New paradigms for conserved, multifactorial, cis-acting regulation of meiotic recombination

Nucleic Acids Research

Volumn 40, Issue 20, 2012, Pages 9983-9989

  Wahls, Wayne P ^a   Davidson, Mari K ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR; ACTIVATING TRANSCRIPTION FACTOR 1; CCAAT BINDING FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HETERODIMER; PROTEIN PCR1; PROTEIN PHP2; PROTEIN PHP3; PROTEIN PHP5; PROTEIN RST2; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; DNA PROTEIN COMPLEX; EPIGENETICS; FUNGAL GENOME; GENETIC ASSOCIATION; GENETIC CONSERVATION; GENETIC REGULATION; HOMOLOGOUS RECOMBINATION; MAMMAL; MITOTIC RECOMBINATION; MOLECULAR BIOLOGY; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION;

DNA; DNA-BINDING PROTEINS; EVOLUTION, MOLECULAR; MEIOSIS; NUCLEOTIDE MOTIFS; RECOMBINATION, GENETIC;

MAMMALIA;

EID: 84869004897     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks761     Document Type: Article

References (64)

1. Goodstadt, L. and Ponting, C.P. (2011) Is the control of recombination conserved among diverse eukaryotes? Heredity, 106, 710-711
2. Lichten, M. and de Massy, B. (2011) The impressionistic landscape of meiotic recombination. Cell, 147, 267-270.
3. Segurel, L., Leffler, E.M. and Przeworski, M. (2011) The case of the fickle fingers: how the PRDM9 zinc finger protein specifies meiotic recombination hotspots in humans. PLoS Biol., 9, e1001211.
4. Gutz, H. (1971) Site specific induction of gene conversion in Schizosaccharomyces pombe. Genetics, 69, 331-337.
5. Schuchert, P., Langsford, M., Kaslin, E. and Kohli, J. (1991) A specific DNA sequence is required for high frequency of recombination in the ade6 gene of fission yeast. EMBO J., 10, 2157-2163.
6. Steiner, W.W., Steiner, E.M., Girvin, A.R. and Plewik, L.E. (2009) Novel nucleotide sequence motifs that produce hotspots of meiotic recombination in Schizosaccharomyces pombe. Genetics, 182, 459-469.
7. Steiner, W.W., Davidow, P.A. and Bagshaw, A.T. (2011) Important characteristics of sequence-specific recombination hotspots in Schizosaccharomyces pombe. Genetics, 187, 385-396.
8. 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.
9. Hinch, A.G., Tandon, A., Patterson, N., Song, Y., Rohland, N., Palmer, C.D., Chen, G.K., Wang, K., Buxbaum, S.G., Akylbekova, E.L. et al. (2011) The landscape of recombination in African Americans. Nature, 476, 170-175.
10. Berg, I.L., Neumann, R., Sarbajna, S., Odenthal-Hesse, L., Butler, N.J. and Jeffreys, A.J. (2011) Variants of the protein PRDM9 differentially regulate a set of human meiotic recombination hotspots highly active in African populations. Proc. Natl Acad. Sci. USA, 108, 12378-12383.
11. 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.
12. Wahls, W.P. and Smith, G.R. (1994) A heteromeric protein that binds to a meiotic homologous recombination hot spot: correlation of binding and hot spot activity. Genes Dev., 8, 1693-1702.
13. Steiner, W.W. and Smith, G.R. (2005) Natural meiotic recombination hot spots in the Schizosaccharomyces pombe genome successfully predicted from the simple sequence motif M26. Mol. Cell. Biol., 25, 9054-9062.
14. Wahls, W.P. and Davidson, M.K. (2010) Discrete DNA sites regulate global distribution of meiotic recombination. Trends Genet., 26, 202-208.
15. White, M.A., Wierdl, M., Detloff, P. and Petes, T.D. (1991) DNA-binding protein RAP1 stimulates meiotic recombination at the HIS4 locus in yeast. Proc. Natl Acad. Sci. USA, 88, 9755-9759.
