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Annual Review of Genetics

Volume 48, 2014

Factors Underlying Restricted Crossover Localization in Barley Meiosis

Abstract

Meiotic recombination results in the formation of cytological structures known as chiasmata at the sites of genetic crossovers (COs). The formation of at least one chiasma/CO between homologous chromosome pairs is essential for accurate chromosome segregation at the first meiotic division as well as for generating genetic variation. Although DNA double-strand breaks, which initiate recombination, are widely distributed along the chromosomes, this is not necessarily reflected in the chiasma distribution. In many species there is a tendency for chiasmata to be distributed in favored regions along the chromosomes, whereas in others, such as barley and some other grasses, chiasma localization is extremely pronounced. Localization of chiasma to the distal regions of barley chromosomes restricts the genetic variation available to breeders. Studies reviewed herein are beginning to provide an explanation for chiasma localization in barley. Moreover, they suggest a potential route to manipulating chiasma distribution that could be of value to plant breeders.

Keyword(s): cereals, chiasma, chromosome synapsis, poaceae, recombination
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2014-11-23
2024-04-24
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Literature Cited

  1. Akhunov ED, Akhunova AR, Linkiewicz AM, Dubcovsky J, Hummel D. 1.  et al. 2003. Synteny perturbations between wheat homoeologous chromosomes caused by locus duplications and deletions correlate with recombination rates. Proc. Natl. Acad. Sci. USA 100:10836–41 [Google Scholar]
  2. Albini SM, Jones GH. 2.  1988. Synaptonemal complex spreading in Allium cepa and Allium fistulosum. II. Pachytene observations: the SC karyotype and the correspondence of late recombination nodules and chiasmata. Genome 30:399–410 [Google Scholar]
  3. Anderson LK, Doyle GG, Brigham B, Carter J, Hooker KD. 3.  et al. 2003. High-resolution crossover maps for each bivalent of Zea mays using recombination nodules. Genetics 165:849–65 [Google Scholar]
  4. Armstrong SJ, Franklin FCH, Jones GH. 4.  2003. A meiotic time-course for Arabidopsis thaliana. Sex. Plant Reprod. 16:141–49 [Google Scholar]
  5. Armstrong SJ, Jones GH. 5.  2003. Meiotic cytology and chromosome behaviour in wild-type Arabidopsis thaliana. J. Exp. Bot. 54:1–10 [Google Scholar]
  6. Baptista-Giacomelli FR, Pagliarini MS, de Almeida JL. 6.  2000. Meiotic behavior in several Brazilian oat cultivars (Avena sativa L.). Cytologia (Tokyo) 65:371–78 [Google Scholar]
  7. Barakate A, Higgins JD, Vivera S, Stephens J, Perry RM. 7.  et al. 2014. The synaptonemal complex protein ZYP1 is required for imposition of meiotic crossovers in barley. Plant Cell 26:729–40 [Google Scholar]
  8. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C. 8.  et al. 2010. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327:836–40 [Google Scholar]
  9. Bennett MD, Finch RA. 9.  1971. Duration of meiosis in barley. Genet. Res. 17:209–14 [Google Scholar]
  10. Bennett MD, Leitch IJ. 10.  2005. Nuclear DNA amounts in angiosperms: progress, problems and prospects. Ann. Bot. 95:45–90 [Google Scholar]
  11. Berchowitz LE, Copenhaver GP. 11.  2010. Genetic interference: Don't stand so close to me. Curr. Genomics 11:91–102 [Google Scholar]
  12. Bishop DK, Zickler D. 12.  2004. Early decision: meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117:9–15 [Google Scholar]
