Chromodomains direct integration of retrotransposons to heterochromatin

Genome Research

Volumn 18, Issue 3, 2008, Pages 359-369

  Gao, Xiang ^a,c   Hou, Yi ^a   Ebina, Hirotaka ^b   Levin, Henry L ^b   Voytas, Daniel F ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DNA MODIFICATION; DNA SEQUENCE; EPIGENETICS; GENE INSERTION SEQUENCE; GENETIC EPIGENESIS; GENETIC VARIABILITY; GENOME ANALYSIS; HETEROCHROMATIN; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN METHYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RETROPOSON; SCHIZOSACCHAROMYCES POMBE; SEQUENCE ANALYSIS; TRANSPOSON;

ANIMALS; BINDING SITES; EPIGENESIS, GENETIC; GENOMICS; HETEROCHROMATIN; HISTONES; INTEGRASES; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, NUCLEIC ACID; RETROELEMENTS;

SCHIZOSACCHAROMYCES POMBE;

EID: 40449136688     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.7146408     Document Type: Article

References (99)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
2. The Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
3. Asakawa, K., Toya, M., Sato, M., Kanai, M., Kume, K., Goshima, T., Garcia, M.A., Hirata, D., and Toda, T. 2005. Mal3, the fission yeast EB1 homologue, cooperates with Bub1 spindle checkpoint to prevent monopolar attachment. EMBO Rep. 6: 1194-1200.
4. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. 1987. Current protocols in molecular biology. Greene/Wiley Interscience, New York.
5. Bachman, N., Gelbart, M.E., Tsukiyama, T., and Boeke, J.D. 2005. TFIIIB subunit Bdp1p is required for periodic integration of the Ty1 retrotransposon and targeting of Isw2p to S. cerevisiae tDNAs. Genes & Dev. 19: 955-964.
6. Bannister, A.J., Zegerman, P., Partridge, J.F., Miska, E.A., Thomas, J.O., Allshire, R.C., and Kouzarides, T. 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410: 120-124.
7. Banno, H., Ikeda, Y., Niu, Q.W., and Chua, N.H. 2001. Overexpression of Arabidopsis ESR1 induces initiation of shoot regeneration. Plant Cell 13: 2609-2618.
8. Behrens, R., Hayles, J., and Nurse, P. 2000. Fission yeast retrotransposon Tf1 integration is targeted to 5′ ends of open reading frames. Nucleic Acids Res. 28: 4709-4716.
9. Boeke, J.D. and Devine, S.E. 1998. Yeast retrotransposons: Finding a nice quiet neighborhood. Cell 93: 1087-1089.
10. Bosher, J.M. and Labouesse, M. 2000. RNA interference: Genetic wand and genetic watchdog. Nat. Cell Biol. 2: E31-E36. doi: 10.1038/35000102.
11. Bowen, N.J., Jordan, I.K., Epstein, J.A., Wood, V., and Levin, H.L. 2003. Retrotransposons and their recognition of pol II promoters: A comprehensive survey of the transposable elements from the complete genome sequence of Schizosaccharomyces pombe. Genome Res. 13: 1984-1997.
12. Brehm, A., Tufteland, K.R., Aasland, R., and Becker, P.B. 2004. The many colours of chromodomains. BioEssays 26: 133-140.
13. Bushman, F.D. 2003. Targeting survival: Integration site selection by retroviruses and LTR-retrotransposons. Cell 115: 135-138.
14. Cheng, Z., Dong, F., Langdon, T., Ouyang, S., Buell, C.R., Gu, M., Blattner, F.R., and Jiang, J. 2002. Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14: 1691-1704.
15. Ciuffi, A., Llano, M., Poeschla, E., Hoffmann, C., Leipzig, J., Shinn, P., Ecker, J.R., and Bushman, F. 2005. A role for LEDGF/p75 in targeting HIV DNA integration. Nat. Med. 11: 1287-1289.
16. Cuff, J.A., Clamp, M.E., Siddiqui, A.S., Finlay, M., and Barton, G.J. 1998. JPred: A consensus secondary structure prediction server. Bioinformatics 14: 892-893.
17. Dean, R.A., Talbot, N.J., Ebbole, D.J., Farman, M.L., Mitchell, T.K., Orbach, M.J., Thon, M., Kulkarni, R., Xu, J.R., Pan, H., et al. 2005. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434: 980-986.
