Deep Genome-Wide Measurement of Meiotic Gene Conversion Using Tetrad Analysis in Arabidopsis thaliana

PLoS Genetics

Volumn 8, Issue 10, 2012, Pages

  Sun, Yujin ^a   Ambrose, Jonathan H ^a   Haughey, Brena S ^a   Webster, Tyler D ^a   Pierrie, Sarah N ^a   Muñoz, Daniela F ^a   Wellman, Emily C ^a   Cherian, Shalom ^a   Lewis, Scott M ^a   Berchowitz, Luke E ^a   Copenhaver, Gregory P ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ARABIDOPSIS; ARTICLE; CHROMOSOME 4; DNA SYNTHESIS; FLOWERING; GAMETE; GENE CONVERSION; GENE FREQUENCY; GENE LOCATION; GENE LOCUS; GENE MUTATION; GENETIC ASSOCIATION; GENETIC MANIPULATION; GENETIC VARIABILITY; GENOME ANALYSIS; MEIOSIS; NONHUMAN; PLANT GENOME; PROCESS DEVELOPMENT; PROTEIN EXPRESSION;

ALLELES; ARABIDOPSIS; GENE CONVERSION; GENOME, PLANT; MEIOSIS; MODELS, GENETIC; PLANTS, GENETICALLY MODIFIED; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; RECOMBINATION, GENETIC;

ARABIDOPSIS THALIANA; FUNGI; MAGNOLIOPHYTA;

EID: 84868098927     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002968     Document Type: Article

References (59)