  13. Borde V, Robine N, Lin W, Bonfils S, Geli V, Nicolas A. 13.  2009. Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J. 28:99–111 [Google Scholar]
  14. Bowers JE, Arias MA, Asher R, Avise JA, Ball RT. 14.  et al. 2005. Comparative physical mapping links conservation of microsynteny to chromosome structure and recombination in grasses. Proc. Natl. Acad. Sci. USA 102:13206–11 [Google Scholar]
  15. Buckler ES, Phelps-Durr TL, Buckler CSK, Dawe RK, Doebley JF, Holtsford TP. 15.  1999. Meiotic drive of chromosomal knobs reshaped the maize genome. Genetics 153:415–26 [Google Scholar]
  16. Calvente A, Viera A, Page J, Parra MT, Gomez R. 16.  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]
  17. Carpenter ATC. 17.  1975. Electron microscopy of meiosis in Drosophila melanogaster females. II. The recombination nodule: a recombination-associated structure at pachytene?. Proc. Natl. Acad. Sci. USA 72:3186–89 [Google Scholar]
  18. Caryl AP, Armstrong SJ, Jones GH, Franklin FCH. 18.  2000. A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma 109:62–71 [Google Scholar]
  19. Chelysheva L, Grandont L, Vrielynck N, le Guin S, Mercier R, Grelon M. 19.  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]
  20. Chen Z, Higgins JD, Hui JTL, Li J, Franklin FCH, Berger F. 20.  2011. Retinoblastoma protein is essential for early meiotic events in Arabidopsis. EMBO J. 30:744–55 [Google Scholar]
  21. Choi K, Zhao X, Kelly KA, Venn O, Higgins JD. 21.  et al. 2013. Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters. Nat. Genet. 45:1327–36 [Google Scholar]
  22. Colombo PC, Jones GH. 22.  1997. Chiasma interference is blind to centromeres. Heredity 79:214–27 [Google Scholar]
  23. Crismani W, Girard C, Froger N, Pradillo M, Santos JL. 23.  et al. 2012. FANCM limits meiotic crossovers. Science 336:1588–90 [Google Scholar]
  24. Darlington CD. 24.  1931. Meiosis. Biol. Rev. Biol. Proc. Camb. Philos. Soc. 6:221–64 [Google Scholar]
  25. de Boer E, Dietrich AJ, Hoog C, Stam P, Heyting C. 25.  2007. Meiotic interference among MLH1 foci requires neither an intact axial element structure nor full synapsis. J. Cell Sci. 120:731–36 [Google Scholar]
  26. Dowrick G. 26.  1957. The influence of temperature on meiosis. Heredity 11:37–49 [Google Scholar]
  27. Draper J, Mur LAJ, Jenkins G, Ghosh-Biswas GC, Bablak P. 27.  et al. 2001. Brachypodium distachyon. A new model system for functional genomics in grasses. Plant Physiol. 127:1539–55 [Google Scholar]
  28. Emerson RA, Beadle GW, Fraser AC. 28.  1935. A summary of linkage studies in maize. Cornell Univ. Agric. Stn. Mem. 180:1–83 [Google Scholar]
  29. Erayman M, Sandhu D, Sidhu D, Dilbirligi M, Baenziger PS, Gill KS. 29.  2004. Demarcating the gene-rich regions of the wheat genome. Nucleic Acids Res. 32:3546–65 [Google Scholar]
  30. Falque M, Anderson LK, Stack SM, Gauthier F, Martin OC. 30.  2009. Two types of meiotic crossovers coexist in maize. Plant Cell 21:3915–25 [Google Scholar]
  31. Ferdous M, Higgins JD, Osman K, Lambing C, Roitinger E. 31.  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]
  32. Fletcher HL. 32.  1978. Localized chiasmata due to partial pairing: 3D reconstruction of synaptonemal complexes in male Stethophyma grossum. Chromosoma 65:247–69 [Google Scholar]
  33. Fogwill M. 33.  1958. Differences in crossing-over and chromosome size in the sex cells of Lilium and Fritillaria. Chromosoma 9:493–504 [Google Scholar]
  34. Fox DP. 34.  1973. Control of chiasma distribution in locust, Schistocerca gregaria (Forskal). Chromosoma 43:289–328 [Google Scholar]