18. Derse, D., Crise, B., Li, Y., Princler, G., Lum, N., Stewart, C., McGrath, C.F., Hughes, S.H., Munroe, D.J., and Wu, X. 2007. Human T-cell leukemia virus type 1 integration target sites in the human genome: Comparison with those of other retroviruses. J. Virol. 81: 6731-6741.
19. Dillon, P.J. and Rosen, C.A. 1990. A rapid method for the construction of synthetic genes using the polymerase chain reaction. Biotechniques 9: 298-300.
20. Dong, F., Miller, J.T., Jackson, S.A., Wang, G.L., Ronald, P.C., and Jiang, J. 1998. Rice (Oryza sativa) centromeric regions consist of complex DNA. Proc. Natl. Acad. Sci. 95: 8135-8140.
21. Fischle, W., Wang, Y., Jacobs, S.A., Kim, Y., Allis, C.D., and Khorasanizadeh, S. 2003. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes & Dev. 17: 1870-1881.
22. Flanagan, J.F., Mi, L.Z., Chruszcz, M., Cymborowski, M., Clines, K.L., Kim, Y., Minor, W., Rastinejad, F., and Khorasanizadeh, S. 2005. Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438: 1181-1185.
23. Fransz, P., De Jong, J.H., Lysak, M., Castiglione, M.R., and Schubert, I. 2002. Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. Proc. Natl. Acad. Sci. 99: 14584-14589.
24. Freitag, M., Hickey, P.C., Khlafallah, T.K., Read, N.D., and Selker, E.U. 2004. HP1 is essential for DNA methylation in neurospora. Mol. Cell 13: 427-434.
25. Gai, X. and Voytas, D.F. 1998. A single amino acid change in the yeast retrotransposon Ty5 abolishes targeting to silent chromatin. Mol. Cell 1: 1051-1055.
26. Gaudin, V., Libault, M., Pouteau, S., Juul, T., Zhao, G., Lefebvre, D., and Grandjean, O. 2001. Mutations in LIKE HETEROCHROMATIN PROTEIN 1 affect flowering time and plant architecture in Arabidopsis. Development 128: 4847-4858.
27. Gendrel, A.V., Lippman, Z., Yordan, C., Colot, V., and Martienssen, R.A. 2002. Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297: 1871-1873.
28. Girard, A., Sachidanandam, R., Hannon, G.J., and Carmell, M.A. 2006. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442: 199-202.
29. Gorinsek, B., Gubensek, F., and Kordis, D. 2004. Evolutionary genomics of chromoviruses in eukaryotes. Mol. Biol. Evol. 21: 781-798.
30. Gorinsek, B., Gubensek, F., and Kordis, D. 2005. Phylogenomic analysis of chromoviruses. Cytogenet. Genome Res. 110: 543-552.
31. Grewal, S.I. and Elgin, S.C. 2007. Transcription and RNA interference in the formation of heterochromatin. Nature 447: 399-406.
32. Grewal, S.I. and Jia, S. 2007. Heterochromatin revisited. Nat. Rev. Genet. 8: 35-46.
33. Grewal, S.I. and Rice, J.C. 2004. Regulation of heterochromatin by histone methylation and small RNAs. Curr. Opin. Cell Biol. 16: 230-238.
34. Grivna, S.T., Beyret, E., Wang, Z., and Lin, H. 2006. A novel class of small RNAs in mouse spermatogenic cells. Genes & Dev. 20: 1709-1714.
35. Hall, A.E., Kettler, G.C., and Preuss, D. 2006. Dynamic evolution at pericentromeres. Genome Res. 16: 355-364.
36. Havecker, E.R., Gao, X., and Voytas, D.F. 2005. The Sireviruses, a plant-specific lineage of the Ty1/copia retrotransposons, interact with a family of proteins related to dynein light chain 8. Plant Physiol. 139: 857-868.
37. Hiragami, K. and Festenstein, R. 2005. Heterochromatin protein 1: A pervasive controlling influence. Cell. Mol. Life Sci. 62: 2711-2726.
38. Hizi, A. and Levin, H.L. 2005. The integrase of the long terminal repeat-retrotransposon tf1 has a chromodomain that modulates integrase activities. J. Biol. Chem. 280: 39086-39094.
39. Hoff, E.F., Levin, H.L., and Boeke, J.D. 1998. Schizosaccharomyces pombe retrotransposon Tf2 mobilizes primarily through homologous cDNA recombination. Mol. Cell. Biol. 18: 6839-6852.
40. Houben, A., Demidov, D., Gernand, D., Meister, A., Leach, C.R., and Schubert, I. 2003. Methylation of histone H3 in euchromatin of plant chromosomes depends on basic nuclear DNA content. Plant J. 33: 967-973.
