DNA crossover motifs associated with epigenetic modifications delineate open chromatin regions in arabidopsis

Plant Cell

Volumn 27, Issue 9, 2015, Pages 2427-2436

  Shilo, Shay ^a   Melamed Bessudo, Cathy ^a   Dorone, Yanniv ^a,b   Barkai, Naama ^a   Levy, Avraham A ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN;

ARABIDOPSIS; CHROMATIN; CROSSING OVER; DNA METHYLATION; GENETIC EPIGENESIS; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE MOTIF; PROMOTER REGION; TRINUCLEOTIDE REPEAT;

ARABIDOPSIS; CHROMATIN; CROSSING OVER, GENETIC; DNA METHYLATION; EPIGENESIS, GENETIC; MOLECULAR SEQUENCE DATA; NUCLEOTIDE MOTIFS; PROMOTER REGIONS, GENETIC; TRINUCLEOTIDE REPEATS;

EID: 84943778851     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.15.00391     Document Type: Article

References (53)

1. Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., Ren, J., Li, W.W., and Noble, W.S. (2009). MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37: W202-W208.
2. Bailey, T.L., and Elkan, C. (1994). Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2: 28-36.
3. Bateson, W., Saunders, E.R., and Punnett, R.C. (1906). Further experiments on inheritance in sweet peas and stocks: Preliminary account. Proc. R. Soc. Lond. B 77: 236-238.
4. Baudat, F., Buard, J., Grey, C., Fledel-Alon, A., Ober, C., Przeworski, M., Coop, G., and de Massy, B. (2010). PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327: 836-840.
5. Baudat, F., Imai, Y., and de Massy, B. (2013). Meiotic recombination in mammals: localization and regulation. Nat. Rev. Genet. 14: 794-806.
6. Berchowitz, L.E., and Copenhaver, G.P. (2008). Fluorescent Arabidopsis tetrads: a visual assay for quickly developing large crossover and crossover interference data sets. Nat. Protoc. 3: 41-50.
7. Blecher-Gonen, R., Barnett-Itzhaki, Z., Jaitin, D., Amann-Zalcenstein, D., Lara-Astiaso, D., and Amit, I. (2013). Highthroughput chromatin immunoprecipitation for genome-wide mapping of in vivo protein-DNA interactions and epigenomic states. Nat. Protoc. 8: 539-554.
8. Brunschwig, H., Levi, L., Ben-David, E., Williams, R.W., Yakir, B., and Shifman, S. (2012). Fine-scale maps of recombination rates and hotspots in the mouse genome. Genetics 191: 757-764.
9. Brzeski, J., and Jerzmanowski, A. (2003). Deficient in DNA methylation 1 (DDM1) defines a novel family of chromatin-remodeling factors. J. Biol. Chem. 278: 823-828.
10. Chodavarapu, R.K., et al. (2010). Relationship between nucleosome positioning and DNA methylation. Nature 466: 388-392.
11. Choi, K., and Henderson, I.R. (2015). Meiotic recombination hotspots - a comparative view. Plant J. 83: 52-61.
12. Choi, K., Zhao, X., Kelly, K.A., Venn, O., Higgins, J.D., Yelina, N.E., Hardcastle, T.J., Ziolkowski, P.A., Copenhaver, G.P., Franklin, F.C.H., McVean, G., and Henderson, I.R. (2013). Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters. Nat. Genet. 45: 1327-1336.
13. Colomé-Tatché, M., et al. (2012). Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. Proc. Natl. Acad. Sci. USA 109: 16240-16245.
14. Comeron, J.M., Ratnappan, R., and Bailin, S. (2012). The many landscapes of recombination in Drosophila melanogaster. PLoS Genet. 8: e1002905.
15. Copenhaver, G.P., Browne, W.E., and Preuss, D. (1998). Assaying genome-wide recombination and centromere functions with Arabidopsis tetrads. Proc. Natl. Acad. Sci. USA 95: 247-252.
