Meiosis is the cell division that reshuffles genetic information between generations. Recently, much progress has been made in understanding this process; in particular, the identification and functional analysis of more than 80 plant genes involved in meiosis have dramatically deepened our knowledge of this peculiar cell division. In this review, we provide an overview of advancements in the understanding of all aspects of plant meiosis, including recombination, chromosome synapsis, cell cycle control, chromosome distribution, and the challenge of polyploidy.


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Literature Cited

  1. Agostinho A, Meier B, Sonneville R, Jagut M, Woglar A. 1.  et al. 2013. Combinatorial regulation of meiotic Holliday junction resolution in C. elegans by HIM-6 (BLM) helicase, SLX-4, and the SLX-1, MUS-81 and XPF-1 nucleases. PLOS Genet. 9:e1003591 [Google Scholar]
  2. Aklilu BB, Soderquist RS, Culligan KM. 2.  2014. Genetic analysis of the Replication Protein A large subunit family in Arabidopsis reveals unique and overlapping roles in DNA repair, meiosis and DNA replication. Nucleic Acids Res. 42:3104–18 [Google Scholar]
  3. Al-Kaff N, Knight E, Bertin I, Foote T, Hart N. 3.  et al. 2008. Detailed dissection of the chromosomal region containing the Ph1 locus in wheat Triticum aestivum: with deletion mutants and expression profiling. Ann. Bot. 101:863–72 [Google Scholar]
  4. Allers T, Lichten M. 4.  2001. Intermediates of yeast meiotic recombination contain heteroduplex DNA. Mol. Cell 8:225–31 [Google Scholar]
  5. An XJ, Deng ZY, Wang T. 5.  2011. OsSPO11-4, a rice homologue of the Archaeal TOPVIA protein, mediates double-strand DNA cleavage and interacts with OsTOPVIB. PLOS ONE 6:e20327 [Google Scholar]
  6. Anderson LK, Lohmiller LD, Tang X, Hammond DB, Javernick L. 6.  et al. 2014. Combined fluorescent and electron microscopic imaging unveils the specific properties of two classes of meiotic crossovers. PNAS 111:13415–20 [Google Scholar]
  7. Armstrong SJ, Caryl AP, Jones GH, Franklin FCH. 7.  2002. ASY1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J. Cell Sci. 115:3645–55 [Google Scholar]
  8. Armstrong SJ, Franklin FCH, Jones GH. 8.  2003. A meiotic time-course for Arabidopsis thaliana. Sex. Plant Reprod. 16:141–49 [Google Scholar]
  9. Barakate A, Higgins JD, Vivera S, Stephens J, Perry RM. 9.  et al. 2014. The synaptonemal complex protein ZYP1 is required for imposition of meiotic crossovers in barley. Plant Cell 26:729–40 [Google Scholar]
  10. Basu-Roy S, Gauthier F, Giraut L, Mézard C, Falque M, Martin OC. 10.  2013. Hot regions of noninterfering crossovers coexist with a nonuniformly interfering pathway in Arabidopsis thaliana. Genetics 195:769–79 [Google Scholar]
  11. Bauer E, Falque M, Walter H, Bauland C, Camisan C. 11.  et al. 2013. Intraspecific variation of recombination rate in maize. Genome Biol. 14:R103 [Google Scholar]
  12. Bauknecht M, Kobbe D. 12.  2014. AtGEN1 and AtSEND1, two paralogs in Arabidopsis, possess Holliday junction resolvase activity. Plant Physiol. 166:202–16 [Google Scholar]
  13. Berchowitz LE, Copenhaver GP. 13.  2010. Genetic interference: don't stand so close to me. Curr. Genomics 11:91–102 [Google Scholar]
  14. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP. 14.  2007. The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLOS Genet. 3:e132 [Google Scholar]
  15. Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P. 15.  1997. An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386:414–17 [Google Scholar]
  16. Bhatt AM, Lister C, Page T, Fransz P, Findlay K. 16.  et al. 1999. The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family. Plant J. 19:463–72 [Google Scholar]
  17. Boden SA, Langridge P, Spangenberg G, Able JA. 17.  2009. TaASY1 promotes homologous chromosome interactions and is affected by deletion of Ph1. Plant J. 57:487–97 [Google Scholar]
  18. Borde V, de Massy B. 18.  2013. Programmed induction of DNA double strand breaks during meiosis: setting up communication between DNA and the chromosome structure. Curr. Opin. Genet. Dev. 23:147–55 [Google Scholar]
  19. Börner GV, Barot A, Kleckner N. 19.  2008. Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. PNAS 105:3327–32 [Google Scholar]
  20. Börner GV, Kleckner N, Hunter N. 20.  2004. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117:29–45 [Google Scholar]
  21. Bulankova P, Akimcheva S, Fellner N, Riha K. 21.  2013. Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes. PLOS Genet. 9:e1003508 [Google Scholar]
  22. Bulankova P, Riehs-Kearnan N, Nowack MK, Schnittger A, Riha K. 22.  2010. Meiotic progression in Arabidopsis is governed by complex regulatory interactions between SMG7, TDM1, and the meiosis I-specific cyclin TAM. Plant Cell 22:3791–803 [Google Scholar]
  23. Cai X, Dong F, Edelmann RE, Makaroff CA. 23.  2003. The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J. Cell Sci. 116:2999–3007 [Google Scholar]
