer; 2009. p. 353–75.
49. Cande WZ, Golubovskaya I, Wang RC, Harper L. Meiotic Genes and Meiosis in Maize. In: Bennetzen JL, Hake SC, editors. Maize Handbook—Volume II: Genetics and Genomic2009. p. 353–75.
50. Carlton PM, Cande WZ. Telomeres act autonomously in maize to organize the meiotic bouquet from a semipolarized chromosome orientation. J Cell Biol. 2002;157(2):231–42. Epub 2002/04/17. doi: 10.1083/jcb.200110126 11956226; PubMed Central PMCID: PMC2199251.
51. Williams-Carrier R, Stiffler N, Belcher S, Kroeger T, Stern DB, Monde RA, et al. Use of Illumina sequencing to identify transposon insertions underlying mutant phenotypes in high-copy Mutator lines of maize. Plant J. 2010;63(1):167–77. Epub 2010/04/23. doi: 10.1111/j.1365-313X.2010.04231.x 20409008.
52. McCarty DR, Meeley RB. Transposon Resources for Forward and Reverse Genetics in Maize. In: Bennetzen JL, Hake S, editors. Handbook of Maize: Springer New York; 2009. p. 561–84.
53. Ollion J, Cochennec J, Loll F, Escude C, Boudier T. TANGO: a generic tool for high-throughput 3D image analysis for studying nuclear organization. Bioinformatics. 2013;29(14):1840–1. Epub 2013/05/18. doi: 10.1093/bioinformatics/btt276 23681123; PubMed Central PMCID: PMC3702251.
54. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–5. Epub 2012/08/30. doi: 10.1038/nmeth.2089 22930834; PubMed Central PMCID: PMC5554542.
55. Arganda-Carreras I, Kaynig V, Rueden C, Eliceiri KW, Schindelin J, Cardona A, et al. Trainable Weka Segmentation: a machine learning tool for microscopy pixel classification. Bioinformatics. 2017;33(15):2424–6. Epub 2017/04/04. doi: 10.1093/bioinformatics/btx180 28369169.
56. Mary H, Brouhard GJ. Kappa (κ): Analysis of Curvature in Biological Image Data using B-splines. bioRxiv. 2019. doi: 10.1101/852772
57. Vrielynck N, Chambon A, Vezon D, Pereira L, Chelysheva L, De Muyt A, et al. A DNA topoisomerase VI-like complex initiates meiotic recombination. Science. 2016;351(6276):939–43. Epub 2016/02/27. doi: 10.1126/science.aad5196 26917763.
58. Tock AJ, Henderson IR. Hotspots for Initiation of Meiotic Recombination. Front Genet. 2018;9:521. Epub 2018/11/24. doi: 10.3389/fgene.2018.00521 30467513; PubMed Central PMCID: PMC6237102.
59. Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, Shirahige K, et al. Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell. 2011;146(3):372–83. Epub 2011/08/06. doi: 10.1016/j.cell.2011.07.003 21816273.
60. Blat Y, Protacio RU, Hunter N, Kleckner N. Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell. 2002;111(6):791–802. doi: 10.1016/s0092-8674(02)01167-4 WOS:000179862600006. 12526806
61. Prieler S, Penkner A, Borde V, Klein F. The control of Spo11's interaction with meiotic recombination hotspots. Genes Dev. 2005;19(2):255–69. Epub 2005/01/19. doi: 10.1101/gad.321105 15655113; PubMed Central PMCID: PMC545890.
62. Storlazzi A, Tesse S, Gargano S, James F, Kleckner N, Zickler D. Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division. Genes Dev. 2003;17(21):2675–87. Epub 2003/10/18. doi: 10.1101/gad.275203 14563680; PubMed Central PMCID: PMC280617.
63. Choi K, Zhao X, Tock AJ, Lambing C, Underwood CJ, Hardcastle TJ, et al. Nucleosomes and DNA methylation shape meiotic DSB frequency in Arabidopsis thaliana transposons and gene regulatory regions. Genome Res. 2018;28(4):532–46. Epub 2018/03/14. doi: 10.1101/gr.225599.117 29530928; PubMed Central PMCID: PMC5880243.
64. Romanienko PJ, Camerini-Otero RD. The mouse Spo11 gene is required for meiotic chromosome synapsis. Molecular Cell. 2000;6(5):975–87. doi: 10.1016/s1097-2765(00)00097-6 WOS:000165472100001. 11106738
65. Sidhu GK, Fang C, Olson MA, Falque M, Martin OC, Pawlowski WP. Recombination patterns in maize reveal limits to crossover homeostasis. Proc Natl Acad Sci U S A. 2015;112(52):15982–7. Epub 2015/12/17. doi: 10.1073/pnas.1514265112 26668366; PubMed Central PMCID: PMC4703008.
66. Joshi N, Barot A, Jamison C, Borner GV. Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet. 2009;5(7):e1000557. Epub 2009/07/25. doi: 10.1371/journal.pgen.1000557 19629172; PubMed Central PMCID: PMC2708914.
67. Carballo JA, Panizza S, Serrentino ME, Johnson AL, Geymonat M, Borde V, et al. Budding yeast ATM/ATR control meiotic double-strand break (DSB) levels by down-regulating Rec114, an essential component of the DSB-machinery. PLoS Genet. 2013;9(6):e1003545. Epub 2013/07/05. doi: 10.1371/journal.pgen.1003545 23825959; PubMed Central PMCID: PMC3694840.