  35. Fuchs J, Demidov D, Houben A, Schubert I. 35.  2006. Chromosomal histone modification patterns: from conservation to diversity. Trends Plant Sci. 11:199–208 [Google Scholar]
  36. Fung JC, Rockmill B, Odell M, Roeder GS. 36.  2004. Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116:795–802 [Google Scholar]
  37. Gauthier F, Martin OC, Falque M. 37.  CODA (crossover distribution analyzer): quantitative characterization of crossover position patterns along chromosomes. BMC Bioinform. 12:27 [Google Scholar]
  38. Harper L, Golubovskaya I, Cande WZ. 38.  2004. A bouquet of chromosomes. J. Cell Sci. 117:4025–32 [Google Scholar]
  39. Higgins JD, Armstrong SJ, Franklin FCH, Jones GH. 39.  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]
  40. Higgins JD, Perry RM, Barakat A, Ramsay L, Waugh R. 40.  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]
  41. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH. 41.  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]
  42. Higgins JD, Vignard J, Mercier R, Pugh AG, Franklin FCH, Jones GH. 42.  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]
  43. Hollingsworth NM, Byers B. 43.  1989. Hop1: a yeast meiotic pairing gene. Genetics 121:445–62 [Google Scholar]
  44. Hultén M. 44.  1974. Chiasma distribution at diakinesis in the normal human male. Hereditas 76:55–78 [Google Scholar]
  45. Jackson N, Sanchez-Moran E, Buckling E, Armstrong SJ, Jones GH, Franklin FCH. 45.  2006. Reduced meiotic crossovers and delayed prophase I progression in AtMLH3-deficient Arabidopsis. EMBO J. 25:1315–23 [Google Scholar]
  46. Jones GH. 46.  1987. Chiasmata. Meiosis PB Moens 213–44 Waltham, MA: Acad. Press [Google Scholar]
  47. Jones GH. 47.  1978. Giemsa C-banding of rye meiotic chromosomes and nature of terminal chiasmata. Chromosoma 66:45–57 [Google Scholar]
  48. Jones GH. 48.  1984. The control of chiasma distribution. SEB Symp. 38:293–320 [Google Scholar]
  49. Jones GH, Franklin FC. 49.  2006. Meiotic crossing-over: obligation and interference. Cell 126:246–48 [Google Scholar]
  50. Keeney S, Giroux CN, Kleckner N. 50.  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]
  51. Kellogg EA. 51.  1998. Relationships of cereal crops and other grasses. Proc. Natl. Acad. Sci. USA 95:2005–10 [Google Scholar]
  52. Kleckner N. 52.  2006. Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex. Chromosoma 115:175–94 [Google Scholar]
  53. Kleckner N, Zickler D, Jones GH, Dekker J, Padmore R. 53.  et al. 2004. A mechanical basis for chromosome function. Proc. Natl. Acad. Sci. USA 101:12592–97 [Google Scholar]
  54. Knoll A, Higgins JD, Seeliger K, Reha SJ, Dangel NJ. 54.  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]
  55. Kunzel G, Korzun L, Meister A. 55.  2000. Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics 154:397–412 [Google Scholar]
  56. Kunzel G, Waugh R. 56.  2002. Integration of microsatellite markers into the translocation-based physical RFLP map of barley chromosome 3H. Theor. Appl. Genet. 105:660–65 [Google Scholar]
  57. Ladizinsky G. 57.  2012. Studies in Oat Evolution: A Man's Life with Avena (Springer Briefs in Agriculture) New York: Springer [Google Scholar]
  58. Laurie DA, Jones GH. 58.  1981. Interindividual variation in chiasma distribution in Chorthippus brunneus (Orthoptera, Acrididae). Heredity 47:409–16 [Google Scholar]
  59. Lhuissier FGP, Offenberg HH, Wittich PE, Vischer NOE, Heyting C. 59.  2007. The mismatch repair protein MLH1 marks a subset of strongly interfering crossovers in tomato. Plant Cell 19:862–76 [Google Scholar]
  60. Li X, Chang Y, Xin X, Zhu C, Li X. 60.  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]
