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Annual Review of Plant Biology

Volume 69, 2018

Meiotic Recombination: Mixing It Up in Plants

Abstract

Meiosis halves diploid chromosome numbers to haploid levels that are essential for sexual reproduction in most eukaryotes. Meiotic recombination ensures the formation of bivalents between homologous chromosomes (homologs) and their subsequent proper segregation. It also results in genetic diversity among progeny that influences evolutionary responses to selection. Moreover, crop breeding depends upon the action of meiotic recombination to rearrange elite traits between parental chromosomes. An understanding of the molecular mechanisms that drive meiotic recombination is important for both fundamental research and practical applications. This review emphasizes advances made during the past 5 years, primarily in and rice, by summarizing newly characterized genes and proteins and examining the regulatory mechanisms that modulate their action.

Keyword(s): crossover, crossover distribution, double-strand break, DSB, gene conversion, meiosis, meiotic recombination
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/content/journals/10.1146/annurev-arplant-042817-040431
2018-04-29
2024-04-23
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Literature Cited

  1. Abe K, Osakabe K, Nakayama S, Endo M, Tagiri A. 1.  et al. 2005. Arabidopsis RAD51C gene is important for homologous recombination in meiosis and mitosis. Plant Physiol 139:896–908 [Google Scholar]
  2. Acquaviva L, Drogat J, Dehe PM, de La Roche Saint-Andre C, Geli V. 2.  2013. Spp1 at the crossroads of H3K4me3 regulation and meiotic recombination. Epigenetics 8:355–60 [Google Scholar]
  3. Acquaviva L, Székvölgyi L, Dichtl B, Dichtl BS, de La Roche Saint André C. 3.  et al. 2013. The COMPASS subunit Spp1 links histone methylation to initiation of meiotic recombination. Science 339:215–18 [Google Scholar]
  4. Aklilu BB, Soderquist RS, Culligan KM. 4.  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]
  5. Allers T, Lichten M. 5.  2001. Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106:47–57 [Google Scholar]
  6. An XJ, Deng ZY, Wang T. 6.  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]
  7. Anderson LK, Doyle GG, Brigham B, Carter J, Hooker KD. 7.  et al. 2003. High-resolution crossover maps for each bivalent of Zea mays using recombination nodules. Genetics 165:849–65 [Google Scholar]
  8. Anderson LK, Lohmiller LD, Tang X, Hammond DB, Javernick L. 8.  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]
  9. Andreuzza S, Nishal B, Singh A, Siddiqi I. 9.  2015. The chromatin protein DUET/MMD1 controls expression of the meiotic gene TDM1 during male meiosis in Arabidopsis. PLOS Genet 11:e1005396 [Google Scholar]
  10. Andronic L.10.  2012. Viruses as triggers of DNA rearrangements in host plants. Can. J. Plant Sci. 92:1083–91 [Google Scholar]
  11. Azumi Y, Liu D, Zhao D, Li W, Wang G. 11.  et al. 2002. Homolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein. EMBO J 21:3081–95 [Google Scholar]
  12. Bao Y, Shen X. 12.  2007. SnapShot: chromatin remodeling complexes. Cell 129:632 [Google Scholar]
  13. Barth S, Melchinger AE, Devezi-Savula B, Lubberstedt T. 13.  2000. A high-throughput system for genome-wide measurement of genetic recombination in Arabidopsis thaliana based on transgenic markers. Funct. Integr. Genom. 1:200–6 [Google Scholar]
  14. Barton AB, Pekosz MR, Kurvathi RS, Kaback DB. 14.  2008. Meiotic recombination at the ends of chromosomes in Saccharomyces cerevisiae. Genetics 179:1221–35 [Google Scholar]
  15. Barton AB, Su Y, Lamb J, Barber D, Kaback DB. 15.  2003. A function for subtelomeric DNA in Saccharomyces cerevisiae. Genetics 165:929–34 [Google Scholar]
  16. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C. 16.  et al. 2010. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327:836–40 [Google Scholar]
  17. Baudat F, Imai Y, de Massy B. 17.  2013. Meiotic recombination in mammals: localization and regulation. Nat. Rev. Genet. 14:794–806 [Google Scholar]
  18. Baudry E, Kerdelhue C, Innan H, Stephan W. 18.  2001. Species and recombination effects on DNA variability in the tomato genus. Genetics 158:1725–35 [Google Scholar]
  19. Bauknecht M, Kobbe D. 19.  2014. AtGEN1 and AtSEND1, two paralogs in Arabidopsis, possess Holliday junction resolvase activity. Plant Physiol 166:202–16 [Google Scholar]
  20. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP. 20.  2007. The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLOS Genet 3:e132 [Google Scholar]
  21. Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P. 21.  1997. An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386:414–17 [Google Scholar]
  22. Bleuyard JY, White CI. 22.  2004. The Arabidopsis homologue of Xrcc3 plays an essential role in meiosis. EMBO J 23:439–49 [Google Scholar]
  23. Blitzblau HG, Bell GW, Rodriguez J, Bell SP, Hochwagen A. 23.  2007. Mapping of meiotic single-stranded DNA reveals double-strand-break hotspots near centromeres and telomeres. Curr. Biol. 17:2003–12 [Google Scholar]
  24. Bomblies K, Jones G, Franklin C, Zickler D, Kleckner N. 24.  2016. The challenge of evolving stable polyploidy: Could an increase in “crossover interference distance” play a central role?. Chromosoma 125:287–300 [Google Scholar]
  25. Borde V, de Massy B. 25.  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]
  26. Borde V, Robine N, Lin W, Bonfils S, Geli V, Nicolas A. 26.  2009. Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J 28:99–111 [Google Scholar]
  27. Boyko A, Kathiria P, Zemp FJ, Yao Y, Pogribny I, Kovalchuk I. 27.  2007. Transgenerational changes in the genome stability and methylation in pathogen-infected plants (virus-induced plant genome instability). Nucleic Acids Res 35:1714–25 [Google Scholar]
  28. Brick K, Smagulova F, Khil P, Camerini-Otero RD, Petukhova GV. 28.  2012. Genetic recombination is directed away from functional genomic elements in mice. Nature 485:642–45 [Google Scholar]