41. Huyen, Y., Zgheib, O., Ditullio Jr., R.A., Gorgoulis, V.G., Zacharatos, P., Petty, T.J., Sheston, E.A., Mellert, H.S., Stavridi, E.S., and Halazonetis, T.D. 2004. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432: 406-411.
42. Jacobs, S.A. and Khorasanizadeh, S. 2002. Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295: 2080-2083.
43. Jacobs, S.A., Taverna, S.D., Zhang, Y., Briggs, S.D., Li, J., Eissenberg, J.C., Allis, C.D., and Khorasanizadeh, S. 2001. Specificity of the HP1 chromo domain for the methylated N-terminus of histone H3. EMBO J. 20: 5232-5241.
44. Jiang, J., Nasuda, S., Dong, F., Scherrer, C.W., Woo, S.S., Wing, R.A., Gill, B.S., and Ward, D.C. 1996. A conserved repetitive DNA element located in the centromeres of cereal chromosomes. Proc. Natl. Acad. Sci. 93: 14210-14213.
45. Jiang, J., Birchler, J.A., Parrott, W.A., and Dawe, R.K. 2003. A molecular view of plant centromeres. Trends Plant Sci. 8: 570-575.
46. Jukes, T.H. and Cantor, C. 1969. Evolution of protein molecules. In Mammalian protein metabolism (ed. H.N. Munro), pp. 21-132. Academic Press, New York.
47. Kalderon, D., Roberts, B.L., Richardson, W.D., and Smith, A.E. 1984. A short amino acid sequence able to specify nuclear location. Cell 39: 499-509.
48. Ke, N., Irwin, P.A., and Voytas, D.F. 1997. The pheromone response pathway activates transcription of Ty5 retrotransposons located within silent chromatin of Saccharomyces cerevisiae. EMBO J. 16: 6272-6280.
49. Koonin, E.V., Zhou, S., and Lucchesi, J.C. 1995. The chromo superfamily: New members, duplication of the chromo domain and possible role in delivering transcription regulators to chromatin. Nucleic Acids Res. 23: 4229-4233.
50. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K., and Jenuwein, T. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116-120.
51. Le, Q.H., Melayah, D., Bonnivard, E., Petit, M., and Grandbastien, M.A. 2007. Distribution dynamics of the Tnt1 retrotransposon in tobacco. Mol. Genet. Genomics 278: 639-651.
52. Levin, H.L. 1995. A novel mechanism of self-primed reverse transcription defines a new family of retroelements. Mol. Cell. Biol. 15: 3310-3317.
53. Levin, H.L., Weaver, D.C., and Boeke, J.D. 1993. Novel gene expression mechanism in a fission yeast retroelement: Tf1 proteins are derived from a single primary translation product. EMBO J. 12: 4885-4895.
54. Lewinski, M.K., Yamashita, M., Emerman, M., Ciuffi, A., Marshall, H., Crawford, G., Collins, F., Shinn, P., Leipzig, J., Hannenhalli, S., et al. 2006. Retroviral DNA integration: viral and cellular determinants of target-site selection. PLoS Pathog 2: e60. doi: 10.1371/journal.ppat.0020060.
55. Lippman, Z. and Martienssen, R. 2004. The role of RNA interference in heterochromatic silencing. Nature 431: 364-370.
56. Llano, M., Saenz, D.T., Meehan, A., Wongthida, P., Peretz, M., Walker, W.H., Teo, W., and Poeschla, E.M. 2006. An essential role for LEDGF/p75 in HIV integration. Science 314: 461-464.
57. Malik, H.S. and Eickbush, T.H. 1999. Modular evolution of the integrase domain in the Ty3/Gypsy class of LTR retrotransposons. J. Virol. 73: 5186-5190.
58. Marin, I. and Llorens, C. 2000. Ty3/Gypsy retrotransposons: Description of new Arabidopsis thaliana elements and evolutionary perspectives derived from comparative genomic data. Mol. Biol. Evol. 17: 1040-1049.
59. Martienssen, R., Lippman, Z., May, B., Ronemus, M., and Vaughn, M. 2004. Transposons, tandem repeats, and the silencing of imprinted genes. Cold Spring Harb. Symp. Quant. Biol. 69: 371-379.
60. Maundrell, K. 1993. Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 123: 127-130.
61. Miller, J.T., Dong, F., Jackson, S.A., Song, J., and Jiang, J. 1998. Retrotransposon-related DNA sequences in the centromeres of grass chromosomes. Genetics 150: 1615-1623.
62. Min, J., Zhang, Y., and Xu, R.M. 2003. Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes & Dev. 17: 1823-1828.