68. Franklin AE, McElver J, Sunjevaric I, Rothstein R, Bowen B, Cande WZ. Three-dimensional microscopy of the Rad51 recombination protein during meiotic prophase. Plant Cell. 1999;11(5):809–24. Epub 1999/05/20. doi: 10.1105/tpc.11.5.809 10330467; PubMed Central PMCID: PMC144225.
69. Sprink T, Hartung F. The splicing fate of plant SPO11 genes. Front Plant Sci. 2014;5:214. Epub 2014/07/16. doi: 10.3389/fpls.2014.00214 25018755; PubMed Central PMCID: PMC4071758.
70. Hartung F, Wurz-Wildersinn R, Fuchs J, Schubert I, Suer S, Puchta H. The catalytically active tyrosine residues of both SPO11-1 and SPO11-2 are required for meiotic double-strand break induction in Arabidopsis. Plant Cell. 2007;19(10):3090–9. Epub 2007/10/30. doi: 10.1105/tpc.107.054817 17965269; PubMed Central PMCID: PMC2174718.
71. Grelon M, Vezon D, Gendrot G, Pelletier G. AtSPO11-1 is necessary for efficient meiotic recombination in plants. Embo Journal. 2001;20(3):589–600. doi: 10.1093/emboj/20.3.589 WOS:000166848400028. 11157765
72. Stacey NJ, Kuromori T, Azumi Y, Roberts G, Breuer C, Wada T, et al. Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J. 2006;48(2):206–16. Epub 2006/10/05. doi: 10.1111/j.1365-313X.2006.02867.x 17018031.
73. Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG, Tischfield SE, et al. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell. 2011;144(5):719–31. Epub 2011/03/08. doi: 10.1016/j.cell.2011.02.009 21376234; PubMed Central PMCID: PMC3063416.
74. Fowler KR, Sasaki M, Milman N, Keeney S, Smith GR. Evolutionarily diverse determinants of meiotic DNA break and recombination landscapes across the genome. Genome Res. 2014;24(10):1650–64. Epub 2014/07/16. doi: 10.1101/gr.172122.114 25024163; PubMed Central PMCID: PMC4199369.
75. Lange J, Yamada S, Tischfield SE, Pan J, Kim S, Zhu X, et al. The Landscape of Mouse Meiotic Double-Strand Break Formation, Processing, and Repair. Cell. 2016;167(3):695–708 e16. Epub 2016/10/22. doi: 10.1016/j.cell.2016.09.035 27745971; PubMed Central PMCID: PMC5117687.
76. Moon J, Skibbe D, Timofejeva L, Wang CJ, Kelliher T, Kremling K, et al. Regulation of cell divisions and differentiation by MALE STERILITY32 is required for anther development in maize. Plant J. 2013;76(4):592–602. Epub 2013/09/17. doi: 10.1111/tpj.12318 24033746; PubMed Central PMCID: PMC4239027.
77. Nan GL, Ronceret A, Wang RC, Fernandes JF, Cande WZ, Walbot V. Global transcriptome analysis of two ameiotic1 alleles in maize anthers: defining steps in meiotic entry and progression through prophase I. BMC Plant Biol. 2011;11:120. Epub 2011/08/27. doi: 10.1186/1471-2229-11-120 21867558; PubMed Central PMCID: PMC3180651.
78. Dawe RK, Sedat JW, Agard DA, Cande WZ. Meiotic chromosome pairing in maize is associated with a novel chromatin organization. Cell. 1994;76(5):901–12. doi: 10.1016/0092-8674(94)90364-6 8124724
79. Wang CJ. Analyzing maize meiotic chromosomes with super-resolution structured illumination microscopy. Methods Mol Biol. 2013;990:67–78. Epub 2013/04/06. doi: 10.1007/978-1-62703-333-6_7 23559203.
80. Huang J, Cheng Z, Wang C, Hong Y, Su H, Wang J, et al. Formation of interference-sensitive meiotic cross-overs requires sufficient DNA leading-strand elongation. Proc Natl Acad Sci U S A. 2015;112(40):12534–9. Epub 2015/09/24. doi: 10.1073/pnas.1507165112 26392549; PubMed Central PMCID: PMC4603498.
81. He Y, Wang M, Dukowic-Schulze S, Zhou A, Tiang CL, Shilo S, et al. Genomic features shaping the landscape of meiotic double-strand-break hotspots in maize. Proc Natl Acad Sci U S A. 2017;114(46):12231–6. Epub 2017/11/01. doi: 10.1073/pnas.1713225114 29087335; PubMed Central PMCID: PMC5699076.
82. Pawlowski WP, Golubovskaya IN, Timofejeva L, Meeley RB, Sheridan WF, Cande WZ. Coordination of meiotic recombination, pairing, and synapsis by PHS1. Science. 2004;303(5654):89–92. Epub 2004/01/06. doi: 10.1126/science.1091110 14704428.
83. Timofejeva L, Grebennikova ZK, Gaft M, Golubovskaya I. Ultrastructural features of synaptonemal complexes of maize in norm. Tsitologiya. 1991;33:12–9.
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