  29. Broman KW, Rowe LB, Churchill GA, Paigen K. 29.  2002. Crossover interference in the mouse. Genetics 160:1123–31 [Google Scholar]
  30. Broman KW, Weber JL. 30.  2000. Characterization of human crossover interference. Am. J. Hum. Genet. 66:1911–26 [Google Scholar]
  31. Brown MS, Bishop DK. 31.  2014. DNA strand exchange and RecA homologs in meiosis. Cold Spring Harb. Perspect. Biol. 7:a016659 [Google Scholar]
  32. Cahoon CK, Hawley RS. 32.  2016. Regulating the construction and demolition of the synaptonemal complex. Nat. Struct. Mol. Biol. 23:369–77 [Google Scholar]
  33. Calvente A, Viera A, Page J, Parra MT, Gomez R. 33.  et al. 2005. DNA double-strand breaks and homology search: inferences from a species with incomplete pairing and synapsis. J. Cell Sci. 118:2957–63 [Google Scholar]
  34. Chai B, Huang J, Cairns BR, Laurent BC. 34.  2005. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev 19:1656–61 [Google Scholar]
  35. Chakraborty P, Pankajam AV, Lin G, Dutta A, Krishnaprasad GN. 35.  et al. 2017. Modulating crossover frequency and interference for obligate crossovers in Saccharomyces cerevisiae meiosis. G3 71511–24
  36. Chambers SR, Hunter N, Louis EJ, Borts RH. 36.  1996. The mismatch repair system reduces meiotic homeologous recombination and stimulates recombination-dependent chromosome loss. Mol. Cell. Biol. 16:6110–20 [Google Scholar]
  37. Chang Y, Gong L, Yuan W, Li X, Chen G. 37.  et al. 2009. Replication protein A (RPA1a) is required for meiotic and somatic DNA repair but is dispensable for DNA replication and homologous recombination in rice. Plant Physiol 151:2162–73 [Google Scholar]
  38. Che L, Wang K, Tang D, Liu Q, Chen X. 38.  et al. 2014. OsHUS1 facilitates accurate meiotic recombination in rice. PLOS Genet 10:e1004405 [Google Scholar]
  39. Chelysheva L, Vezon D, Chambon A, Gendrot G, Pereira L. 39.  et al. 2012. The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLOS Genet 8:e1002799 [Google Scholar]
  40. Chen N, Zhou WB, Wang YX, Dong AW, Yu Y. 40.  2014. Polycomb-group histone methyltransferase CLF is required for proper somatic recombination in Arabidopsis. J. Integr. Plant Biol 56:550–58 [Google Scholar]
  41. Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR. 41.  et al. 2008. Global analysis of the meiotic crossover landscape. Dev. Cell 15:401–15 [Google Scholar]
  42. Cheng CH, Lo YH, Liang SS, Ti SC, Lin FM. 42.  et al. 2006. SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 20:2067–81 [Google Scholar]
  43. Choi K, Henderson IR. 43.  2015. Meiotic recombination hotspots—a comparative view. Plant J 83:52–61 [Google Scholar]
  44. Choi K, Zhao X, Kelly KA, Venn O, Higgins JD. 44.  et al. 2013. Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters. Nat. Genet. 45:1327–36 [Google Scholar]
  45. Clapier CR, Cairns BR. 45.  2009. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78:273–304 [Google Scholar]
  46. Cloud V, Chan YL, Grubb J, Budke B, Bishop DK. 46.  2012. Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 337:1222–25 [Google Scholar]
  47. Cole F, Baudat F, Grey C, Keeney S, de Massy B, Jasin M. 47.  2014. Mouse tetrad analysis provides insights into recombination mechanisms and hotspot evolutionary dynamics. Nat. Genet. 46:1072–80 [Google Scholar]
  48. Cole F, Keeney S, Jasin M. 48.  2010. Comprehensive, fine-scale dissection of homologous recombination outcomes at a hot spot in mouse meiosis. Mol. Cell 39:700–10 [Google Scholar]
  49. Colome-Tatche M, Cortijo S, Wardenaar R, Morgado L, Lahouze B. 49.  et al. 2012. Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. PNAS 109:16240–45 [Google Scholar]
  50. Cooper TJ, Wardell K, Garcia V, Neale MJ. 50.  2014. Homeostatic regulation of meiotic DSB formation by ATM/ATR. Exp. Cell Res. 329:124–31 [Google Scholar]
  51. Copenhaver GP, Housworth EA, Stahl FW. 51.  2002. Crossover interference in Arabidopsis. Genetics 160:1631–39 [Google Scholar]
  52. Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, Doutriaux MP. 52.  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]
  53. Crismani W, Girard C, Froger N, Pradillo M, Santos JL. 53.  et al. 2012. FANCM limits meiotic crossovers. Science 336:1588–90 [Google Scholar]
  54. Culligan KM, Britt AB. 54.  2008. Both ATM and ATR promote the efficient and accurate processing of programmed meiotic double-strand breaks. Plant J 55:629–38 [Google Scholar]
  55. Da Ines O, Abe K, Goubely C, Gallego ME, White CI. 55.  2012. Differing requirements for RAD51 and DMC1 in meiotic pairing of centromeres and chromosome arms in Arabidopsis thaliana. PLOS Genet 8:e1002636 [Google Scholar]
  56. Da Ines O, Degroote F, Amiard S, Goubely C, Gallego ME, White CI. 56.  2013. Effects of XRCC2 and RAD51B mutations on somatic and meiotic recombination in Arabidopsis thaliana. Plant J 74:959–70 [Google Scholar]
  57. Da Ines O, Degroote F, Goubely C, Amiard S, Gallego ME, White CI. 57.  2013. Meiotic recombination in Arabidopsis is catalysed by DMC1, with RAD51 playing a supporting role. PLOS Genet 9:e1003787 [Google Scholar]
  58. De Muyt A, Pereira L, Vezon D, Chelysheva L, Gendrot G. 58.  et al. 2009. A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLOS Genet 5:e1000654 [Google Scholar]
  59. De Muyt A, Vezon D, Gendrot G, Gallois JL, Stevens R, Grelon M. 59.  2007. AtPRD1 is required for meiotic double strand break formation in Arabidopsis thaliana. EMBO J 26:4126–37 [Google Scholar]
  60. Demirci S, van Dijk ADJ, Sanchez Perez G, Aflitos SA, de Ridder D, Peters SA. 60.  2017. Distribution, position and genomic characteristics of crossovers in tomato recombinant inbred lines derived from an interspecific cross between Solanum lycopersicum and Solanum pimpinellifolium. Plant J 89:554–64 [Google Scholar]
  61. Desai A, Chee PW, Rong J, May OL, Paterson AH. 61.  2006. Chromosome structural changes in diploid and tetraploid A genomes of Gossypium. Genome 49:336–45 [Google Scholar]
