Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes

PLoS Genetics

Volumn 7, Issue 11, 2011, Pages

  Giraut, Laurène ^a   Falque, Matthieu ^b   Drouaud, Jan ^a   Pereira, Lucie ^a   Martin, Olivier C ^b   Mézard, Christine ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b INRA Institut National de la Recherche Agronomique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; GUANINE;

ARABIDOPSIS; ARTICLE; BASE PAIRING; CHROMOSOME SIZE; CONTROLLED STUDY; CORRELATION ANALYSIS; CPG ISLAND; CROSSING OVER; FEMALE; GENE MAPPING; MALE; MEIOSIS; NONHUMAN; PLANT CHROMOSOME; SEX DIFFERENCE; SYNAPTONEMAL COMPLEX; TRANSPOSON; CHROMOSOME MAP; DNA BASE COMPOSITION; GENETIC RECOMBINATION; GENETICS; PLANT GENE; PLANT GENOME; SINGLE NUCLEOTIDE POLYMORPHISM;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS; BASE COMPOSITION; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; CPG ISLANDS; CROSSING OVER, GENETIC; DNA TRANSPOSABLE ELEMENTS; GENES, PLANT; GENOME, PLANT; MEIOSIS; POLYMORPHISM, SINGLE NUCLEOTIDE; RECOMBINATION, GENETIC;

EID: 81755183075     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002354     Document Type: Article

References (76)