16. Drouaud, J., Khademian, H., Giraut, L., Zanni, V., Bellalou, S., Henderson, I.R., Falque, M., and Mézard, C. (2013). Contrasted patterns of crossover and non-crossover at Arabidopsis thaliana meiotic recombination hotspots. PLoS Genet. 9: e1003922.
17. Feng, S., Jacobsen, S.E., and Reik, W. (2010). Epigenetic reprogramming in plant and animal development. Science 330: 622-627.
18. Francis, K.E., Lam, S.Y., and Copenhaver, G.P. (2006). Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiol. 142: 1004-1013.
19. Francis, K.E., Lam, S.Y., Harrison, B.D., Bey, A.L., Berchowitz, L.E., and Copenhaver, G.P. (2007). Pollen tetrad-based visual assay for meiotic recombination in Arabidopsis. Proc. Natl. Acad. Sci. USA 104: 3913-3918.
20. Giraut, L., Falque, M., Drouaud, J., Pereira, L., Martin, O.C., and Mézard, C. (2011). Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLoS Genet. 7: e1002354.
21. Gore, M.A., Chia, J.M., Elshire, R.J., Sun, Q., Ersoz, E.S., Hurwitz, B.L., Peiffer, J.A., McMullen, M.D., Grills, G.S., Ross-Ibarra, J., Ware, D.H., and Buckler, E.S. (2009). A first-generation haplotype map of maize. Science 326: 1115-1117.
22. Hayashi, K., Yoshida, K., and Matsui, Y. (2005). A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438: 374-378.
23. Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y.C., Laslo, P., Cheng, J.X., Murre, C., Singh, H., and Glass, C.K. (2010). Simple combinations of lineage-determining transcription factors primecis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38: 576-589.
24. Henson, S., Bishop, R.P., Morzaria, S., Spooner, P.R., Pelle, R., Poveda, L., Ebeling, M., Küng, E., Certa, U., Daubenberger, C.A., and Qi, W. (2012). High-resolution genotyping and mapping of recombination and gene conversion in the protozoan Theileria parva using whole genome sequencing. BMC Genomics 13: 503.
25. Horton, M.W., et al. (2012). Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nat. Genet. 44: 212-216.
26. Hou, Y., Fan, W., Yan, L., Li, R., Lian, Y., Huang, J., Li, J., Xu, L., Tang, F., Xie, X.S., and Qiao, J. (2013). Genome analyses of single human oocytes. Cell 155: 1492-1506.
27. Kaplan, N., Moore, I.K., Fondufe-Mittendorf, Y., Gossett, A.J., Tillo, D., Field, Y., LeProust, E.M., Hughes, T.R., Lieb, J.D., Widom, J., and Segal, E. (2009). The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458: 362-366.
28. Li, X., Li, L., and Yan, J. (2015). Dissecting meiotic recombination based on tetrad analysis by single-microspore sequencing in maize. Nat. Commun. 6: 6648.
29. Lu, P., Han, X., Qi, J., Yang, J., Wijeratne, A.J., Li, T., and Ma, H. (2012a). 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: 508-518.
30. Lu, S., et al. (2012b). Probing meiotic recombination and aneuploidy of single sperm cells by whole-genome sequencing. Science 338: 1627-1630.
31. Mancera, E., Bourgon, R., Brozzi, A., Huber, W., and Steinmetz, L.M. (2008). High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454: 479-485.
32. Melamed-Bessudo, C., and Levy, A.A. (2012). Deficiency in DNA methylation increases meiotic crossover rates in euchromatic but not in heterochromatic regions in Arabidopsis. Proc. Natl. Acad. Sci. USA 109: E981-E988.
33. Melamed-Bessudo, C., Yehuda, E., Stuitje, A.R., and Levy, A.A. (2005). A new seed-based assay for meiotic recombination in Arabidopsis thaliana. Plant J. 43: 458-466.
34. Mirouze, M., Lieberman-Lazarovich, M., Aversano, R., Bucher, E., Nicolet, J., Reinders, J., and Paszkowski, J. (2012). Loss of DNA methylation affects the recombination landscape in Arabidopsis. Proc. Natl. Acad. Sci. USA 109: 5880-5885.