  62. Doonan JH, Kitsios G. 62.  2009. Functional evolution of cyclin-dependent kinases. Mol. Biotechnol. 42:14–29 [Google Scholar]
  63. Drouaud J, Khademian H, Giraut L, Zanni V, Bellalou S. 63.  et al. 2013. Contrasted patterns of crossover and non-crossover at Arabidopsis thaliana meiotic recombination hotspots. PLOS Genet 9:e1003922 [Google Scholar]
  64. Drouaud J, Mercier R, Chelysheva L, Berard A, Falque M. 64.  et al. 2007. Sex-specific crossover distributions and variations in interference level along Arabidopsis thaliana chromosome 4. PLOS Genet 3:e106 [Google Scholar]
  65. Dubin MJ, Zhang P, Meng D, Remigereau MS, Osborne EJ. 65.  et al. 2015. DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. eLife 4:e05255 [Google Scholar]
  66. Duroc Y, Kumar R, Ranjha L, Adam C, Guerois R. 66.  et al. 2017. Concerted action of the MutLβ heterodimer and Mer3 helicase regulates the global extent of meiotic gene conversion. eLife 6:e21900 [Google Scholar]
  67. Durrant WE, Wang S, Dong XN. 67.  2007. Arabidopsis SNI1 and RAD51D regulate both gene transcription and DNA recombination during the defense response. PNAS 104:4223–27 [Google Scholar]
  68. Dvorak J, Luo MC, Yang ZL. 68.  1998. Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing Aegilops species. Genetics 148:423–34 [Google Scholar]
  69. Ellermeier C, Higuchi EC, Phadnis N, Holm L, Geelhood JL. 69.  et al. 2010. RNAi and heterochromatin repress centromeric meiotic recombination. PNAS 107:8701–5 [Google Scholar]
  70. Elliot CG.70.  1955. The effect of temperature on chiasma frequency. Heredity 9:385–98 [Google Scholar]
  71. Falque M, Anderson LK, Stack SM, Gauthier F, Martin OC. 71.  2009. Two types of meiotic crossovers coexist in maize. Plant Cell 21:3915–25 [Google Scholar]
  72. Fasching CL, Cejka P, Kowalczykowski SC, Heyer WD. 72.  2015. Top3-Rmi1 dissolve Rad51-mediated D loops by a topoisomerase-based mechanism. Mol. Cell 57:595–606 [Google Scholar]
  73. Fernandes JB, Duhamel M, Seguela-Arnaud M, Froger N, Girard C, Choinard S. 73.  et al. 2017. FIGL1 and its novel partner FLIP form a conserved complex that regulates homologous recombination. bioRxiv159657 https://doi.org/10.1101/159657 [Crossref]
  74. Fernandes JB, Seguela-Arnaud M, Larchevêque C, Lloyd AH, Mercier R. 74.  2017. Unleashing meiotic crossovers in hybrid plants. bioRxiv159640 https://doi.org/10.1101/159640 [Crossref]
  75. Flaus A, Martin DM, Barton GJ, Owen-Hughes T. 75.  2006. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res 34:2887–905 [Google Scholar]
  76. Francis KE, Lam SY, Harrison BD, Bey AL, Berchowitz LE, Copenhaver GP. 76.  2007. Pollen tetrad-based visual assay for meiotic recombination in Arabidopsis. PNAS 104:3913–18 [Google Scholar]
  77. Fritsch O, Benvenuto G, Bowler C, Molinier J, Hohn B. 77.  2004. The INO80 protein controls homologous recombination in Arabidopsis thaliana. Mol. Cell 16:479–85 [Google Scholar]
  78. Fu M, Wang C, Xue F, Higgins J, Chen M. 78.  et al. 2016. The DNA topoisomerase VI-B subunit OsMTOPVIB is essential for meiotic recombination initiation in rice. Mol. Plant 9:1539–41 [Google Scholar]
  79. Gari K, Decaillet C, Stasiak AZ, Stasiak A, Constantinou A. 79.  2008. The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. Mol. Cell 29:141–48 [Google Scholar]
  80. Girard C, Chelysheva L, Choinard S, Froger N, Macaisne N. 80.  et al. 2015. AAA-ATPase FIDGETIN-LIKE 1 and helicase FANCM antagonize meiotic crossovers by distinct mechanisms. PLOS Genet 11:e1005369 [Google Scholar]
  81. Girard C, Crismani W, Froger N, Mazel J, Lemhemdi A. 81.  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]
  82. Giraut L, Falque M, Drouaud J, Pereira L, Martin OC, Mezard C. 82.  2011. Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLOS Genet 7:e1002354 [Google Scholar]
  83. Golubovskaya IN, Harper LC, Pawlowski WP, Schichnes D, Cande WZ. 83.  2002. The pam1 gene is required for meiotic bouquet formation and efficient homologous synapsis in maize (Zea mays L.). Genetics 162:1979–93 [Google Scholar]
  84. Grandont L, Jenczewski E, Lloyd A. 84.  2013. Meiosis and its deviations in polyploid plants. Cytogenet. Genome Res. 140:171–84 [Google Scholar]
  85. Gray S, Cohen PE. 85.  2016. Control of meiotic crossovers: from double-strand break formation to designation. Annu. Rev. Genet. 50:175–210 [Google Scholar]
  86. Grelon M, Vezon D, Gendrot G, Pelletier G. 86.  2001. AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20:589–600 [Google Scholar]
  87. Grey C, Sommermeyer V, Borde V, de Massy B. 87.  2011. [What defines the genetic map? The specification of meiotic recombination sites]. Med. Sci. 27:63–69 [Google Scholar]
  88. Halldorsson BV, Hardarson MT, Kehr B, Styrkarsdottir U, Gylfason A. 88.  et al. 2016. The rate of meiotic gene conversion varies by sex and age. Nat. Genet. 48:1377–84 [Google Scholar]
  89. Hartung F, Suer S, Puchta H. 89.  2007. Two closely related RecQ helicases have antagonistic roles in homologous recombination and DNA repair in Arabidopsis thaliana. PNAS 104:18836–41 [Google Scholar]
  90. Hartung F, Wurz-Wildersinn R, Fuchs J, Schubert I, Suer S, Puchta H. 90.  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]
  91. Henderson IR.91.  2012. Control of meiotic recombination frequency in plant genomes. Curr. Opin. Plant Biol. 15:556–61 [Google Scholar]
  92. Higgins JD, Buckling EF, Franklin FC, Jones GH. 92.  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]
  93. Higgins JD, Osman K, Jones GH, Franklin FC. 93.  2014. Factors underlying restricted crossover localization in barley meiosis. Annu. Rev. Genet. 48:29–47 [Google Scholar]
  94. Higgins JD, Perry RM, Barakate A, Ramsay L, Waugh R. 94.  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]
  95. Hochwagen A, Marais GA. 95.  2010. Meiosis: a PRDM9 guide to the hotspots of recombination. Curr. Biol. 20:R271–74 [Google Scholar]
  96. Horton MW, Hancock AM, Huang YS, Toomajian C, Atwell S. 96.  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]