  24. Callender TL, Hollingsworth NM. 24.  2010. Mek1 suppression of meiotic double-strand break repair is specific to sister chromatids, chromosome autonomous and independent of Rec8 cohesin complexes. Genetics 185:771–82 [Google Scholar]
  25. Carlile TM, Amon A. 25.  2008. Meiosis I is established through division-specific translational control of a cyclin. Cell 133:280–91 [Google Scholar]
  26. Carvalho A, Delgado M, Barão A, Frescatada M, Ribeiro E. 26.  et al. 2010. Chromosome and DNA methylation dynamics during meiosis in the autotetraploid Arabidopsis arenosa. Sex. Plant Reprod. 23:29–37 [Google Scholar]
  27. Chang L, Ma H, Xue H-W. 27.  2009. Functional conservation of the meiotic genes SDS and RCK in male meiosis in the monocot rice. Cell Res. 19:768–82 [Google Scholar]
  28. Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N. 28.  et al. 2005. AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J. Cell Sci. 118:4621–32 [Google Scholar]
  29. Chelysheva L, Gendrot G, Vezon D, Doutriaux M-P, Mercier R, Grelon M. 29.  2007. ZIP4/SPO22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLOS Genet. 3:e83 [Google Scholar]
  30. Chelysheva L, Grandont L, Vrielynck N, le Guin S, Mercier R, Grelon M. 30.  2010. An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: immunodetection of cohesins, histones and MLH1. Cytogenet. Genome Res. 129:143–53 [Google Scholar]
  31. Chelysheva L, Vezon D, Belcram K, Gendrot G, Grelon M. 31.  2008. The Arabidopsis BLAP75/RMI1 homologue plays crucial roles in meiotic double-strand break repair. PLOS Genet. 4:e1000309 [Google Scholar]
  32. Chelysheva L, Vezon D, Chambon A, Gendrot G, Pereira L. 32.  et al. 2012. The Arabidopsis HEI10 is a new ZMM protein related to ZIP3. PLOS Genet. 8:e1002799 [Google Scholar]
  33. Chen C, Zhang W, Timofejeva L, Gerardin Y, Ma H. 33.  2005. The Arabidopsis ROCK-N-ROLLERS gene encodes a homolog of the yeast ATP-dependent DNA helicase MER3 and is required for normal meiotic crossover formation. Plant J. 43:321–34 [Google Scholar]
  34. Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR. 34.  et al. 2008. Global analysis of the meiotic crossover landscape. Dev. Cell 15:401–15 [Google Scholar]
  35. Choi K, Zhao X, Kelly KA, Venn O, Higgins JD. 35.  et al. 2013. Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters. Nat. Genet. 45:1327–36 [Google Scholar]
  36. Cifuentes M, Grandont L, Moore G, Chèvre AM, Jenczewski E. 36.  2010. Genetic regulation of meiosis in polyploid species: new insights into an old question. New Phytol. 186:29–36 [Google Scholar]
  37. Cifuentes M, Rivard M, Pereira L, Chelysheva L, Mercier R. 37.  2013. Haploid meiosis in Arabidopsis: double-strand breaks are formed and repaired but without synapsis and crossovers. PLOS ONE 8:e72431 [Google Scholar]
  38. Cloud V, Chan Y-L, Grubb J, Budke B, Bishop DK. 38.  2012. Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 337:1222–25 [Google Scholar]
  39. Comeron JM, Ratnappan R, Bailin S. 39.  2012. The many landscapes of recombination in Drosophila melanogaster. PLOS Genet. 8:e1002905 [Google Scholar]
  40. Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, Doutriaux MP. 40.  1999. Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell 11:1623–34 [Google Scholar]
  41. Creighton HB, McClintock B. 41.  1931. A correlation of cytological and genetical crossing-over in Zea mays. PNAS 17:492–97 [Google Scholar]
  42. Crismani W, Girard C, Froger N, Pradillo M, Santos JL. 42.  et al. 2012. FANCM limits meiotic crossovers. Science 336:1588–90 [Google Scholar]
  43. Crismani W, Girard C, Mercier R. 43.  2013. Tinkering with meiosis. J. Exp. Bot. 64:55–65 [Google Scholar]
  44. Crismani W, Portemer V, Froger N, Chelysheva L, Horlow C. 44.  et al. 2013. MCM8 is required for a pathway of meiotic double-strand break repair independent of DMC1 in Arabidopsis thaliana. PLOS Genet. 9:e1003165 [Google Scholar]
  45. Cromer L, Heyman J, Touati S, Harashima H, Araou E. 45.  et al. 2012. OSD1 promotes meiotic progression via APC/C inhibition and forms a regulatory network with TDM and CYCA1;2/TAM. PLOS Genet. 8:e1002865 [Google Scholar]
  46. Cromer L, Jolivet S, Horlow C, Chelysheva L, Heyman J. 46.  et al. 2013. Centromeric cohesion is protected twice at meiosis, by SHUGOSHINs at anaphase I and by PATRONUS at interkinesis. Curr. Biol. 23:2090–99 [Google Scholar]
  47. d'Erfurth I, Cromer L, Jolivet S, Girard C, Horlow C. 47.  et al. 2010. The cyclin-A CYCA1;2/TAM is required for the meiosis I to meiosis II transition and cooperates with OSD1 for the prophase to first meiotic division transition. PLOS Genet. 6:e1000989 [Google Scholar]
  48. d'Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Mercier R. 48.  2009. Turning meiosis into mitosis. PLOS Biol. 7:e1000124 [Google Scholar]