35. Morgan, T.H. (1911). Random segregation versus coupling in Mendelian inheritance. Science 34: 384.
36. Myers, S., Freeman, C., Auton, A., Donnelly, P., and McVean, G. (2008). A common sequence motif associated with recombination hot spots and genome instability in humans. Nat. Genet. 40: 1124-1129
37. Oliver, C., Pradillo, M., Corredor, E., and Cuñado, N. (2013). The dynamics of histone H3 modifications is species-specific in plant meiosis. Planta 238: 23-33.
38. Preuss, D., Rhee, S.Y., and Davis, R.W. (1994). Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264: 1458-1460.
39. Qi, J., Chen, Y., Copenhaver, G.P., and Ma, H. (2014). Detection of genomic variations and DNA polymorphisms and impact on analysis of meiotic recombination and genetic mapping. Proc. Natl. Acad. Sci. USA 111: 10007-10012.
40. Rodgers-Melnick, E., Bradbury, P.J., Elshire, R.J., Glaubitz, J.C., Acharya, C.B., Mitchell, S.E., Li, C., Li, Y., and Buckler, E.S. (2015). Recombination in diverse maize is stable, predictable, and associated with genetic load. Proc. Natl. Acad. Sci. USA 112: 3823-3828.
41. San Filippo, J., Sung, P., and Klein, H. (2008). Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77: 229-257.
42. Sasaki, H., and Matsui, Y. (2008). Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat. Rev. Genet. 9: 129-140.
43. Segal, E., and Widom, J. (2009). Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr. Opin. Struct. Biol. 19: 65-71.
44. Smagulova, F., Gregoretti, I.V., Brick, K., Khil, P., Camerini-Otero, R.D., and Petukhova, G.V. (2011). Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472: 375-378.
45. Sun, Y., Ambrose, J.H., Haughey, B.S., Webster, T.D., Pierrie, S.N., Muñoz, D.F., Wellman, E.C., Cherian, S., Lewis, S.M., Berchowitz, L.E., and Copenhaver, G.P. (2012). Deep genome-wide measurement of meiotic gene conversion using tetrad analysis in Arabidopsis thaliana. PLoS Genet. 8: e1002968.
46. Vizir, I.Y., and Korol, A.B. (1990). Sex difference in recombination frequency in Arabidopsis. Heredity (Edinb.) 65: 379-383.
47. Wang, J., Fan, H.C., Behr, B., and Quake, S.R. (2012). Genome-wide single-cell analysis of recombination activity and de novo mutation rates in human sperm. Cell 150: 402-412.
48. Wijnker, E., et al. (2013). The genomic landscape of meiotic crossovers and gene conversions in Arabidopsis thaliana. eLife 2: e01426.
49. Yang, S., Yuan, Y., Wang, L., Li, J., Wang, W., Liu, H., Chen, J.-Q., Hurst, L.D., and Tian, D. (2012). Great majority of recombination events in Arabidopsis are gene conversion events. Proc. Natl. Acad. Sci. USA 109: 20992-20997.
50. Yelina, N.E., et al. (2012). Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLoS Genet. 8: e1002844.
51. Yelina, N.E., Ziolkowski, P.A., Miller, N., Zhao, X., Kelly, K.A., Muñoz, D.F., Mann, D.J., Copenhaver, G.P., and Henderson, I.R. (2013). High-throughput analysis of meiotic crossover frequency and interference via flow cytometry of fluorescent pollen in Arabidopsis thaliana. Nat. Protoc. 8: 2119-2134.
52. Youds, J.L., and Boulton, S.J. (2011). The choice in meiosis - defining the factors that influence crossover or non-crossover formation. J. Cell Sci. 124: 501-513.
53. Zemach, A., Kim, M.Y., Hsieh, P.-H., Coleman-Derr, D., Eshed-Williams, L., Thao, K., Harmer, S.L., and Zilberman, D. (2013). The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153: 193-205