  97. Hu Q, Li Y, Wang H, Shen Y, Zhang C. 97.  et al. 2017. Meiotic chromosome association 1 interacts with TOP3α and regulates meiotic recombination in rice. Plant Cell 29:1697–708 [Google Scholar]
  98. Hu Q, Tang D, Wang H, Shen Y, Chen X. 98.  et al. 2016. The exonuclease homolog OsRAD1 promotes accurate meiotic double-strand break repair by suppressing nonhomologous end joining. Plant Physiol 172:1105–16 [Google Scholar]
  99. Huang JY, Cheng Z, Wang C, Hong Y, Su H. 99.  et al. 2015. Formation of interference-sensitive meiotic cross-overs requires sufficient DNA leading-strand elongation. PNAS 112:12534–39 [Google Scholar]
  100. Huang JY, Copenhaver GP, Ma H, Wang YX. 100.  2016. New insights into the role of DNA synthesis in meiotic recombination. Sci. Bull. 61:1260–69 [Google Scholar]
  101. Hunter CM, Huang W, Mackay TF, Singh ND. 101.  2016. The genetic architecture of natural variation in recombination rate in Drosophila melanogaster. PLOS Genet 12:e1005951 [Google Scholar]
  102. Hunter N.102.  2015. Meiotic recombination: the essence of heredity. Cold Spring Harb. Perspect. Biol. 7:a016618 [Google Scholar]
  103. 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]
  104. Jensen-Seaman MI, Furey TS, Payseur BA, Lu Y, Roskin KM. 104.  et al. 2004. Comparative recombination rates in the rat, mouse, and human genomes. Genome Res 14:528–38 [Google Scholar]
  105. Ji JH, Tang D, Shen Y, Xue Z, Wang H. 105.  et al. 2016. P31comet, a member of the synaptonemal complex, participates in meiotic DSB formation in rice. PNAS 113:10577–82 [Google Scholar]
  106. Ji JH, Tang D, Wang KJ, Wang M, Che LX. 106.  et al. 2012. The role of OsCOM1 in homologous chromosome synapsis and recombination in rice meiosis. Plant J 72:18–30 [Google Scholar]
  107. Ji JH, Tang D, Wang M, Li YF, Zhang L. 107.  et al. 2013. MRE11 is required for homologous synapsis and DSB processing in rice meiosis. Chromosoma 122:363–76 [Google Scholar]
  108. Joshi N, Brown MS, Bishop DK, Borner GV. 108.  2015. Gradual implementation of the meiotic recombination program via checkpoint pathways controlled by global DSB levels. Mol. Cell 57:797–811 [Google Scholar]
  109. Kawabe A, Forrest A, Wright SI, Charlesworth D. 109.  2008. High DNA sequence diversity in pericentromeric genes of the plant Arabidopsis lyrata. Genetics 179:985–95 [Google Scholar]
  110. Keeney S.110.  2008. Spo11 and the formation of DNA double-strand breaks in meiosis. Genome Dyn. Stab. 2:81–123 [Google Scholar]
  111. Keeney S, Giroux CN, Kleckner N. 111.  1997. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375–84 [Google Scholar]
  112. Keeney S, Lange J, Mohibullah N. 112.  2014. Self-organization of meiotic recombination initiation: general principles and molecular pathways. Annu. Rev. Genet. 48:187–214 [Google Scholar]
  113. Kleckner N, Storlazzi A, Zickler D. 113.  2003. Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length. Trends Genet 19:623–28 [Google Scholar]
  114. Kniewel R, Keeney S. 114.  2009. Histone methylation sets the stage for meiotic DNA breaks. EMBO J 28:81–83 [Google Scholar]
  115. Knoll A, Higgins JD, Seeliger K, Reha SJ, Dangel NJ. 115.  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]
  116. Komiya R, Ohyanagi H, Niihama M, Watanabe T, Nakano M. 116.  et al. 2014. Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. Plant J 78:385–97 [Google Scholar]
  117. Kovalchuk I, Kovalchuk O, Kalck V, Boyko V, Filkowski J. 117.  et al. 2003. Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 423:760–62 [Google Scholar]
  118. Kumar SV, Wigge PA. 118.  2010. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–47 [Google Scholar]
  119. Lake CM, Hawley RS. 119.  2016. Becoming a crossover-competent DSB. Semin. Cell Dev. Biol. 54:117–25 [Google Scholar]
  120. Lam I, Keeney S. 120.  2014. Mechanism and regulation of meiotic recombination initiation. Cold Spring Harb. Perspect. Biol. 7:a016634 [Google Scholar]
  121. Lam I, Mohibullah N, Keeney S. 121.  2017. Sequencing Spo11 oligonucleotides for mapping meiotic DNA double-strand breaks in yeast. Methods Mol. Biol. 1471:51–98 [Google Scholar]
  122. Lambing C, Franklin FC, Wang CR. 122.  2017. Understanding and manipulating meiotic recombination in plants. Plant Physiol 173:1530–42 [Google Scholar]
  123. Lambing C, Osman K, Nuntasoontorn K, West A, Higgins JD. 123.  et al. 2015. Arabidopsis PCH2 mediates meiotic chromosome remodeling and maturation of crossovers. PLOS Genet 11:e1005372 [Google Scholar]
  124. Lange J, Pan J, Cole F, Thelen MP, Jasin M, Keeney S. 124.  2011. ATM controls meiotic double-strand-break formation. Nature 479:237–40 [Google Scholar]
  125. Leflon M, Grandont L, Eber F, Huteau V, Coriton O. 125.  et al. 2010. Crossovers get a boost in Brassica allotriploid and allotetraploid hybrids. Plant Cell 22:2253–64 [Google Scholar]
  126. Li W, Chen C, Markmann-Mulisch U, Timofejeva L, Schmelzer E. 126.  et al. 2004. The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. PNAS 101:10596–601 [Google Scholar]
  127. Li W, Yang X, Lin Z, Timofejeva L, Xiao R. 127.  et al. 2005. The AtRAD51C gene is required for normal meiotic chromosome synapsis and double-stranded break repair in Arabidopsis. Plant Physiol 138:965–76 [Google Scholar]
  128. Li X, Chang Y, Xin X, Zhu C, Li X. 128.  et al. 2013. Replication protein A2c coupled with replication protein A1c regulates crossover formation during meiosis in rice. Plant Cell 25:3885–99 [Google Scholar]
  129. Lin YJ.129.  1982. Temperature and chiasma formation in Rhoeo spathacea var. variegata. Genetica 60:25–30 [Google Scholar]
  130. Lin Z, Kong H, Nei M, Ma H. 130.  2006. Origins and evolution of the recA/RAD51 gene family: evidence for ancient gene duplication and endosymbiotic gene transfer. PNAS 103:10328–33 [Google Scholar]
  131. Liu H, Nonomura KI. 131.  2016. A wide reprogramming of histone H3 modifications during male meiosis I in rice is dependent on the Argonaute protein MEL1. J. Cell Sci. 129:3553–61 [Google Scholar]