  49. d'Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M. 49.  et al. 2008. Mutations in AtPS1 (Arabidopsis thaliana Parallel Spindle 1) lead to the production of diploid pollen grains. PLOS Genet. 4:e1000274 [Google Scholar]
  50. Da Ines O, Degroote F, Amiard S, Goubely C, Gallego ME, White CI. 50.  2013. Effects of xrcc2 and rad51b mutations on somatic and meiotic recombination in Arabidopsis thaliana. Plant J. 74:959–70 [Google Scholar]
  51. Da Ines O, Degroote F, Goubely C, Amiard S, Gallego ME, White CI. 51.  2013. Meiotic recombination in Arabidopsis is catalysed by DMC1, with RAD51 playing a supporting role. PLOS Genet. 9:e1003787 [Google Scholar]
  52. De Massy B. 52.  2013. Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu. Rev. Genet. 47:563–99 [Google Scholar]
  53. De Muyt A, Jessop L, Kolar E, Sourirajan A, Chen J. 53.  et al. 2012. Blm helicase ortholog Sgs1 is a central regulator of meiotic recombination intermediate metabolism. Mol. Cell 46:43–53 [Google Scholar]
  54. De Muyt A, Pereira L, Vezon D, Chelysheva L, Gendrot G. 54.  et al. 2009. A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLOS Genet. 5:e1000654 [Google Scholar]
  55. De Muyt A, Vezon D, Gendrot G, Gallois J-L, Stevens R, Grelon M. 55.  2007. AtPRD1 is required for meiotic double strand break formation in Arabidopsis thaliana. EMBO J. 26:4126–37 [Google Scholar]
  56. De Veylder L, Larkin JC, Schnittger A. 56.  2011. Molecular control and function of endoreplication in development and physiology. Trends Plant Sci. 16:624–34 [Google Scholar]
  57. Deng Z-Y, Wang T. 57.  2007. OsDMC1 is required for homologous pairing in Oryza sativa. Plant Mol. Biol. 65:31–42 [Google Scholar]
  58. Dissmeyer N, Nowack MK, Pusch S, Stals H, Inzé D. 58.  et al. 2007. T-loop phosphorylation of Arabidopsis CDKA;1 is required for its function and can be partially substituted by an aspartate residue. Plant Cell 19:972–85 [Google Scholar]
  59. Dooner HK. 59.  2002. Extensive interallelic polymorphisms drive meiotic recombination into a crossover pathway. Plant Cell 14:1173–83 [Google Scholar]
  60. Dooner HK, He L. 59a.  2014. Polarized gene conversion at the bz locus of maize. PNAS 111:13918–23 [Google Scholar]
  61. Dray E, Siaud N, Dubois E, Doutriaux M-P. 60.  2006. Interaction between Arabidopsis BRCA2 and its partners RAD51, DMC1, and DSS1. Plant Physiol. 140:1059–69 [Google Scholar]
  62. Drouaud J, Khademian H, Giraut L, Zanni V, Bellalou S. 61.  et al. 2013. Contrasted patterns of crossover and non-crossover at Arabidopsis thaliana meiotic recombination hotspots. PLOS Genet. 9:e1003922 [Google Scholar]
  63. Duroc Y, Lemhemdi A, Larchevêque C, Hurel A, Cuacos M. 62.  et al. 2014. . The kinesin AtPSS1 promotes synapsis and is required for proper crossover distribution in meiosis. PLOS Genet. 10:e1004674 [Google Scholar]
  64. Edlinger B, Schlögelhofer P. 63.  2011. Have a break: determinants of meiotic DNA double strand break (DSB) formation and processing in plants. J. Exp. Bot. 62:1545–63 [Google Scholar]
  65. Erilova A, Brownfield L, Exner V, Rosa M, Twell D. 64.  et al. 2009. Imprinting of the polycomb group gene MEDEA serves as a ploidy sensor in Arabidopsis. PLOS Genet. 5:e1000663 [Google Scholar]
  66. Eschbach V, Kobbe D. 65.  2014. Different replication protein a complexes of Arabidopsis thaliana have different DNA-binding properties as a function of heterotrimer composition. Plant Cell Physiol. 55:1460–72 [Google Scholar]
  67. Falque M, Anderson LK, Stack SM, Gauthier F, Martin OC. 66.  2009. Two types of meiotic crossovers coexist in maize. Plant Cell 21:3915–25 [Google Scholar]
  68. Ferdous M, Higgins JD, Osman KE, Lambing C, Roitinger E. 67.  et al. 2012. Inter-homolog crossing-over and synapsis in Arabidopsis meiosis are dependent on the chromosome axis protein AtASY3. PLOS Genet. 8:e1002507 [Google Scholar]
  69. Forterre P, Gribaldo S, Gadelle D, Serre M-C. 68.  2007. Origin and evolution of DNA topoisomerases. Biochimie 89:427–46 [Google Scholar]
  70. Gerton JL, Hawley RS. 69.  2005. Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat. Rev. Genet. 6:477–87 [Google Scholar]
  71. Girard C, Crismani W, Froger N, Mazel J, Lemhemdi A. 70.  et al. 2014. FANCM-associated proteins MHF1 and MHF2, but not the other Fanconi anemia factors, limit meiotic crossovers. Nucleic Acids Res. 42:9087–95 [Google Scholar]
  72. Giraut L, Falque M, Drouaud J, Pereira L, Martin OC, Mézard C. 71.  2011. Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLOS Genet. 7:e1002354 [Google Scholar]
  73. Glover J, Grelon M, Craig S, Chaudhury A, Dennis E. 72.  1998. Cloning and characterization of MS5 from Arabidopsis: a gene critical in male meiosis. Plant J. 15:345–56 [Google Scholar]
  74. Goldfarb T, Lichten M. 73.  2010. Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLOS Biol. 8:e1000520 [Google Scholar]