1. Lynn A, Ashley T, Hassold T, (2004) Variation in human meiotic recombination. Annu Rev Genomics Hum Genet 5: 317-349.
2. Sturtevant AH, (1915) The behavior of the chromosomes as studied through linkage. Molecular and General Genetics 13: 234-287.
3. Copenhaver GP, Housworth EA, Stahl FW, (2002) Crossover interference in Arabidopsis. Genetics 160: 1631-1639.
4. Housworth EA, Stahl FW, (2003) Crossover interference in humans. Am J Hum Genet 73: 188-197.
5. Falque M, Mercier R, Mezard C, de Vienne D, Martin OC, (2007) Patterns of recombination and MLH1 foci density along mouse chromosomes: modeling effects of interference and obligate chiasma. Genetics 176: 1453-1467.
6. Falque M, Anderson LK, Stack SM, Gauthier F, Martin OC, (2009) Two types of meiotic crossovers coexist in maize. Plant Cell 21: 3915-3925.
7. Foss E, Lande R, Stahl FW, Steinberg CM, (1993) Chiasma interference as a function of genetic distance. Genetics 133: 681-691.
8. McPeek MS, Speed TP, (1995) Modeling interference in genetic recombination. Genetics 139: 1031-1044.
9. Talbert PB, Henikoff S, (2010) Centromeres convert but don't cross. PLoS Biol 8: e1000326 doi:1000310.1001371/journal.pbio.1000326.
10. Westphal T, Reuter G, (2002) Recombinogenic effects of suppressors of position-effect variegation in Drosophila. Genetics 160: 609-621.
11. Jensen-Seaman MI, Furey TS, Payseur BA, Lu Y, Roskin KM, et al. (2004) Comparative recombination rates in the rat, mouse, and human genomes. Genome Res 14: 528-538.
12. Backström N, Forstmeier W, Schielzeth H, Mellenius H, Nam K, et al. (2010) The recombination landscape of the zebra finch Taeniopygia guttata genome. Genome Res 20: 485-495.
13. Beye M, Gattermeier I, Hasselmann M, Gempe T, Schioett M, et al. (2006) Exceptionally high levels of recombination across the honey bee genome. Genome Res 16: 1339-1344.
14. Gore MA, Chia JM, Elshire RJ, Sun Q, Ersoz ES, et al. (2009) A first-generation haplotype map of maize. Science 20: 1115-1117.
15. Duret L, Arndt PF, (2008) The impact of recombination on nucleotide substitutions in the human genome. PLoS Genet 4: e1000071 doi:1000010.1001371/journal.pgen1000071.
16. Marsolier-Kergoat MC, Yeramian E, (2009) GC content and recombination: Reassessing the causal ffects for the Saccharomyces cerevisiae genome. Genetics 183: 31-38.
17. Drouaud J, Camilleri C, Bourguignon PY, Canaguier A, Berard A, et al. (2006) Variation in crossing-over rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination "hot spots". Genome Res 16: 106-114.
18. Marais G, Charlesworth B, Wright SI, (2004) Recombination and base composition: the case of the highly self-fertilizing plant Arabidopsis thaliana. Genome Biol 5: R45.
19. Myers S, Bottolo L, Freeman C, McVean G, Donnelly P, (2005) A fine-scale map of recombination rates and hotspots across the human genome. Science 310: 321-324.
20. Nachman MW, (2002) Variation in recombination rate across the genome: evidence and implications. Curr Opin Genet Dev 12: 657-663.
21. Petes TD, (2001) Meiotic recombination hot spots and cold spots. Nat Rev Genet 2: 360-369.
22. Lenormand T, (2003) The evolution of sex dimorphism in recombination. Genetics 163: 811-822.
23. Haldane JBS, (1922) Sex ratio and unisexual sterility in hybrid animals. J Genet 12: 101-109.
24. Ved Brat S, (1966) Genetic systems in Allium. Sex differences in meiosis. Chromosomes Today 1: 31-40.
25. Kearsey MJ, Ramsay LD, Jennings DE, Lydiate DJ, Bohuon EJR, et al. (1996) Higher recombination frequencies in female compared to male meioses in Brassica oleracea. Theor Appl Genet 92: 363-367.
26. Armstrong SJ, Jones GH, (2001) Female meiosis in wild-type Arabidopsis thaliana and in two meiotic mutants. Sex Plant Reprod 13: 177-183.
27. Drouaud J, Mercier R, Chelysheva L, Berard A, Falque M, et al. (2007) Sex-specific crossover distributions and variations in interference level along Arabidopsis thaliana chromosome 4. PLoS Genet 3: e106 doi:110.1371/journal.pgen.0030106.
28. Miles LG, Isberg SR, Glenn TC, Lance SL, Dalzell P, et al. (2009) A genetic linkage map for the saltwater crocodile (Crocodylus porosus). BMC Genomics 10: 339.
29. Hedrick PW, (2007) Sex: Differences in mutation, recombination, selection, gene flow and genetic drift. Evolution 61: 2750-2771.
30. Heyting C, Dietrich AJ, (1992) Synaptosomal complexes and the organization of chromatin during meiotic prophase. Cell Biol Int Rep 16: 749-760.
31. Kleckner N, Storlazzi A, Zickler D, (2003) Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length. Trends Genet 19: 623-628.
32. Wallace BM, Hulten MA, (1985) Meiotic chromosome pairing in the normal human female. Ann Hum Genet 49: 215-226.
33. Croft JA, Jones GH, (1989) Chromosome pairing and chiasma formation in spermatocytes and oocytes of Dendrocoelum lacteum (Turbellaria, Tricladida): A cytogenetical and ultrastructural study. Heredity 63: 97-106.
34. Wallace BM, Wallace H, (2003) Synaptonemal complex karyotype of zebrafish. Heredity 90: 136-140.
35. Fox DP, (1973) The control of chiasma distribution in the locust, Schistocerca gregaria (Forskål). Chromosoma 43: 289-328.
36. Quevedo C, Del Cerro AL, Santos JL, Jones GH, (1997) Correlated variation of chiasma frequency and synaptonemal complex length in Locusta migratoria. Heredity 78: 515-519.
37. Tease C, Hulten MA, (2004) Inter-sex variation in synaptonemal complex lengths largely determine the different recombination rates in male and female germ cells. Cytogenet Genome Res 107: 208-215.
38. AGI, (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
39. Bennett MD, Leitch IJ, Price HJ, Johnston JS, (2003) Comparison with Caenorhabditis (~100 Mb) and Drosophila (~175 Mb) using flow cytometry show genome size in Arabidopsis to be ~157 Mb and thus ~25% larger than the Arabidopsis genome initiative estimate of ~125 Mb. Annals of Botany 91: 547-557.