  132. Liu M, Shi S, Zhang S, Xu P, Lai J. 132.  et al. 2014. SUMO E3 ligase AtMMS21 is required for normal meiosis and gametophyte development in Arabidopsis. BMC Plant Biol 14:153 [Google Scholar]
  133. Liu S, Yeh CT, Ji T, Ying K, Wu H. 133.  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]
  134. Liu Y, Deng YT, Li G, Zhao J. 134.  2013. Replication factor C1 (RFC1) is required for double-strand break repair during meiotic homologous recombination in Arabidopsis. Plant J 73:154–65 [Google Scholar]
  135. Lloyd A, Bomblies K. 135.  2016. Meiosis in autopolyploid and allopolyploid Arabidopsis. Curr. Opin. Plant Biol 30:116–22 [Google Scholar]
  136. Lorenz A, Osman F, Sun W, Nandi S, Steinacher R, Whitby MC. 136.  2012. The fission yeast FANCM ortholog directs non-crossover recombination during meiosis. Science 336:1585–88 [Google Scholar]
  137. Lu P, Han X, Qi J, Yang J, Wijeratne AJ. 137.  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]
  138. Lucht JM, Mauch-Mani B, Steiner HY, Metraux JP, Ryals J, Hohn B. 138.  2002. Pathogen stress increases somatic recombination frequency in Arabidopsis. Nat. Genet 30:311–14 [Google Scholar]
  139. Lukaszewski AJ, Kopecky D. 139.  2010. The Ph1 locus from wheat controls meiotic chromosome pairing in autotetraploid rye (Secale cereale L.). Cytogenet. Genome Res. 129:117–23 [Google Scholar]
  140. Luo Q, Li Y, Shen Y, Cheng Z. 140.  2014. Ten years of gene discovery for meiotic event control in rice. J. Genet. Genom. 41:125–37 [Google Scholar]
  141. Maga G, Stucki M, Spadari S, Hubscher U. 141.  2000. DNA polymerase switching: I. Replication factor C displaces DNA polymerase α prior to PCNA loading. J. Mol. Biol. 295:791–801 [Google Scholar]
  142. Maloisel L, Bhargava J, Roeder GS. 142.  2004. A role for DNA polymerase δ in gene conversion and crossing over during meiosis in Saccharomyces cerevisiae. Genetics 167:1133–42 [Google Scholar]
  143. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM. 143.  2008. High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454:479–85 [Google Scholar]
  144. Martini E, Diaz RL, Hunter N, Keeney S. 144.  2006. Crossover homeostasis in yeast meiosis. Cell 126:285–95 [Google Scholar]
  145. Mason AS, Nelson MN, Castello M-C, Yan G, Cowling WA. 145.  2011. Genotypic effects on the frequency of homoeologous and homologous recombination in Brassica napus×B. carinata hybrids. Theor. Appl. Genet. 122:543–53 [Google Scholar]
  146. McVey M, Khodaverdian VY, Meyer D, Cerqueira PG, Heyer WD. 146.  2016. Eukaryotic DNA polymerases in homologous recombination. Annu. Rev. Genet. 50:393–421 [Google Scholar]
  147. Melamed-Bessudo C, Levy AA. 147.  2012. Deficiency in DNA methylation increases meiotic crossover rates in euchromatic but not in heterochromatic regions in Arabidopsis. PNAS 109:E981–88 [Google Scholar]
  148. Mercier R, Mezard C, Jenczewski E, Macaisne N, Grelon M. 148.  2015. The molecular biology of meiosis in plants. Annu. Rev. Plant Biol. 66:297–327 [Google Scholar]
  149. Meselson M, Stahl FW. 149.  1958. The replication of DNA in Escherichia coli. PNAS 44:671–82 [Google Scholar]
  150. Miao C, Tang D, Zhang H, Wang M, Li Y. 150.  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]
  151. Mickelbart MV, Hasegawa PM, Bailey-Serres J. 151.  2015. Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nat. Rev. Genet. 16:237–51 [Google Scholar]
  152. Mirouze M, Lieberman-Lazarovich M, Aversano R, Bucher E, Nicolet J. 152.  et al. 2012. Loss of DNA methylation affects the recombination landscape in Arabidopsis. PNAS 109:5880–85 [Google Scholar]
  153. Modliszewski JL, Copenhaver GP. 153.  2017. Meiotic recombination gets stressed out: CO frequency is plastic under pressure. Curr. Opin. Plant Biol. 36:95–102 [Google Scholar]
  154. Mohrmann L, Verrijzer CP. 154.  2005. Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes. Biochim. Biophys. Acta 1681:59–73 [Google Scholar]
  155. Molinier J, Ries G, Zipfel C, Hohn B. 155.  2006. Transgeneration memory of stress in plants. Nature 442:1046–49 [Google Scholar]
  156. Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C. 156.  et al. 2010. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327:876–79 [Google Scholar]
  157. Neale MJ, Pan J, Keeney S. 157.  2005. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436:1053–57 [Google Scholar]
  158. Ngo GH, Lydall D. 158.  2015. The 9-1-1 checkpoint clamp coordinates resection at DNA double strand breaks. Nucleic Acids Res 43:5017–32 [Google Scholar]
  159. Nicolas SD, Leflon M, Monod H, Eber F, Coriton O. 159.  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]
  160. Nimmo ER, Pidoux AL, Perry PE, Allshire RC. 160.  1998. Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe. Nature 392:825–28 [Google Scholar]
  161. Nimonkar AV, Sica RA, Kowalczykowski SC. 161.  2009. Rad52 promotes second-end DNA capture in double-stranded break repair to form complement-stabilized joint molecules. PNAS 106:3077–82 [Google Scholar]
  162. Nonomura K, Morohoshi A, Nakano M, Eiguchi M, Miyao A. 162.  et al. 2007. A germ cell–specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell 19:2583–94 [Google Scholar]
  163. Nonomura K, Nakano M, Fukuda T, Eiguchi M, Miyao A. 163.  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]
  164. Nottke AC, Kim HM, Colaiacovo MP. 164.  2017. Wrestling with chromosomes: the roles of SUMO during meiosis. Adv. Exp. Med. Biol. 963:185–96 [Google Scholar]
  165. Oakley HA.165.  1985. Meiosis in Mesostoma ehrenbergii ehrenbergii (Turbellaria, Rhabdocoela). III. Univalent chromosome segregation during the first meiotic division in spermatocytes. Chromosoma 91:95–100 [Google Scholar]
  166. Olivier M, Da Ines O, Amiard S, Serra H, Goubely C. 166.  et al. 2016. The structure-specific endonucleases MUS81 and SEND1 are essential for telomere stability in Arabidopsis. Plant Cell 28:74–86 [Google Scholar]
  167. Oshino T, Abiko M, Saito R, Ichiishi E, Endo M. 167.  et al. 2007. Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants. Mol. Genet. Genom. 278:31–42 [Google Scholar]