  75. Golubovskaya IN, Hamant O, Timofejeva L, Wang C-JR, Braun D. 74.  et al. 2006. Alleles of afd1 dissect REC8 functions during meiotic prophase I. J. Cell Sci. 119:3306–15 [Google Scholar]
  76. Grandont L, Cuñado N, Coriton O, Huteau V, Eber F. 75.  et al. 2014. Homoeologous chromosome sorting and progression of meiotic recombination in Brassica napus: Ploidy does matter!. Plant Cell 26:1448–63 [Google Scholar]
  77. Grandont L, Jenczewski E, Lloyd A. 76.  2013. Meiosis and its deviations in polyploid plants. Cytogenet. Genome Res. 140:171–84 [Google Scholar]
  78. Greer E, Martín AC, Pendle A, Colas I, Jones AME. 77.  et al. 2012. The Ph1 locus suppresses Cdk2-type activity during premeiosis and meiosis in wheat. Plant Cell 24:152–62 [Google Scholar]
  79. Grelon M, Vezon D, Gendrot G, Pelletier G. 78.  2001. AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J. 20:589–600 [Google Scholar]
  80. Griffiths S, Sharp R, Foote TN, Bertin I, Wanous M. 79.  et al. 2006. Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439:749–52 [Google Scholar]
  81. Hamant O, Golubovskaya I, Meeley R, Fiume E, Timofejeva L. 80.  et al. 2005. A REC8-dependent plant Shugoshin is required for maintenance of centromeric cohesion during meiosis and has no mitotic functions. Curr. Biol. 15:948–54 [Google Scholar]
  82. Harashima H, Dissmeyer N, Schnittger A. 81.  2013. Cell cycle control across the eukaryotic kingdom. Trends Cell Biol. 23:345–56 [Google Scholar]
  83. Hartung F, Angelis KJ, Meister A, Schubert I, Melzer M, Puchta H. 82.  2002. An Archaebacterial topoisomerase homolog not present in other eukaryotes is indispensable for cell proliferation of plants. Curr. Biol. 12:1787–91 [Google Scholar]
  84. Hartung F, Suer S, Knoll A, Wurz-Wildersinn R, Puchta H. 83.  2008. Topoisomerase 3α and RMI1 suppress somatic crossovers and are essential for resolution of meiotic recombination intermediates in Arabidopsis thaliana. PLOS Genet. 4:e1000285 [Google Scholar]
  85. Hartung F, Wurz-Wildersinn R, Fuchs J, Schubert I, Suer S, Puchta H. 84.  2007. The catalytically active tyrosine residues of both SPO11-1 and SPO11-2 are required for meiotic double-strand break induction in Arabidopsis. Plant Cell 19:3090–99 [Google Scholar]
  86. He L, Dooner HK. 85.  2009. Haplotype structure strongly affects recombination in a maize genetic interval polymorphic for helitron and retrotransposon insertions. PNAS 106:8410–16 [Google Scholar]
  87. Henry IM, Dilkes BP, Tyagi A, Gao J, Christensen B, Comai L. 86.  2014. The BOY NAMED SUE quantitative trait locus confers increased meiotic stability to an adapted natural allopolyploid of Arabidopsis. Plant Cell 26:181–94 [Google Scholar]
  88. Heyman J, De Veylder L. 87.  2012. The anaphase-promoting complex/cyclosome in control of plant development. Mol. Plant 5:1182–94 [Google Scholar]
  89. Higgins JD, Armstrong SJ, Franklin FCH, Jones GH. 88.  2004. The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev. 18:2557–70 [Google Scholar]
  90. Higgins JD, Buckling EF, Franklin FCH, Jones GH. 89.  2008. Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. Plant J. 54:152–62 [Google Scholar]
  91. Higgins JD, Perry RM, Barakate A, Ramsay L, Waugh R. 90.  et al. 2012. Spatiotemporal asymmetry of the meiotic program underlies the predominantly distal distribution of meiotic crossovers in barley. Plant Cell 24:4096–109 [Google Scholar]
  92. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH. 91.  2005. The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev. 19:2488–500 [Google Scholar]
  93. Higgins JD, Vignard J, Mercier R, Pugh AG, Franklin FCH, Jones GH. 92.  2008. AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. Plant J. 55:28–39 [Google Scholar]
  94. Higgins JD, Wright KM, Bomblies K, Franklin FCH. 93.  2014. Cytological techniques to analyze meiosis in Arabidopsis arenosa for investigating adaptation to polyploidy. Front. Plant Sci. 4:546 [Google Scholar]
  95. Hollister JD, Arnold BJ, Svedin E, Xue KS, Dilkes BP, Bomblies K. 94.  2012. Genetic adaptation associated with genome-doubling in autotetraploid Arabidopsis arenosa. PLOS Genet. 8:e1003093 [Google Scholar]
  96. Hong L, Tang D, Zhu K, Wang K, Li M, Cheng Z. 95.  2012. Somatic and reproductive cell development in rice anther is regulated by a putative glutaredoxin. Plant Cell 24:577–88 [Google Scholar]
  97. Hörandl E. 96.  2009. A combinational theory for maintenance of sex. Heredity 103:445–57 [Google Scholar]
  98. Horton MW, Hancock AM, Huang YS, Toomajian C, Atwell S. 97.  et al. 2012. Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nat. Genet. 44:212–16 [Google Scholar]
  99. Hyppa RW, Smith GR. 98.  2010. Crossover invariance determined by partner choice for meiotic DNA break repair. Cell 142:243–55 [Google Scholar]
  100. Ishibashi T, Kimura S, Sakaguchi K. 99.  2006. A higher plant has three different types of RPA heterotrimeric complex. J. Biochem. 139:99–104 [Google Scholar]