16. White, M.A., Dominska, M. and Petes, T.D. (1993) Transcription factors are required for the meiotic recombination hotspot at the HIS4 locus in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 90, 6621-6625.
17. Fan, Q., Xu, F. and Petes, T.D. (1995) Meiosis-specific double-strand DNA breaks at the HIS4 recombination hot spot in the yeast Saccharomyces cerevisiae: control in cis and trans. Mol. Cell. Biol., 15, 1679-1688.
18. Mieczkowski, P.A., Dominska, M., Buck, M.J., Gerton, J.L., Lieb, J.D. and Petes, T.D. (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, 1014-1027.
19. Pan, J., Sasaki, M., Kniewel, R., Murakami, H., Blitzblau, H.G., Tischfield, S.E., Zhu, X., Neale, M.J., Jasin, M., Socci, N.D. et al. (2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell, 144, 719-731.
20. Cromie, G.A., Hyppa, R.W., Cam, H.P., Farah, J.A., Grewal, S.I. and Smith, G.R. (2007) A discrete class of intergenic DNA dictates meiotic DNA break hotspots in fission yeast. PLoS Genet., 3, e141.
21. Hyppa, R.W., Cromie, G.A. and Smith, G.R. (2008) Indistinguishable landscapes of meiotic DNA breaks in rad50+ and rad50S strains of fission yeast revealed by a novel rad50+ recombination intermediate. PLoS Genet., 4, e1000267.
22. Jiang, H., Li, N., Gopalan, V., Zilversmit, M.M., Varma, S., Nagarajan, V., Li, J., Mu, J., Hayton, K., Henschen, B. et al. (2011) High recombination rates and hotspots in a Plasmodium falciparum genetic cross. Genome. Biol., 12, R33.
23. Kulathinal, R.J., Bennett, S.M., Fitzpatrick, C.L. and Noor, M.A. (2008) Fine-scale mapping of recombination rate in Drosophila refines its correlation to diversity and divergence. Proc. Natl Acad. Sci. USA, 105, 10051-10056.
24. Miller, D.E., Takeo, S., Nandanan, K., Paulson, A., Gogol, M.M., Noll, A.C., Perera, A.G., Walton, K.N., Gilliland, W.D., Li, H. et al. (2012) A whole-chromosome analysis of meiotic recombination in Drosophila melanogaster. G3 (Bethesda), 2, 249-260.
25. Stevison, L.S. and Noor, M.A. (2010) Genetic and evolutionary correlates of fine-scale recombination rate variation in Drosophila persimilis. J. Mol. Evol., 71, 332-345.
26. Bessoltane, N., Toffano-Nioche, C., Solignac, M. and Mougel, F. (2012) Fine scale analysis of crossover and non-crossover and detection of recombination sequence motifs in the honeybee (Apis mellifera). PLoS One, 7, e36229.
27. Billings, T., Sargent, E.E., Szatkiewicz, J.P., Leahy, N., Kwak, I.Y., Bektassova, N., Walker, M., Hassold, T., Graber, J.H., Broman, K.W. et al. (2010) Patterns of recombination activity on mouse chromosome 11 revealed by high resolution mapping. PLoS One, 5, e15340.
28. Wu, M., Kwoh, C.K., Przytycka, T.M., Li, J. and Zheng, J. (2012) Epigenetic functions enriched in transcription factors binding to mouse recombination hotspots. Proteome Sci., 10(Suppl 1), S11.
29. Zhang, J., Li, F., Li, J., Zhang, M. and Zhang, X. (2004) Evidence and characteristics of putative human alpha recombination hotspots. Hum. Mol. Genet., 13, 2823-2828.
30. Myers, S., Bottolo, L., Freeman, C., McVean, G. and Donnelly, P. (2005) A fine-scale map of recombination rates and hotspots across the human genome. Science, 310, 321-324.
31. Zahn-Zabal, M., Lehmann, E. and Kohli, J. (1995) Hot spots of recombination in fission yeast: inactivation of the M26 hot spot by deletion of the ade6 promoter and the novel hotspot ura4-aim. Genetics, 140, 469-478.