  168. Osman K, Higgins JD, Sanchez-Moran E, Armstrong SJ, Franklin FC. 168.  2011. Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 190:523–44 [Google Scholar]
  169. Osman K, Sanchez-Moran E, Mann SC, Jones GH, Franklin FC. 169.  2009. Replication protein A (AtRPA1a) is required for class I crossover formation but is dispensable for meiotic DNA break repair. EMBO J 28:394–404 [Google Scholar]
  170. Parvanov ED, Petkov PM, Paigen K. 170.  2010. Prdm9 controls activation of mammalian recombination hotspots. Science 327:835 [Google Scholar]
  171. Pecinka A, Fang W, Rehmsmeier M, Levy AA, Mittelsten Scheid O. 171.  2011. Polyploidization increases meiotic recombination frequency in Arabidopsis. BMC Biol 9:24 [Google Scholar]
  172. Pelé A, Falque M, Trotoux G, Eber F, Nègre S. 172.  et al. 2017. Amplifying recombination genome-wide and reshaping crossover landscapes in Brassicas. PLOS Genet 13:e1006794 [Google Scholar]
  173. Perrella G, Consiglio MF, Aiese-Cigliano R, Cremona G, Sanchez-Moran E. 173.  et al. 2010. Histone hyperacetylation affects meiotic recombination and chromosome segregation in Arabidopsis. Plant J 62:796–806 [Google Scholar]
  174. Phillips D, Jenkins G, Macaulay M, Nibau C, Wnetrzak J. 174.  et al. 2015. The effect of temperature on the male and female recombination landscape of barley. New Phytol 208:421–29 [Google Scholar]
  175. Pinon V, Yao X, Dong A, Shen WH. 175.  2017. SDG2-mediated H3K4me3 is crucial for chromatin condensation and mitotic division during male gametogenesis in Arabidopsis. Plant Physiol 174:1205–15 [Google Scholar]
  176. Pintard L, Kurz T, Glaser S, Willis JH, Peter M, Bowerman B. 176.  2003. Neddylation and deneddylation of CUL-3 is required to target MEI-1/Katanin for degradation at the meiosis-to-mitosis transition in C. elegans. Curr. Biol 13:911–21 [Google Scholar]
  177. Pradillo M, Varas J, Oliver C, Santos JL. 177.  2014. On the role of AtDMC1, AtRAD51 and its paralogs during Arabidopsis meiosis. Front. Plant Sci. 5:23 [Google Scholar]
  178. Qi J, Chen Y, Copenhaver GP, Ma H. 178.  2014. Detection of genomic variations and DNA polymorphisms and impact on analysis of meiotic recombination and genetic mapping. PNAS 111:10007–12 [Google Scholar]
  179. Qiao H, Offenberg HH, Anderson LK. 179.  2012. Altered distribution of MLH1 foci is associated with changes in cohesins and chromosome axis compaction in an asynaptic mutant of tomato. Chromosoma 121:291–305 [Google Scholar]
  180. Qiao H, Prasada Rao HB, Yang Y, Fong JH, Cloutier JM. 180.  et al. 2014. Antagonistic roles of ubiquitin ligase HEI10 and SUMO ligase RNF212 regulate meiotic recombination. Nat. Genet. 46:194–99 [Google Scholar]
  181. Qin Y, Zhao L, Skaggs MI, Andreuzza S, Tsukamoto T. 181.  et al. 2014. ACTIN-RELATED PROTEIN6 regulates female meiosis by modulating meiotic gene expression in Arabidopsis. Plant Cell 26:1612–28 [Google Scholar]
  182. Rao HB, Qiao H, Bhatt SK, Bailey LR, Tran HD. 182.  et al. 2017. A SUMO–ubiquitin relay recruits proteasomes to chromosome axes to regulate meiotic recombination. Science 355:403–7 [Google Scholar]
  183. Ribeiro J, Abby E, Livera G, Martini E. 183.  2016. RPA homologs and ssDNA processing during meiotic recombination. Chromosoma 125:265–76 [Google Scholar]
  184. Robert T, Nore A, Brun C, Maffre C, Crimi B. 184.  et al. 2016. The TopoVIB-like protein family is required for meiotic DNA double-strand break formation. Science 351:943–49 [Google Scholar]
  185. Roberts NY, Osman K, Armstrong SJ. 185.  2009. Telomere distribution and dynamics in somatic and meiotic nuclei of Arabidopsis thaliana. Cytogenet. Genome Res 124:193–201 [Google Scholar]
  186. Rockmill B, Voelkel-Meiman K, Roeder GS. 186.  2006. Centromere-proximal crossovers are associated with precocious separation of sister chromatids during meiosis in Saccharomyces cerevisiae. Genetics 174:1745–54 [Google Scholar]
  187. Roitinger E, Hofer M, Kocher T, Pichler P, Novatchkova M. 187.  et al. 2015. Quantitative phosphoproteomics of the ataxia telangiectasia-mutated (ATM) and ataxia telangiectasia-mutated and Rad3-related (ATR) dependent DNA damage response in Arabidopsis thaliana. Mol. Cell. Proteom 14:556–71 [Google Scholar]
  188. Saini R, Singh AK, Dhanapal S, Saeed TH, Hyde GJ, Baskar R. 188.  2017. Brief temperature stress during reproductive stages alters meiotic recombination and somatic mutation rates in the progeny of Arabidopsis. BMC Plant Biol 17:103 [Google Scholar]
  189. Saintenac C, Falque M, Martin OC, Paux E, Feuillet C, Sourdille P. 189.  2008. Detailed recombination studies along chromosome 3B provide new insights on crossover distribution in wheat (Triticum aestivum L.). Genetics 181:393–403 [Google Scholar]
  190. Saintenac C, Faure S, Remay A, Choulet F, Ravel C. 190.  et al. 2011. Variation in crossover rates across a 3-Mb contig of bread wheat (Triticum aestivum) reveals the presence of a meiotic recombination hotspot. Chromosoma 120:185–98 [Google Scholar]
  191. Salome PA, Bomblies K, Fitz J, Laitinen RA, Warthmann N. 191.  et al. 2012. The recombination landscape in Arabidopsis thaliana F2 populations. Heredity 108:447–55 [Google Scholar]
  192. Schwartz EK, Heyer WD. 192.  2011. Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma 120:109–27 [Google Scholar]
  193. Seeliger K, Dukowic-Schulze S, Wurz-Wildersinn R, Pacher M, Puchta H. 193.  2012. BRCA2 is a mediator of RAD51- and DMC1-facilitated homologous recombination in Arabidopsis thaliana. New Phytol 193:364–75 [Google Scholar]
  194. Seguela-Arnaud M, Choinard S, Larcheveque C, Girard C, Froger N. 194.  et al. 2017. RMI1 and TOP3α limit meiotic CO formation through their C-terminal domains. Nucleic Acids Res 45:1860–71 [Google Scholar]
  195. Seguela-Arnaud M, Crismani W, Larcheveque C, Mazel J, Froger N. 195.  et al. 2015. Multiple mechanisms limit meiotic crossovers: TOP3α and two BLM homologs antagonize crossovers in parallel to FANCM. PNAS 112:4713–18 [Google Scholar]