  101. Iwata E, Ikeda S, Abe N, Kobayashi A, Kurata M. 100.  et al. 2012. Roles of GIG1 and UVI4 in genome duplication in Arabidopsis thaliana. Plant Signal. Behav. 7:1079–81 [Google Scholar]
  102. Izawa D, Goto M, Yamashita A, Yamano H, Yamamoto M. 101.  2005. Fission yeast Mes1p ensures the onset of meiosis II by blocking degradation of cyclin Cdc13p. Nature 434:529–33 [Google Scholar]
  103. Jackson N, Sanchez-Moran E, Buckling E, Armstrong SJ, Jones GH, Franklin FCH. 102.  2006. Reduced meiotic crossovers and delayed prophase I progression in AtMLH3-deficient Arabidopsis. EMBO J. 25:1315–23 [Google Scholar]
  104. Jahns MT, Vezon D, Chambon A, Pereira L, Falque M. 103.  et al. 2014. Crossover localisation is regulated by the neddylation posttranslational regulatory pathway. PLOS Biol. 12:e1001930 [Google Scholar]
  105. Jain M, Tyagi AK, Khurana JP. 104.  2006. Overexpression of putative topoisomerase 6 genes from rice confers stress tolerance in transgenic Arabidopsis plants. FEBS J. 273:5245–60 [Google Scholar]
  106. Jenczewski E, Alix K. 105.  2004. From diploids to allopolyploids: the emergence of efficient pairing control genes in plants. Crit. Rev. Plant Sci. 23:21–45 [Google Scholar]
  107. Jolivet S, Vezon D, Froger N, Mercier R. 106.  2006. Non conservation of the meiotic function of the Ski8/Rec103 homolog in Arabidopsis. Genes Cells 11:615–22 [Google Scholar]
  108. Kaul ML, Murthy TG. 107.  1985. Mutant genes affecting higher plant meiosis. Theor. Appl. Genet. 70:449–66 [Google Scholar]
  109. Kevei Z, Baloban M, Da Ines O, Tiricz H, Kroll A. 108.  et al. 2011. Conserved Cdc20 cell cycle functions are carried out by two of the five isoforms in Arabidopsis thaliana. PLOS ONE 6:e20618 [Google Scholar]
  110. Kim KP, Weiner BM, Zhang L, Jordan A, Dekker J, Kleckner NE. 109.  2010. Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143:924–37 [Google Scholar]
  111. Kimata Y, Trickey M, Izawa D, Gannon J, Yamamoto M, Yamano H. 110.  2008. A mutual inhibition between APC/C and its substrate Mes1 required for meiotic progression in fission yeast. Dev. Cell 14:446–54 [Google Scholar]
  112. Knoll A, Higgins JD, Seeliger K, Reha SJ, Dangel NJ. 111.  et al. 2012. The Fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic cells in Arabidopsis. Plant Cell 24:1448–64 [Google Scholar]
  113. Kong A, Gudbjartsson DF, Sainz J, Jonsdottir GM, Gudjonsson SA. 112.  et al. 2002. A high-resolution recombination map of the human genome. Nat. Genet. 31:241–47 [Google Scholar]
  114. Kumar R, Bourbon H-M, de Massy B. 113.  2010. Functional conservation of Mei4 for meiotic DNA double-strand break formation from yeasts to mice. Genes Dev. 24:1266–80 [Google Scholar]
  115. Kurzbauer M-T, Uanschou C, Chen D, Schlögelhofer P. 114.  2012. The recombinases DMC1 and RAD51 are functionally and spatially separated during meiosis in Arabidopsis. Plant Cell 24:2058–70 [Google Scholar]
  116. Lam SY, Horn SR, Radford SJ, Housworth EA, Stahl FW, Copenhaver GP. 115.  2005. Crossover interference on nucleolus organizing region-bearing chromosomes in Arabidopsis. Genetics 170:807–12 [Google Scholar]
  117. Lao JP, Cloud V, Huang C-C, Grubb J, Thacker D. 116.  et al. 2013. Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLOS Genet. 9:e1003978 [Google Scholar]
  118. Leflon M, Grandont L, Eber F, Huteau V, Coriton O. 117.  et al. 2010. Crossovers get a boost in Brassica allotriploid and allotetraploid hybrids. Plant Cell 22:2253–64 [Google Scholar]
  119. Li X, Dawe RK. 118.  2009. Fused sister kinetochores initiate the reductional division in meiosis I. Nat. Cell Biol. 11:1103–8 [Google Scholar]
  120. Liu S, Yeh C-T, Ji T, Ying K, Wu H. 119.  et al. 2009. Mu transposon insertion sites and meiotic recombination events co-localize with epigenetic marks for open chromatin across the maize genome. PLOS Genet. 5:e1000733 [Google Scholar]
  121. Liu Z, Makaroff CA. 120.  2006. Arabidopsis separase AESP is essential for embryo development and the release of cohesin during meiosis. Plant Cell 18:1213–25 [Google Scholar]
  122. Lloyd AH, Milligan AS, Langridge P, Able JA. 121.  2007. TaMSH7: a cereal mismatch repair gene that affects fertility in transgenic barley (Hordeum vulgare L.). BMC Plant Biol. 7:67 [Google Scholar]
  123. Lloyd AH, Ranoux M, Vautrin S, Glover N, Fourment J. 122.  et al. 2014. Meiotic gene evolution: Can you teach a new dog new tricks?. Mol. Biol. Evol. 31:1724–27 [Google Scholar]
  124. Louis EJ, Borts RH. 123.  2003. Meiotic recombination: too much of a good thing?. Curr. Biol. 13:R953–55 [Google Scholar]
  125. Lu P, Han X, Qi J, Yang J, Wijeratne AJ. 124.  et al. 2012. Analysis of Arabidopsis genome-wide variations before and after meiosis and meiotic recombination by resequencing Landsberg erecta and all four products of a single meiosis. Genome Res. 22:508–18 [Google Scholar]