40. Toyota M, Matsuda K, Kakutani T, Terao Morita M, Tasaka M, (2010) Developmental changes in crossover frequency in Arabidopsis. Plant J 65: 589-599.
41. Lopez E, Pradillo M, Romero C, Santos JL, Cunado N, (2008) Pairing and synapsis in wild type Arabidopsis thaliana. Chromosome Res 16: 701-708.
42. Albini SM, (1994) A karyotype of the Arabidopsis thaliana genome derived from synaptonemal complex analysis at prophase I of meiosis. Plant Journal 5: 665-672.
43. Kong A, Gudbjartsson DF, Sainz J, Jonsdottir GM, Gudjonsson SA, et al. (2002) A high-resolution recombination map of the human genome. Nat Genet 31: 241-247.
44. Mets DG, Meyer BJ, (2009) Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139: 73-86.
45. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM, (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454: 479-485.
46. Basheva EA, Bidau CJ, Borodin PM, (2008) General pattern of meiotic recombination in male dogs estimated by MLH1 and RAD51 immunolocalization. Chromosome Res 16: 709-719.
47. Froenicke L, Anderson LK, Wienberg J, Ashley T, (2002) Male mouse recombination maps for each autosome identified by chromosome painting. Am J Hum Genet 71: 1353-1368.
48. Pigozzi MI, Solari AJ, (1999) Equal frequencies of recombination nodules in both sexes of the pigeon suggest a basic difference with eutherian mammals. Genome 42: 315-321.
49. Jones GH, (1984) The control of chiasma distribution. Symp Soc Exp Biol 38: 293-320.
50. Jones GH, Franklin FC, (2006) Meiotic crossing-over: Obligation and Interference. Cell 126: 246-248.
51. Pardo-Manuel de Villena F, Sapienza C, (2001) Recombination is proportional to the number of chromosome arms in mammalsMammalian Genome 12: 318-322.
52. Coop G, Przeworski M, (2007) An evolutionary view of human recombination. Nat Rev Genet 8: 23-34.
53. Fledel-Alon A, Wilson DJ, Broman K, Wen X, Ober C, et al. (2009) Broad-scale recombination patterns underlying proper disjunction in humans. PLoS Genet 5: e1000658 doi:1000610.1001371/journal.pgen.1000658.
54. Li W, Freudenberg J, (2011) A mathematical framework for examining whether a minimum number of chiasmata is required per metacentric chromosome or chromosome arm in human. Genomics 97: 186-192.
55. Li W, Freudenberg J, (2009) Two-parameters characterization of chromosome-scale recombination rate. Genome Res 19: 2300-2307.
56. Mezard C, Vignard J, Drouaud J, Mercier R, (2007) The road to crossovers: plants have their say. Trends Genet 23: 91-99.
57. Osman K, Higgins JD, Sanchez-Moran E, Armstrong SJ, Franklin FCH, (2011) Pathways to meiotic recombination in Arabidopsis thaliana. New Phytologist 190: 523-544.
58. Lhuissier FG, Offenberg HH, Wittich PE, Vischer NO, Heyting C, (2007) The mismatch repair protein MLH1 marks a subset of strongly interfering crossovers in tomato. Plant Cell 19: 862-876.
59. de Boer E, Lhuissier FG, Heyting C, (2009) Cytological analysis of interference in mouse meiosis. Methods Mol Biol pp. 355-382.
60. Borodin PM, Karamysheva TV, Rubtsov NB, (2008) Immunofluorescent analysis of meiotic recombination and interference in the domestic cat. Tsitologiia 50: 62-66.
61. Matise TC, Chen F, Chen W, De La Vega FM, Hansen M, et al. (2007) A second-generation combined linkage physical map of the human genome. Genome Res 17: 1783-1786.
62. Rasmussen S, Holm P, (1978) Human meiosis II. Chromosome pairing and recombination nodules in human spermatocytes. Carlsberg Research Communications 43: 275-327.
63. Bojko M, (1983) Human meiosis VIII. Chromosome pairing and formation of the synaptonemal complex in oocytes. Carlsberg Research Communications 48: 457-483.
64. Chelysheva L, Gendrot G, Vezon D, Doutriaux MP, Mercier R, et al. (2007) Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLoS Genet 3: e83 doi:10.1371/journal.pgen.0030083.
65. Dawe RK, (1998) Meiotic chromosome organization and segregation in plants. Annu Rev Plant Physiol Plant Mol Biol 49: 371-395.
66. Gerton JL, DeRisi J, Shroff R, Lichten M, Brown PO, et al. (2000) Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 97: 11383-11390.
67. Birdsell JA, (2002) Integrating genomics, bioinformatics, and classical genetics to study the effects of recombination on genome evolution. Mol Biol Evol 19: 1181-1197.
68. Myers S, Spencer CC, Auton A, Bottolo L, Freeman C, et al. (2006) The distribution and causes of meiotic recombination in the human genome. Biochem Soc Trans 34: 526-530.
69. Eyre-Walker A, (1993) Recombination and mammalian genome evolution. Proc Biol Sci 252: 237-243.
70. Marais G, (2003) Biased gene conversion: implications for genome and sex evolution. Trends Genet 19: 330-338.
71. Marsolier-Kergoat M-C, (2011) A simple model for the influence of meiotic conversion tracts on GC content. PLoS One 6: e16109 doi:16110.11371/journal.pone.0016109.
72. Bomblies K, Yant L, Laitinen RA, Kim ST, Hollister JD, et al. (2010) Local-scale patterns of genetic variability, outcrossing, and spatial structure in natural stands of Arabidopsis thaliana. PLoS Genet 6: e1000890 doi:1000810.1001371/journal.pgen.1000890.
73. Jander G, Norris SR, Rounsley SD, Bush DF, Levin IM, et al. (2002) Arabidopsis map-based cloning in the post-genome era. Plant Physiol 129: 440-450.
74. Broman KW, Weber JL, (2000) Characterization of human crossover interference. Am J Hum Genet 66: 1911-1926.
75. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc, Ser B, Methodol 57: 289-300.
76. Roudier F, Ahmed I, Berard C, Sarazin A, Mary-Huard T, et al. (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30: 1928-1938.