  196. Serra H, Da Ines O, Degroote F, Gallego ME, White CI. 196.  2013. Roles of XRCC2, RAD51B and RAD51D in RAD51-independent SSA recombination. PLOS Genet 9:e1003971 [Google Scholar]
  197. Shen X, De Jonge J, Forsberg SK, Pettersson ME, Sheng Z. 197.  et al. 2014. Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality. PLOS Genet 10:e1004842 [Google Scholar]
  198. Shilatifard A.198.  2012. The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu. Rev. Biochem. 81:65–95 [Google Scholar]
  199. Shilo S, Melamed-Bessudo C, Dorone Y, Barkai N, Levy AA. 199.  2015. DNA crossover motifs associated with epigenetic modifications delineate open chromatin regions in Arabidopsis. Plant Cell 27:2427–36 [Google Scholar]
  200. Shodhan A, Kataoka K, Mochizuki K, Novatchkova M, Loidl J. 200.  2017. A Zip3-like protein plays a role in crossover formation in the SC-less meiosis of the protist Tetrahymena. Mol. Biol. Cell 28:825–33 [Google Scholar]
  201. Shultz RW, Tatineni VM, Hanley-Bowdoin L, Thompson WF. 201.  2007. Genome-wide analysis of the core DNA replication machinery in the higher plants Arabidopsis and rice. Plant Physiol 144:1697–714 [Google Scholar]
  202. Si W, Yuan Y, Huang J, Zhang X, Zhang Y. 202.  et al. 2015. Widely distributed hot and cold spots in meiotic recombination as shown by the sequencing of rice F2 plants. New Phytol 206:1491–502 [Google Scholar]
  203. Sidhu GK, Fang C, Olson MA, Falque M, Martin OC, Pawlowski WP. 203.  2015. Recombination patterns in maize reveal limits to crossover homeostasis. PNAS 112:15982–87 [Google Scholar]
  204. Singh TR, Saro D, Ali AM, Zheng XF, Du CH. 204.  et al. 2010. MHF1–MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. Mol. Cell 37:879–86 [Google Scholar]
  205. Smagulova F, Gregoretti IV, Brick K, Khil P, Camerini-Otero RD, Petukhova GV. 205.  2011. Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472:375–78 [Google Scholar]
  206. Sommermeyer V, Beneut C, Chaplais E, Serrentino ME, Borde V. 206.  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]
  207. Song J, Bent AF. 207.  2014. Microbial pathogens trigger host DNA double-strand breaks whose abundance is reduced by plant defense responses. PLOS Pathog 10:e1004030 [Google Scholar]
  208. Stacey NJ, Kuromori T, Azumi Y, Roberts G, Breuer C. 208.  et al. 2006. Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J 48:206–16 [Google Scholar]
  209. Stewart MN, Dawson DS. 209.  2008. Changing partners: moving from non-homologous to homologous centromere pairing in meiosis. Trends Genet 24:564–73 [Google Scholar]
  210. Su H, Cheng Z, Huang J, Lin J, Copenhaver GP. 210.  et al. 2017. Arabidopsis RAD51, RAD51C and XRCC3 proteins form a complex and facilitate RAD51 localization on chromosomes for meiotic recombination. PLOS Genet 13:e1006827 [Google Scholar]
  211. Su Y, Barton AB, Kaback DB. 211.  2000. Decreased meiotic reciprocal recombination in subtelomeric regions in Saccharomyces cerevisiae. Chromosoma 109:467–75 [Google Scholar]
  212. Suay L, Zhang DS, Eber F, Jouy H, Lode M. 212.  et al. 2014. 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]
  213. Sun Y, Ambrose JH, Haughey BS, Webster TD, Pierrie SN. 213.  et al. 2012. Deep genome-wide measurement of meiotic gene conversion using tetrad analysis in Arabidopsis thaliana. PLOS Genet 8:e1002968 [Google Scholar]
  214. Sym M, Roeder GS. 214.  1994. Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79:283–92 [Google Scholar]
  215. Symington LS.215.  2014. End resection at double-strand breaks: mechanism and regulation. Cold Spring Harb. Perspect. Biol. 6:a016436 [Google Scholar]
  216. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW. 216.  1983. The double-strand-break repair model for recombination. Cell 33:25–35 [Google Scholar]
  217. Terasawa M, Ogawa H, Tsukamoto Y, Shinohara M, Shirahige K. 217.  et al. 2007. Meiotic recombination–related DNA synthesis and its implications for cross-over and non-cross-over recombinant formation. PNAS 104:5965–70 [Google Scholar]
  218. Uanschou C, Siwiec T, Pedrosa-Harand A, Kerzendorfer C, Sanchez-Moran E. 218.  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]
  219. Vrielynck N, Chambon A, Vezon D, Pereira L, Chelysheva L. 219.  et al. 2016. A DNA topoisomerase VI–like complex initiates meiotic recombination. Science 351:939–43 [Google Scholar]
  220. Wang C, Higgins JD, He Y, Lu P, Zhang D, Liang W. 220.  2017. Resolvase OsGEN1 mediates DNA repair by homologous recombination. Plant Physiol 173:1316–29 [Google Scholar]
  221. Wang H, Hu Q, Tang D, Liu X, Du G. 221.  et al. 2016. OsDMC1 is not required for homologous pairing in rice meiosis. Plant Physiol 171:230–41 [Google Scholar]
  222. Wang J, Niu B, Huang J, Wang H, Yang X. 222.  et al. 2016. The PHD finger protein MMD1/DUET ensures the progression of male meiotic chromosome condensation and directly regulates the expression of the condensin gene CAP-D3. Plant Cell 28:1894–909 [Google Scholar]
  223. Wang K, Wang M, Tang D, Shen Y, Miao C. 223.  et al. 2012. The role of rice HEI10 in the formation of meiotic crossovers. PLOS Genet 8:e1002809 [Google Scholar]
  224. Wang M, Wang K, Tang D, Wei C, Li M. 224.  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]
  225. Wang S, Zickler D, Kleckner N, Zhang L. 225.  2015. Meiotic crossover patterns: obligatory crossover, interference and homeostasis in a single process. Cell Cycle 14:305–14 [Google Scholar]
  226. Wang Y, Cheng Z, Huang J, Shi Q, Hong Y. 226.  et al. 2012. The DNA REPLICATION FACTOR RFC1 is required for interference-sensitive meiotic crossovers in Arabidopsis thaliana. PLOS Genet 8:e1003039 [Google Scholar]
  227. Wang Y, Xiao R, Wang H, Cheng Z, Li W. 227.  et al. 2014. The Arabidopsis RAD51 paralogs RAD51B, RAD51D and XRCC2 play partially redundant roles in somatic DNA repair and gene regulation. New Phytol 201:292–304 [Google Scholar]
  228. Ward JO, Reinholdt LG, Motley WW, Niswander LM, Deacon DC. 228.  et al. 2007. Mutation in mouse Hei10, an E3 ubiquitin ligase, disrupts meiotic crossing over. PLOS Genet 3:e139 [Google Scholar]