  126. Lukaszewski AJ, Kopecky D, Linc G. 125.  2012. Inversions of chromosome arms 4AL and 2BS in wheat invert the patterns of chiasma distribution. Chromosoma 121:201–8 [Google Scholar]
  127. Luo Q, Tang D, Wang M, Luo W, Zhang L. 126.  et al. 2013. The role of OsMSH5 in crossover formation during rice meiosis. Mol. Plant 6:729–42 [Google Scholar]
  128. Macaisne N, Novatchkova M, Peirera L, Vezon D, Jolivet S. 127.  et al. 2008. SHOC1, an XPF endonuclease-related protein, is essential for the formation of class I meiotic crossovers. Curr. Biol. 18:1432–37 [Google Scholar]
  129. Macaisne N, Vignard J, Mercier R. 128.  2011. SHOC1 and PTD form an XPF-ERCC1-like complex that is required for formation of class I crossovers. J. Cell Sci. 124:2687–91 [Google Scholar]
  130. Madgwick S, Hansen DV, Levasseur M, Jackson PK, Jones KT. 129.  2006. Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis. J. Cell Biol. 174:791–801 [Google Scholar]
  131. Malik S-B, Ramesh MA, Hulstrand AM, Logsdon JM. 130.  2007. Protist homologs of the meiotic Spo11 gene and topoisomerase VI reveal an evolutionary history of gene duplication and lineage-specific loss. Mol. Biol. Evol. 24:2827–41 [Google Scholar]
  132. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM. 131.  2008. High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454:479–85 [Google Scholar]
  133. Marimuthu MP, Jolivet S, Ravi M, Pereira L, Davda JN. 132.  et al. 2011. Synthetic clonal reproduction through seeds. Science 331:876 [Google Scholar]
  134. Marston AL, Amon A. 133.  2004. Meiosis: cell-cycle controls shuffle and deal. Nat. Rev. Mol. Cell Biol. 5:983–97 [Google Scholar]
  135. Martinez M, Cuñado N, Carcelén N, Romero C. 134.  2001. The Ph1 and Ph2 loci play different roles in the synaptic behaviour of hexaploid wheat Triticum aestivum. Theor. Appl. Genet. 103:398–405 [Google Scholar]
  136. Mayer KFX, Rogers J, Doležel J, Pozniak C, Eversole K. 135.  et al. 2014. A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:1251788 [Google Scholar]
  137. Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L. 136.  et al. 2005. Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3, whereas the other one is not. Curr. Biol. 15:692–701 [Google Scholar]
  138. Miao C, Tang D, Zhang H, Wang M, Li Y. 137.  et al. 2013. CENTRAL REGION COMPONENT1, a novel synaptonemal complex component, is essential for meiotic recombination initiation in rice. Plant Cell 25:2998–3009 [Google Scholar]
  139. Muyt A, De Mercier R, Mézard C, Grelon M. 138.  2009. Meiotic recombination and crossovers in plants. Genome Dyn. 5:14–25 [Google Scholar]
  140. Myers S, Bottolo L, Freeman C, McVean G, Donnelly P. 139.  2005. A fine-scale map of recombination rates and hotspots across the human genome. Science 310:321–24 [Google Scholar]
  141. Myers S, Spencer CCA, Auton A, Bottolo L, Freeman C. 140.  et al. 2006. The distribution and causes of meiotic recombination in the human genome. Biochem. Soc. Trans. 34:526–30 [Google Scholar]
  142. Neale MJ, Pan J, Keeney S. 141.  2005. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436:1053–57 [Google Scholar]
  143. Nicolas SD, Leflon M, Monod H, Eber F, Coriton O. 142.  et al. 2009. Genetic regulation of meiotic cross-overs between related genomes in Brassica napus haploids and hybrids. Plant Cell 21:373–85 [Google Scholar]
  144. Nonomura K-I, Nakano M, Fukuda T, Eiguchi M, Miyao A. 143.  et al. 2004. The novel gene HOMOLOGOUS PAIRING ABERRATION IN RICE MEIOSIS1 of rice encodes a putative coiled-coil protein required for homologous chromosome pairing in meiosis. Plant Cell 16:1008–20 [Google Scholar]
  145. Nonomura K-I, Nakano M, Murata K, Miyoshi K, Eiguchi M. 144.  et al. 2004. An insertional mutation in the rice PAIR2 gene, the ortholog of Arabidopsis ASY1, results in a defect in homologous chromosome pairing during meiosis. Mol. Genet. Genomics 271:121–29 [Google Scholar]
  146. Ohe M, Inoue D, Kanemori Y, Sagata N. 145.  2007. Erp1/Emi2 is essential for the meiosis I to meiosis II transition in Xenopus oocytes. Dev. Biol. 303:157–64 [Google Scholar]
  147. Pecinka A, Fang W, Rehmsmeier M, Levy AA, Mittelsten Scheid O. 146.  2011. Polyploidization increases meiotic recombination frequency in Arabidopsis. BMC Biol. 9:24 [Google Scholar]
  148. Pesin JA, Orr-Weaver TL. 147.  2008. Regulation of APC/C activators in mitosis and meiosis. Annu. Rev. Cell Dev. Biol. 24:475–99 [Google Scholar]
  149. Puizina J, Siroky J, Mokros P, Schweizer D, Riha K. 148.  2004. MRE11 deficiency in Arabidopsis is associated with chromosomal instability in somatic cells and SPO11-dependent genome fragmentation during meiosis. Plant Cell 16:1968–78 [Google Scholar]
  150. Qi J, Chen Y, Copenhaver GP, Ma H. 149.  2014. Detection of genomic variations and DNA polymorphisms and impact on analysis of meiotic recombination and genetic mapping. PNAS 111:10007–12 [Google Scholar]