  61. Lima de Faria A, Jaworska H. 61.  1972. Relation between chromosome size gradient and sequence of DNA replication in rye. Hereditas 70:39–57 [Google Scholar]
  62. Loidl J. 62.  1989. Effects of elevated temperature on meiotic chromosome synapsis in Allium ursinum. Chromosoma 97:449–58 [Google Scholar]
  63. Lukaszewski AJ. 63.  1992. A comparison of physical distribution of recombination in chromosome 1R in diploid rye and in hexaploid triticale. Theor. Appl. Genet. 83:1048–53 [Google Scholar]
  64. Lukaszewski AJ. 64.  2008. Unexpected behavior of an inverted rye chromosome arm in wheat. Chromosoma 117:569–78 [Google Scholar]
  65. Lukaszewski AJ, Curtis CA. 65.  1993. Physical distribution of recombination in B-genome chromosomes of tetraploid wheat. Theor. Appl. Genet. 86:121–27 [Google Scholar]
  66. Lukaszewski AJ, Kopecky D, Linc G. 66.  2012. Inversions of chromosome arms 4AL and 2BS in wheat invert the patterns of chiasma distribution. Chromosoma 121:201–8 [Google Scholar]
  67. Marcon E, Moens P. 67.  2003. MLH1p and MLH3p localize to precociously induced chiasmata of okadaic-acid-treated mouse spermatocytes. Genetics 165:2283–87 [Google Scholar]
  68. Mayer KFX, Waugh R, Langridge P, Close TJ, Wise RP. 68.  et al. 2012. A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–16 [Google Scholar]
  69. McClintock B. 69.  1948. Mutable loci in maize. Carnegie Inst. Wash. Year Book 47:155–69 [Google Scholar]
  70. Mercier R, Grelon M. 70.  2008. Meiosis in plants: ten years of gene discovery. Cytogenet. Genome Res. 120:281–90 [Google Scholar]
  71. Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L. 71.  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]
  72. Mieczkowski PA, Dominska M, Buck MJ, Gerton JL, Lieb JD, Petes TD. 72.  2006. Global analysis of the relationship between the binding of the Bas1p transcription factor and meiosis-specific double-strand DNA breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 26:1014–27 [Google Scholar]
  73. Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C. 73.  et al. 2010. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327:876–79 [Google Scholar]
  74. Naranjo T, Valenzuela NT, Perera E. 74.  2010. Chiasma frequency is region specific and chromosome conformation dependent in a rye chromosome added to wheat. Cytogenet. Genome Res. 129:133–42 [Google Scholar]
  75. Newton WCF, Darlington CD. 75.  1930. Fritillaria meleagris chiasma formation and distribution. J. Genet. 22:1–14 [Google Scholar]
  76. Nonomura KI, Nakano M, Eiguchi M, Suzuki T, Kurata N. 76.  2006. PAIR2 is essential for homologous chromosome synapsis in rice meiosis I. J. Cell Sci. 119:217–25 [Google Scholar]
  77. Oakley HA, Jones GH. 77.  1982. Meiosis in Mesostoma ehrenbergii ehrenbergii (Turbellaria, Rhabdocoela). I. Chromosoma pairing, synaptonemal complexes and chiasma localization in spermatogenesis. Chromosoma 85:311–22 [Google Scholar]
  78. Osman K, Higgins JD, Sanchez-Moran E, Armstrong SJ, Franklin FCH. 78.  2011. Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol. 190:523–44 [Google Scholar]
  79. Page SL, Hawley RS. 79.  2004. The genetics and molecular biology of the synaptonemal complex. Annu. Rev. Cell Dev. Biol. 20:525–58 [Google Scholar]
  80. Paigen K, Petkov P. 80.  2010. Mammalian recombination hot spots: properties, control and evolution. Nat. Rev. Genet. 11:221–33 [Google Scholar]
  81. Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG. 81.  et al. 2011. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144:719–31 [Google Scholar]