32. Kon, N., Krawchuk, M.D., Warren, B.G., Smith, G.R. and Wahls, W.P. (1997) Transcription factor Mts1/Mts2 (Atf1/Pcr1, Gad7/Pcr1) activates the M26 meiotic recombination hotspot in Schizosaccharomyces pombe. Proc. Natl Acad. Sci. USA, 94, 13765-13770.
33. Heckman, D.S., Geiser, D.M., Eidell, B.R., Stauffer, R.L., Kardos, N.L. and Hedges, S.B. (2001) Molecular evidence for the early colonization of land by fungi and plants. Science, 293, 1129-1133.
34. 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.
35. Berg, I.L., Neumann, R., Lam, K.W., Sarbajna, S., Odenthal- Hesse, L., May, C.A. and Jeffreys, A.J. (2010) PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nat. Genet., 42, 859-863.
36. Kong, A., Thorleifsson, G., Gudbjartsson, D.F., Masson, G., Sigurdsson, A., Jonasdottir, A., Walters, G.B., Jonasdottir, A., Gylfason, A., Kristinsson, K.T. et al. (2010) Fine-scale recombination rate differences between sexes, populations and individuals. Nature, 467, 1099-1103.
37. Grey, C., Barthes, P., Chauveau-Le Friec, G., Langa, F., Baudat, F. and de Massy, B. (2011) Mouse PRDM9 DNA-binding specificity determines sites of histone H3 lysine 4 trimethylation for initiation of meiotic recombination. PLoS Biol., 9, e1001176.
38. Brick, K., Smagulova, F., Khil, P., Camerini-Otero, R.D. and Petukhova, G.V. (2012) Genetic recombination is directed away from functional genomic elements in mice. Nature, 485, 642-645.
39. Gao, J., Davidson, M.K. and Wahls, W.P. (2008) Distinct regions of ATF/CREB proteins Atf1 and Pcr1 control recombination hotspot ade6-M26 and the osmotic stress response. Nucleic Acids Res., 36, 2838-2851.
40. Davidson, M.K., Shandilya, H.K., Hirota, K., Ohta, K. and Wahls, W.P. (2004) Atf1-Pcr1-M26 complex links stress-activated MAPK and cAMP-dependent protein kinase pathways via chromatin remodeling of cgs2+. J. Biol. Chem., 279, 50857-50863.
41. Jia, S., Noma, K. and Grewal, S.I. (2004) RNAi-independent heterochromatin nucleation by the stress-activated ATF/CREB family proteins. Science, 304, 1971-1976.
42. Yamada, T., Mizuno, K., Hirota, K., Kon, N., Wahls, W.P., Hartsuiker, E., Murofushi, H., Shibata, T. and Ohta, K. (2004) Roles of histone acetylation and chromatin remodeling factor in a meiotic recombination hotspot. EMBO J., 23, 1792-1803.
43. Kon, N., Schroeder, S.C., Krawchuk, M.D. and Wahls, W.P. (1998) Regulation of the Mts1-Mts2-dependent ade6-M26 meiotic recombination hotspot and developmental decisions by the Spc1 mitogen-activated protein kinase of fission yeast. Mol. Cell. Biol., 18, 7575-7583.
44. Mizuno, K., Hasemi, T., Ubukata, T., Yamada, T., Lehmann, E., Kohli, J., Watanabe, Y., Iino, Y., Yamamoto, M., Fox, M.E. et al. (2001) Counteracting regulation of chromatin remodeling at a fission yeast cAMP response element-related recombination hotspot by stress-activated protein kinase, cAMP-dependent kinase and meiosis regulators. Genetics, 159, 1467-1478.
45. Hirota, K., Steiner, W.W., Shibata, T. and Ohta, K. (2007) Multiple modes of chromatin configuration at natural meiotic recombination hot spots in fission yeast. Eukaryot. Cell, 6, 2072-2080.
46. Gao, J., Davidson, M.K. and Wahls, W.P. (2009) Phosphorylation- independent regulation of Atf1-promoted meiotic recombination by stress-activated, p38 kinase Spc1 of fission yeast. PLoS One, 4, e5533.