1. Lichten M, Borts RH, Haber JE, (1987) Meiotic gene conversion and crossing over between dispersed homologous sequences occurs frequently in Saccharomyces cerevisiae. Genetics 115: 233-246.
2. Lindegren CC, (1955) Non-Mendelian Segregation in a Single Tetrad of Saccharomyces Ascribed to Gene Conversion. Science (New York, NY) 121: 605-607.
3. Chen J-M, Cooper DN, Chuzhanova N, Férec C, Patrinos GP, (2007) Gene conversion: mechanisms, evolution and human disease. Nature reviews Genetics 8: 762-775.
4. Keeney S, Giroux CN, Kleckner N, (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375-384.
5. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW, (1983) The double-strand-break repair model for recombination. Cell 33: 25-35.
6. Allers T, Lichten M, (2001) Intermediates of yeast meiotic recombination contain heteroduplex DNA. Molecular cell 8: 225-231.
7. Allers T, Lichten M, (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47-57.
8. McMahill MS, Sham CW, Bishop DK, (2007) Synthesis-dependent strand annealing in meiosis. PLoS Biol 5: e299 doi:10.1371/journal.pbio.0050299.
9. Borts RH, Chambers SR, Abdullah MF, (2000) The many faces of mismatch repair in meiosis. Mutation research 451: 129-150.
10. Duret L, Galtier N, (2009) Biased gene conversion and the evolution of mammalian genomic landscapes. Annual review of genomics and human genetics 10: 285-311.
11. Muyle A, Serres-Giardi L, Ressayre A, Escobar J, Glémin S, (2011) GC-biased gene conversion and selection affect GC content in the Oryza genus (rice). Molecular biology and evolution 28: 2695-2706.
12. Serres-Giardi L, Belkhir K, David J, Glémin S, (2012) Patterns and evolution of nucleotide landscapes in seed plants. The Plant cell 24: 1379-1397.
13. Winkler H, (1932) Konversions-Theorie und Austasch-Theorie. Biologisches Zentralblatt 52: 163-189.
14. Zickler H, (1934) Genetische Untersuchungen an einem heterothallischen Askomyzeten (Bombardia lunata nov. spec.). Planta 22: 573-613.
15. 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.
16. Gay J, Myers S, McVean G, (2007) Estimating meiotic gene conversion rates from population genetic data. Genetics 177: 881-894.
17. Berchowitz LE, Copenhaver GP, (2010) Genetic interference: don't stand so close to me. Current genomics 11: 91-102.
18. Shi J, Wolf SE, Burke JM, Presting GG, Ross-Ibarra J, et al.(2010) Widespread gene conversion in centromere cores. PLoS Biol 8: e1000327 doi:10.1371/journal.pbio.1000327.
19. Choo KH, (1998) Why is the centromere so cold? Genome Res 8: 81-82.
20. Beadle GW, (1932) A Possible Influence of the Spindle Fibre on Crossing-Over in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 18: 160-165.
21. Lu P, Han X, Qi J, Yang J, Wijeratne AJ, et al.(2011) Analysis of Arabidopsis genome-wide variations before and after meiosis and meiotic recombination by re-sequencing Landsberg erecta and all four products of a single meiosis. Genome Res 22: 508-18.
22. Berchowitz LE, Copenhaver GP, (2009) Visual markers for detecting gene conversion directly in the gametes of Arabidopsis thaliana. Methods in molecular biology (Clifton, NJ) 557: 99-114.
23. Francis KE, Lam SY, Harrison BD, Bey AL, Berchowitz LE, et al.(2007) Pollen tetrad-based visual assay for meiotic recombination in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 104: 3913-3918.
24. Twell D, Yamaguchi J, McCormick S, (1990) Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Development (Cambridge, England) 109: 705-713.
25. Francis KE, Lam SY, Copenhaver GP, (2006) Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant physiology 142: 1004-1013.
26. Preuss D, Rhee SY, Davis RW, (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science (New York, NY) 264: 1458-1460.
27. Berchowitz LE, Copenhaver GP, (2008) Fluorescent Arabidopsis tetrads: a visual assay for quickly developing large crossover and crossover interference data sets. Nature protocols 3: 41-50.
28. Borts RH, Haber JE, (1987) Meiotic recombination in yeast: alteration by multiple heterozygosities. Science (New York, NY) 237: 1459-1465.
29. Dooner HK, (2002) Extensive interallelic polymorphisms drive meiotic recombination into a crossover pathway. The Plant cell 14: 1173-1183.
30. Jorgensen R, Snyder C, Jones JDG, (1987) T-DNA is organized predominantly in inverted repeat structures in plants transformed with Agrobacterium tumefaciens C58 derivatives. MGG Molecular & General Genetics 207: 471-477.
31. Szabados L, Kovács I, Oberschall A, Abrahám E, Kerekes I, et al.(2002) Distribution of 1000 sequenced T-DNA tags in the Arabidopsis genome. The Plant journal: for cell and molecular biology 32: 233-242.
32. Krysan PJ, Young JC, Jester PJ, Monson S, Copenhaver G, et al.(2002) Characterization of T-DNA insertion sites in Arabidopsis thaliana and the implications for saturation mutagenesis. Omics: a journal of integrative biology 6: 163-174.
33. Greene Ea, Codomo Ca, Taylor NE, Henikoff JG, Till BJ, et al.(2003) Spectrum of chemically induced mutations from a large-scale reverse-genetic screen in Arabidopsis. Genetics 164: 731-740.
34. Kovalchuk I, Kovalchuk O, Hohn B, (2000) Genome-wide variation of the somatic mutation frequency in transgenic plants. The EMBO journal 19: 4431-4438.
35. Schultes NP, Szostak JW, (1990) Decreasing gradients of gene conversion on both sides of the initiation site for meiotic recombination at the ARG4 locus in yeast. Genetics 126: 813-822.
36. Malone RE, Bullard S, Lundquist S, Kim S, Tarkowski T, (1992) A meiotic gene conversion gradient opposite to the direction of transcription. Nature 359: 154-155.
37. Sun H, Treco D, Schultes NP, Szostak JW, (1989) Double-strand breaks at an initiation site for meiotic gene conversion. Nature 338: 87-90.
38. Detloff P, White MA, Petes TD, (1992) Analysis of a gene conversion gradient at the HIS4 locus in Saccharomyces cerevisiae. Genetics 132: 113-123.
39. Nicolas a, Petes TD, (1994) Polarity of meiotic gene conversion in fungi: contrasting views. Experientia 50: 242-252.
40. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP, (2007) The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genet 3: e132 doi:10.1371/journal.pgen.0030132.
41. The Arabidopsis GenomeInitiative(2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
42. Copenhaver GP, Nickel K, Kuromori T, Benito MI, Kaul S, et al.(1999) Genetic Definition and Sequence Analysis of Arabidopsis Centromeres. Science 286: 2468-2474.
43. Copenhaver GP, (2003) Using Arabidopsis to understand centromere function: progress and prospects. Chromosome research: an international journal on the molecular, supramolecular and evolutionary aspects of chromosome biology 11: 255-262.
44. Copenhaver GP, Pikaard CS, (1996) Two-dimensional RFLP analyses reveal megabase-sized clusters of rRNA gene variants in Arabidopsis thaliana, suggesting local spreading of variants as the mode for gene homogenization during concerted evolution. The Plant journal: for cell and molecular biology 9: 273-282.
45. Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L, et al.(2005) Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3,whereas the other one is not. Current biology: CB 15: 692-701.
46. Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N, et al.(2005) AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. Journal of cell science 118: 4621-4632.
47. Sanchez-Moran E, Santos J-L, Jones GH, Franklin FCH, (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes & development 21: 2220-2233.
48. Copenhaver GP, Browne WE, Preuss D, (1998) Assaying genome-wide recombination and centromere functions with Arabidopsis tetrads. Proceedings of the National Academy of Sciences of the United States of America 95: 247-252.
49. Sanchez Moran E, Armstrong SJ, Santos JL, Franklin FC, Jones GH, (2001) Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Research 9: 121-128.
50. Sturtevant AH, (1925) The Effects of Unequal Crossing over at the Bar Locus in Drosophila. Genetics 10: 117-147.
51. Novitski E, (1955) Genetic measures of centromere activity in Drosophila melanogaster. Journal of cellular physiology Supplement 45: 151-169.
52. Haber JE, Thorburn PC, Rogers D, (1984) Meiotic and mitotic behavior of dicentric chromosomes in Saccharomyces cerevisiae. Genetics 106: 185-205.
53. Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG, et al.(2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144: 719-731.
54. Schwartz D, (1953) Evidence for Sister-Strand Crossing over in Maize. Genetics 38: 251-260.
55. Michaelis A, (1959) Uber Das Verhalten Eines Ringchromosoms In Der Mitose Und Meiose Von Antirrhinum majus L. Chromosoma 10: 144-162.
56. Goldfarb T, Lichten M, (2010) Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS Biol 8: e1000520 doi:10.1371/journal.pbio.1000520.
57. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, et al.(2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science (New York, NY) 301: 653-657.
58. Forsbach A, Schubert D, Lechtenberg B, Gils M, Schmidt R, (2003) A comprehensive characterization of single-copy T-DNA insertions in the Arabidopsis thaliana genome. Plant molecular biology 52: 161-176.
59. McDonald JH (2009) Handbook of Biological Statistics. 2nd ed. Baltimore, Maryland: Sparky House Publishing.