  229. Waterworth WM, Altun C, Armstrong SJ, Roberts N, Dean PJ. 229.  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]
  230. Wijnker E, van Dun K, de Snoo CB, Lelivelt CL, Keurentjes JJ. 230.  et al. 2012. Reverse breeding in Arabidopsis thaliana generates homozygous parental lines from a heterozygous plant. Nat. Genet. 44:467–70 [Google Scholar]
  231. Wijnker E, Velikkakam James G, Ding J, Becker F, Klasen JR. 231.  et al. 2013. The genomic landscape of meiotic crossovers and gene conversions in Arabidopsis thaliana. eLife 2:e01426 [Google Scholar]
  232. Wilson JY.232.  1959. Temperature effect on chiasma frequency in the bluebell Endymion nonscriptus. Chromosoma 10:337–54 [Google Scholar]
  233. Wold MS.233.  1997. Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 66:61–92 [Google Scholar]
  234. Wu S, Shi Y, Mulligan P, Gay F, Landry J. 234.  et al. 2007. A YY1–INO80 complex regulates genomic stability through homologous recombination–based repair. Nat. Struct. Mol. Biol. 14:1165–72 [Google Scholar]
  235. Wu Z, Ji JH, Tang D, Wang HJ, Shen Y. 235.  et al. 2015. OsSDS is essential for DSB formation in rice meiosis. Front. Plant Sci. 6:21 [Google Scholar]
  236. Wyatt HD, West SC. 236.  2014. Holliday junction resolvases. Cold Spring Harb. Perspect. Biol. 6:a023192 [Google Scholar]
  237. Xin Q, Shen Y, Li X, Lu W, Wang X. 237.  et al. 2016. MS5 mediates early meiotic progression and its natural variants may have applications for hybrid production in Brassica napus. Plant Cell 28:1263–78 [Google Scholar]
  238. Xu J, Zhao L, Xu Y, Zhao W, Sung P, Wang HW. 238.  2017. Cryo-EM structures of human RAD51 recombinase filaments during catalysis of DNA-strand exchange. Nat. Struct. Mol. Biol. 24:40–46 [Google Scholar]
  239. Xue Z, Li Y, Zhang L, Shi W, Zhang C. 239.  et al. 2016. OsMTOPVIB promotes meiotic DNA double-strand break formation in rice. Mol. Plant 9:1535–38 [Google Scholar]
  240. Yamada S, Ohta K, Yamada T. 240.  2013. Acetylated histone H3K9 is associated with meiotic recombination hotspots, and plays a role in recombination redundantly with other factors including the H3K4 methylase Set1 in fission yeast. Nucleic Acids Res 41:3504–17 [Google Scholar]
  241. Yang H, Lu P, Wang Y, Ma H. 241.  2011. The transcriptome landscape of Arabidopsis male meiocytes from high-throughput sequencing: the complexity and evolution of the meiotic process. Plant J 65:503–16 [Google Scholar]
  242. Yang X, Makaroff CA, Ma H. 242.  2003. The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis. Plant Cell 15:1281–95 [Google Scholar]
  243. Yang Y, Ishino S, Yamagami T, Kumamaru T, Satoh H, Ishino Y. 243.  2012. The OsGEN-L protein from Oryza sativa possesses Holliday junction resolvase activity as well as 5′-flap endonuclease activity. J. Biochem. 151:317–27 [Google Scholar]
  244. Yelina NE, Choi K, Chelysheva L, Macaulay M, de Snoo B. 244.  et al. 2012. Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLOS Genet 8:e1002844 [Google Scholar]
  245. Yelina NE, Lambing C, Hardcastle TJ, Zhao X, Santos B, Henderson IR. 245.  2015. DNA methylation epigenetically silences crossover hot spots and controls chromosomal domains of meiotic recombination in Arabidopsis. Genes Dev 29:2183–202 [Google Scholar]
  246. Yu Z, Kim Y, Dernburg AF. 246.  2016. Meiotic recombination and the crossover assurance checkpoint in Caenorhabditis elegans. Semin. Cell Dev. Biol 54:106–16 [Google Scholar]
  247. Yuan J, Chen J. 247.  2013. FIGNL1-containing protein complex is required for efficient homologous recombination repair. PNAS 110:10640–45 [Google Scholar]
  248. Zhang C, Song Y, Cheng ZH, Wang YX, Zhu J. 248.  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]
  249. Zhang L, Liang Z, Hutchinson J, Kleckner N. 249.  2014. Crossover patterning by the beam-film model: analysis and implications. PLOS Genet 10:e1004042 [Google Scholar]
  250. Zhang L, Wang S, Yin S, Hong S, Kim KP, Kleckner N. 250.  2014. Topoisomerase II mediates meiotic crossover interference. Nature 511:551–56 [Google Scholar]
  251. Zheng T, Nibau C, Phillips DW, Jenkins G, Armstrong SJ, Doonan JH. 251.  2014. CDKG1 protein kinase is essential for synapsis and male meiosis at high ambient temperature in Arabidopsis thaliana. PNAS 111:2182–87 [Google Scholar]
  252. Zhou L, Han J, Chen Y, Wang Y, Liu YG. 252.  2017. Bivalent Formation 1, a plant-conserved gene, encodes an OmpH/coiled-coil motif-containing protein required for meiotic recombination in rice. J. Exp. Bot. 68:2163–74 [Google Scholar]
  253. Zickler D, Kleckner N. 253.  2015. Recombination, pairing, and synapsis of homologs during meiosis. Cold Spring Harb. Perspect. Biol. 7:a016626 [Google Scholar]
  254. Zickler D, Kleckner N. 254.  2016. A few of our favorite things: pairing, the bouquet, crossover interference and evolution of meiosis. Semin. Cell Dev. Biol. 54:135–48 [Google Scholar]
  255. Ziolkowski PA, Berchowitz LE, Lambing C, Yelina NE, Zhao X. 255.  et al. 2015. Juxtaposition of heterozygous and homozygous regions causes reciprocal crossover remodelling via interference during Arabidopsis meiosis. eLife 4:e03708 [Google Scholar]
  256. Ziolkowski PA, Henderson IR. 256.  2017. Interconnections between meiotic recombination and sequence polymorphism in plant genomes. New Phytol 213:1022–29 [Google Scholar]
  257. Ziolkowski PA, Underwood CJ, Lambing C, Martinez-Garcia M, Lawrence EJ. 257.  et al. 2017. Natural variation and dosage of the HEI10 meiotic E3 ligase control Arabidopsis crossover recombination. Genes Dev 31:306–17 [Google Scholar]
/content/journals/10.1146/annurev-arplant-042817-040431
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Meiotic Recombination: Mixing It Up in Plants
Annual Review of Plant Biology 69, 577 (2018); https://doi.org/10.1146/annurev-arplant-042817-040431
/content/journals/10.1146/annurev-arplant-042817-040431
/content/journals/10.1146/annurev-arplant-042817-040431
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