47. Kirkpatrick, D.T., Fan, Q. and Petes, T.D. (1999) Maximal stimulation of meiotic recombination by a yeast transcription factor requires the transcription activation domain and a DNA-binding domain. Genetics, 152, 101-115.
48. Oliver, P.L., Goodstadt, L., Bayes, J.J., Birtle, Z., Roach, K.C., Phadnis, N., Beatson, S.A., Lunter, G., Malik, H.S. and Ponting, C.P. (2009) Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet., 5, e1000753.
49. Hayashi, K., Yoshida, K. and Matsui, Y. (2005) A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature, 438, 374-378.
50. Axelsson, E., Webster, M.T., Ratnakumar, A., Ponting, C.P. and Lindblad-Toh, K. (2012) Death of PRDM9 coincides with stabilization of the recombination landscape in the dog genome. Genome Res., 22, 51-63.
51. Auton, A., Fledel-Alon, A., Pfeifer, S., Venn, O., Segurel, L., Street, T., Leffler, E.M., Bowden, R., Aneas, I., Broxholme, J. et al. (2012) A fine-scale chimpanzee genetic map from population sequencing. Science, 336, 193-198.
52. Sollier, J., Lin, W., Soustelle, C., Suhre, K., Nicolas, A., Geli, V. and de La Roche Saint-Andre, C. (2004) Set1 is required for meiotic S-phase onset, double-strand break formation and middle gene expression. EMBO J., 23, 1957-1967.
53. Borde, V., Robine, N., Lin, W., Bonfils, S., Geli, V. and Nicolas, A. (2009) Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J., 28, 99-111.
54. Brocks, J.J., Logan, G.A., Buick, R. and Summons, R.E. (1999) Archean molecular fossils and the early rise of eukaryotes. Science, 285, 1033-1036.
55. Reddy, K.C. and Villeneuve, A.M. (2004) C. elegans HIM-17 links chromatin modification and competence for initiation of meiotic recombination. Cell, 118, 439-452.
56. Yamashita, K., Shinohara, M. and Shinohara, A. (2004) Rad6-Bre1-mediated histone H2B ubiquitylation modulates the formation of double-strand breaks during meiosis. Proc. Natl Acad. Sci. USA, 101, 11380-11385.
57. Hirota, K., Mizuno, K., Shibata, T. and Ohta, K. (2008) Distinct chromatin modulators regulate the formation of accessible and repressive chromatin at the fission yeast recombination hotspot ade6-M26. Mol. Biol. Cell, 19, 1162-1173.
58. Buard, J., Barthes, P., Grey, C. and de Massy, B. (2009) Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J., 28, 2616-2624.
59. 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.
60. Merker, J.D., Dominska, M., Greenwell, P.W., Rinella, E., Bouck, D.C., Shibata, Y., Strahl, B.D., Mieczkowski, P. and Petes, T.D. (2008) The histone methylase Set2p and the histone deacetylase Rpd3p repress meiotic recombination at the HIS4 meiotic recombination hotspot in Saccharomyces cerevisiae. DNA Repair (Amst.), 7, 1298-1308.
61. Mieczkowski, P.A., Dominska, M., Buck, M.J., Lieb, J.D. and Petes, T.D. (2007) Loss of a histone deacetylase dramatically alters the genomic distribution of Spo11p-catalyzed DNA breaks in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 104, 3955-3960.
62. 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.
63. de Castro, E., Soriano, I., Marin, L., Serrano, R., Quintales, L. and Antequera, F. (2011) Nucleosomal organization of replication origins and meiotic recombination hotspots in fission yeast. EMBO J., 31, 124-137.
64. Szankasi, P., Heyer, W.D., Schuchert, P. and Kohli, J. (1988) DNA sequence analysis of the ade6 gene of Schizosaccharomyces pombe. Wild-type and mutant alleles including the recombination hot spot allele ade6-M26. J. Mol. Biol., 204, 917-925.