  151. Ramesh MA, Malik S-B, Logsdon JM. 150.  2005. A phylogenomic inventory of meiotic genes: evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr. Biol. 15:185–91 [Google Scholar]
  152. Ramsey J, Schemske DW. 151.  2002. Neopolyploidy in flowering plants. Annu. Rev. Ecol. Syst. 33:589–639 [Google Scholar]
  153. Riehs N, Akimcheva S, Puizina J, Bulankova P, Idol RA. 152.  et al. 2008. Arabidopsis SMG7 protein is required for exit from meiosis. J. Cell Sci. 121:2208–16 [Google Scholar]
  154. Ronceret A, Doutriaux M-P, Golubovskaya IN, Pawlowski WP. 153.  2009. PHS1 regulates meiotic recombination and homologous chromosome pairing by controlling the transport of RAD50 to the nucleus. PNAS 106:20121–26 [Google Scholar]
  155. Sakaguchi K, Ishibashi T, Uchiyama Y, Iwabata K. 154.  2009. The multi-replication protein A (RPA) system—a new perspective. FEBS J. 276:943–63 [Google Scholar]
  156. Sanchez-Moran E, Osman K, Higgins JD, Pradillo M, Cuñado N. 155.  et al. 2008. ASY1 coordinates early events in the plant meiotic recombination pathway. Cytogenet. Genome Res. 120:302–12 [Google Scholar]
  157. Sanchez-Moran E, Santos J-L, Jones GH, Franklin FCH. 156.  2007. ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev. 21:2220–33 [Google Scholar]
  158. Sebastian J, Ravi M, Andreuzza S, Panoli AP, Marimuthu MPA, Siddiqi I. 157.  2009. The plant adherin AtSCC2 is required for embryogenesis and sister-chromatid cohesion during meiosis in Arabidopsis. Plant J. 59:1–13 [Google Scholar]
  159. Sekelsky JJ, McKim KS, Chin GM, Hawley RS. 158.  1995. The Drosophila meiotic recombination gene mei-9 encodes a homologue of the yeast excision repair protein Rad1. Genetics 141:619–27 [Google Scholar]
  160. Shao T, Tang D, Wang K, Wang M, Che L. 159.  et al. 2011. OsREC8 is essential for chromatid cohesion and metaphase I monopolar orientation in rice meiosis. Plant Physiol. 156:1386–96 [Google Scholar]
  161. Shen Y, Tang D, Wang K, Wang M, Huang J. 160.  et al. 2012. ZIP4 in homologous chromosome synapsis and crossover formation in rice meiosis. J. Cell Sci. 125:2581–91 [Google Scholar]
  162. Sheridan SD, Yu X, Roth R, Heuser JE, Sehorn MG. 161.  et al. 2008. A comparative analysis of Dmc1 and Rad51 nucleoprotein filaments. Nucleic Acids Res. 36:4057–66 [Google Scholar]
  163. Siaud N, Dray E, Gy I, Gérard E, Takvorian N, Doutriaux M-P. 162.  2004. BRCA2 is involved in meiosis in Arabidopsis thaliana as suggested by its interaction with DMC1. EMBO J. 23:1392–401 [Google Scholar]
  164. Singh DK, Andreuzza S, Panoli AP, Siddiqi I. 163.  2013. AtCTF7 is required for establishment of sister chromatid cohesion and association of cohesin with chromatin during meiosis in Arabidopsis. BMC Plant Biol. 13:117 [Google Scholar]
  165. Sommermeyer V, Beneut C, Chaplais E, Serrentino ME, Borde V. 164.  2013. Spp1, a member of the Set1 complex, promotes meiotic DSB formation in promoters by tethering histone H3K4 methylation sites to chromosome axes. Mol. Cell 49:43–54 [Google Scholar]
  166. Stacey NJ, Kuromori T, Azumi Y, Roberts G, Breuer C. 165.  et al. 2006. Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J. 48:206–16 [Google Scholar]
  167. Suay L, Zhang D, Lod M, Huteau V, Coriton O. 166.  et al. 2013. Crossover rate between homologous chromosomes and interference are regulated by the addition of specific unpaired chromosomes in Brassica. New Phytol. 201:645–56 [Google Scholar]
  168. Sugimoto-Shirasu K, Stacey NJ, Corsar J, Roberts K, McCann MC. 167.  2002. DNA topoisomerase VI is essential for endoreduplication in Arabidopsis. Curr. Biol. 12:1782–86 [Google Scholar]
  169. Sun Y, Ambrose JH, Haughey BS, Webster TD, Pierrie SN. 168.  et al. 2012. Deep genome-wide measurement of meiotic gene conversion using tetrad analysis in Arabidopsis thaliana. PLOS Genet. 8:e1002968 [Google Scholar]
  170. Sutton T, Whitford R, Baumann U, Dong C, Able JA, Langridge P. 169.  2003. The Ph2 pairing homoeologous locus of wheat (Triticum aestivum): identification of candidate meiotic genes using a comparative genetics approach. Plant J. 36:443–56 [Google Scholar]
  171. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW. 170.  1983. The double-strand-break repair model for recombination. Cell 33:25–35 [Google Scholar]
  172. Tang W, Wu JQ, Guo Y, Hansen DV, Perry JA. 171.  et al. 2008. Cdc2 and Mos regulate Emi2 stability to promote the meiosis I-meiosis II transition. Mol. Biol. Cell 19:3536–43 [Google Scholar]
  173. Tsubouchi H, Roeder GS. 172.  2006. Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev. 20:1766–75 [Google Scholar]
  174. Uanschou C, Ronceret A, Von Harder M, De Muyt A, Vezon D. 173.  et al. 2013. Sufficient amounts of functional HOP2/MND1 complex promote interhomolog DNA repair but are dispensable for intersister DNA repair during meiosis in Arabidopsis. Plant Cell 25:4924–40 [Google Scholar]