  82. Parvanov ED, Petkov PM, Paigen K. 82.  2010. Prdm9 controls activation of mammalian recombination hotspots. Science 327:835 [Google Scholar]
  83. Perrella G, Consiglio MF, Aiese-Cigliano R, Cremona G, Sanchez-Moran E. 83.  et al. 2010. Histone hyperacetylation affects meiotic recombination and chromosome segregation in Arabidopsis. Plant J. 62:796–806 [Google Scholar]
  84. Phillips D, Nibau C, Wnetrzak J, Jenkins G. 84.  2012. High resolution analysis of meiotic chromosome structure and behaviour in barley (Hordeum vulgare L.). PLoS ONE 7:e39539 [Google Scholar]
  85. Phillips D, Wnetrzak J, Nibau C, Barakate A, Ramsay L. 85.  et al. 2013. Quantitative high resolution mapping of HvMLH3 foci in barley pachytene nuclei reveals a strong distal bias and weak interference. J. Exp. Bot. 64:2139–54 [Google Scholar]
  86. Pryor A, Faulkner K, Rhoades MM, Peacock WJ. 86.  1980. Asynchronous replication of heterochromatin in maize. Proc. Natl. Acad. Sci. USA 77:6705–9 [Google Scholar]
  87. Ronceret A, Pawlowski WP. 87.  2010. Chromosome dynamics in meiotic prophase I in plants. Cytogenet. Genome Res. 129:173–83 [Google Scholar]
  88. Scherthan H. 88.  2001. A bouquet makes ends meet. Nat. Rev. Mol. Cell Biol. 2:621–27 [Google Scholar]
  89. Smagulova F, Gregoretti IV, Brick K, Khil P, Camerini-Otero RD, Petukhova GV. 89.  2011. Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472:375–78 [Google Scholar]
  90. Sturtevant AH. 90.  1913. The linear arrangement of six sex-linked factors in Drosophila, as shown by their mode of association. J. Exp. Zool. 14:43–59 [Google Scholar]
  91. Tease C. 91.  1978. Cytological detection of crossing-over in BrdU substituted meiotic chromosomes using the fluorescent plus giemsa technique. Nature 272:823–24 [Google Scholar]
  92. Tease C, Jones GH. 92.  1978. Analysis of exchanges in differentially stained meiotic chromosomes of Locusta migrotoria after BrdU substitution and FPG staining. I. Crossover exchanges in monochiasmate bivalents. Chromosoma 69:163–78 [Google Scholar]
  93. Thompson EA, Roeder GS. 93.  1989. Expression and DNA sequence of RED1, a gene required for meiosis I chromosome segregation in yeast. Mol. Gen. Genet. 218:293–301 [Google Scholar]
  94. Wallace BMN, Jones GH. 94.  1978. Incomplete chromosome pairing and its relation to chiasma localization in Stethophyma grossum spermocytes. Heredity 40:385–96 [Google Scholar]
  95. Wang KJ, Wang M, Tang D, Shen Y, Qin BX. 95.  et al. 2011. PAIR3, an axis-associated protein, is essential for the recruitment of recombination elements onto meiotic chromosomes in rice. Mol. Biol. Cell 22:12–19 [Google Scholar]
  96. Wang M, Wang KJ, Tang D, Wei CX, Li M. 96.  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]
  97. Watson JD, Callan HG. 97.  1963. The form of bivalent chromosomes in newt oocytes at first metaphase of meiosis. Q. J. Microsc. Sci. 104:281–95 [Google Scholar]
  98. Yuan WY, Li XW, Chang YX, Wen RY, Chen GX. 98.  et al. 2009. Mutation of the rice gene PAIR3 results in lack of bivalent formation in meiosis. Plant J. 59:303–15 [Google Scholar]
  99. Zickler D, Kleckner N. 99.  1999. Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33:603–754 [Google Scholar]
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Factors Underlying Restricted Crossover Localization in Barley Meiosis
Annual Review of Genetics 48, 29 (2014); https://doi.org/10.1146/annurev-genet-120213-092509
/content/journals/10.1146/annurev-genet-120213-092509
/content/journals/10.1146/annurev-genet-120213-092509
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