  175. Uanschou C, Siwiec T, Pedrosa-Harand A, Kerzendorfer C, Sanchez-Moran E. 174.  et al. 2007. A novel plant gene essential for meiosis is related to the human CtIP and the yeast COM1/SAE2 gene. EMBO J. 26:5061–70 [Google Scholar]
  176. Vignard J, Siwiec T, Chelysheva L, Vrielynck N, Gonord F. 175.  et al. 2007. The interplay of RECA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLOS Genet. 3:1894–906 [Google Scholar]
  177. Villeneuve AM, Hillers KJ. 176.  2001. Whence meiosis?. Cell 106:647–50 [Google Scholar]
  178. Wang K, Tang D, Wang M, Lu J, Yu H. 177.  et al. 2009. MER3 is required for normal meiotic crossover formation, but not for presynaptic alignment in rice. J. Cell Sci. 122:2055–63 [Google Scholar]
  179. Wang K, Wang M, Tang D, Shen Y, Miao C. 178.  et al. 2012. The role of rice HEI10 in the formation of meiotic crossovers. PLOS Genet. 8:e1002809 [Google Scholar]
  180. Wang M, Tang D, Wang K, Shen Y, Qin B. 179.  et al. 2011. OsSGO1 maintains synaptonemal complex stabilization in addition to protecting centromeric cohesion during rice meiosis. Plant J. 67:583–94 [Google Scholar]
  181. Wang M, Wang K, Tang D, Wei C, Li M. 180.  et al. 2010. The central element protein ZEP1 of the synaptonemal complex regulates the number of crossovers during meiosis in rice. Plant Cell 22:417–30 [Google Scholar]
  182. Watanabe Y. 181.  2012. Geometry and force behind kinetochore orientation: lessons from meiosis. Nat. Rev. Mol. Cell Biol. 13:370–82 [Google Scholar]
  183. Waterworth WM, Altun C, Armstrong SJ, Roberts N, Dean PJ. 182.  et al. 2007. NBS1 is involved in DNA repair and plays a synergistic role with ATM in mediating meiotic homologous recombination in plants. Plant J. 52:41–52 [Google Scholar]
  184. Wijeratne AJ, Chen C, Zhang W, Timofejeva L, Ma H. 183.  2006. The Arabidopsis thaliana PARTING DANCERS gene encoding a novel protein is required for normal meiotic homologous recombination. Mol. Biol. Cell 17:1331–43 [Google Scholar]
  185. Wijnker E, Schnittger A. 184.  2013. Control of the meiotic cell division program in plants. Plant Reprod. 26:143–58 [Google Scholar]
  186. Wijnker E, van Dun K, de Snoo CB, Lelivelt CLC, Keurentjes JJB. 185.  et al. 2012. Reverse breeding in Arabidopsis thaliana generates homozygous parental lines from a heterozygous plant. Nat. Genet. 44:467–70 [Google Scholar]
  187. Wijnker E, Velikkakam James G, Ding J, Becker F, Klasen JR. 186.  et al. 2013. The genomic landscape of meiotic crossovers and gene conversions in Arabidopsis thaliana. eLife 2:e01426 [Google Scholar]
  188. Wu L, Hickson ID. 187.  2003. The bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426:870–74 [Google Scholar]
  189. Xu X, Hsia AP, Zhang L, Nikolau BJ, Schnable PS. 188.  1995. Meiotic recombination break points resolve at high rates at the 5′ end of a maize coding sequence. Plant Cell 7:2151–61 [Google Scholar]
  190. Yant L, Hollister JD, Wright KM, Arnold BJ, Higgins JD. 189.  et al. 2013. Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr. Biol. 23:2151–56 [Google Scholar]
  191. Yao H, Zhou Q, Li J, Smith H, Yandeau M. 190.  et al. 2002. Molecular characterization of meiotic recombination across the 140-kb multigenic a1-sh2 interval of maize. PNAS 99:6157–62 [Google Scholar]
  192. Yelina NE, Choi K, Chelysheva L, Macaulay M, de Snoo B. 191.  et al. 2012. Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLOS Genet. 8:e1002844 [Google Scholar]
  193. Yin Y, Cheong H, Friedrichsen D, Zhao Y, Hu J. 192.  et al. 2002. A crucial role for the putative Arabidopsis topoisomerase VI in plant growth and development. PNAS 99:10191–96 [Google Scholar]
  194. Yu H, Wang M, Tang D, Wang K, Chen F. 193.  et al. 2010. OsSPO11-1 is essential for both homologous chromosome pairing and crossover formation in rice. Chromosoma 119:625–36 [Google Scholar]
  195. Yuan W, Li X, Chang Y, Wen R, Chen G. 194.  et al. 2009. Mutation of the rice gene PAIR3 results in lack of bivalent formation in meiosis. Plant J. 59:303–15 [Google Scholar]
  196. Zakharyevich K, Tang S, Ma Y, Hunter N. 195.  2012. Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149:334–47 [Google Scholar]
  197. Zamariola L, De Storme N, Vannerum K, Vandepoele K, Armstrong SJ. 196.  et al. 2014. SHUGOSHINs and PATRONUS protect meiotic centromere cohesion in Arabidopsis thaliana. Plant J. 77:782–94 [Google Scholar]
  198. Zhang C, Song Y, Cheng Z-H, Wang Y-X, Zhu J. 197.  et al. 2012. The Arabidopsis thaliana DSB formation (AtDFO) gene is required for meiotic double-strand break formation. Plant J. 72:271–81 [Google Scholar]
  199. Zhang L, Ma H. 198.  2012. Complex evolutionary history and diverse domain organization of set proteins suggest divergent regulatory interactions. New Phytol. 195:248–63 [Google Scholar]
  200. Zhang L, Wang S, Yin S, Hong S, Kim KP, Kleckner N. 199.  2014. Topoisomerase II mediates meiotic crossover interference. Nature 511:551–56 [Google Scholar]

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