63. Miyao, A., Tanaka, K., Murata, K., Sawaki, H., Takeda, S., Abe, K., Shinozuka, Y., Onosato, K., and Hirochika, H. 2003. Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell 15: 1771-1780.
64. Moreno, S., Klar, A., and Nurse, P. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194: 795-823.
65. Mou, Z., Kenny, A.E., and Curcio, M.J. 2006. Hos2 and Set3 promote integration of Ty1 retrotransposons at tRNA genes in Saccharomyces cerevisiae. Genetics 172: 2157-2167.
66. Nagaki, K., Cheng, Z., Ouyang, S., Talbert, P.B., Kim, M., Jones, K.M., Henikoff, S., Buell, C.R., and Jiang, J. 2004. Sequencing of a rice centromere uncovers active genes. Nat. Genet. 36: 138-145.
67. Nakagawa, H., Lee, J.K., Hurwitz, J., Allshire, R.C., Nakayama, J., Grewal, S.I., Tanaka, K., and Murakami, Y. 2002. Fission yeast CENP-B homologs nucleate centromeric heterochromatin by promoting heterochromatin-specific histone tail modifications. Genes & Dev. 16: 1766-1778.
68. Nakayama, J., Rice, J.C., Strahl, B.D., Allis, C.D., and Grewal, S.I. 2001. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292: 110-113.
69. Nakayashiki, H., Kiyotomi, K., Tosa, Y., and Mayama, S. 1999. Transposition of the retrotransposon MAGGY in heterologous species of filamentous fungi. Genetics 153: 693-703.
70. Nielsen, P.R., Nietlispach, D., Mott, H.R., Callaghan, J., Bannister, A., Kouzarides, T., Murzin, A.G., Murzina, N.V., and Laue, E.D. 2002. Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9. Nature 416: 103-107.
71. Noma, K., Sugiyama, T., Cam, H., Verdel, A., Zofall, M., Jia, S., Moazed, D., and Grewal, S.I. 2004. RITS acts in cis to promote RNA interference- mediated transcriptional and post-transcriptional silencing. Nat. Genet. 36: 1174-1180.
72. Ochman, H., Gerber, A.S., and Hartl, D.L. 1988. Genetic applications of an inverse polymerase chain reaction. Genetics 120: 621-623.
73. Pereira, V. 2004. Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome. Genome Biol. 5: R79. doi: 10.1186/gb-2004-5-10-r79.
74. Peters, A.H., O'Carroll, D., Scherthan, H., Mechtler, K., Sauer, S., Schofer, C., Weipoltshammer, K., Pagani, M., Lachner, M., Kohlmaier, A., et al. 2001. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107: 323-337.
75. Peterson-Burch, B.D., Nettleton, D., and Voytas, D.F. 2004. Genomic neighborhoods for Arabidopsis retrotransposons: A role for targeted integration in the distribution of the Metaviridae. Genome Biol. 5: R78. doi: 10.1186/gb-2004-5-10-r78.
76. Sadaie, M., Iida, T., Urano, T., and Nakayama, J. 2004. A chromodomain protein, Chp1, is required for the establishment of heterochromatin in fission yeast. EMBO J. 23: 3825-3835.
77. SanMiguel, P., Tikhonov, A., Jin, Y.K., Motchoulskaia, N., Zakharov, D., Melake-Berhan, A., Springer, P.S., Edwards, K.J., Lee, M., Avramova, Z., et al. 1996. Nested retrotransposons in the intergenic regions of the maize genome. Science 274: 765-768.
78. Sasaki, T., Matsumoto, T., Yamamoto, K., Sakata, K., Baba, T., Katayose, Y., Wu, J., Niimura, Y., Cheng, Z., Nagamura, Y., et al. 2002. The genome sequence and structure of rice chromosome 1. Nature 420: 312-316.
79. Schroder, A., Shinn, P., Chen, H., Berry, C., Ecker, J., and Bushman, F. 2002. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110: 521-529.
80. Shun, M.C., Raghavendra, N.K., Vandegraaff, N., Daigle, J.E., Hughes, S., Kellam, P., Cherepanov, P., and Engelman, A. 2007. LEDGF/p75 functions downstream from preintegration complex formation to effect gene-specific HIV-1 integration. Genes & Dev. 21: 1767-1778.
81. Sijen, T. and Plasterk, R.H. 2003. Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature 426: 310-314.
82. Singleton, T.L. and Levin, H.L. 2002. A long terminal repeat retrotransposon of fission yeast has strong preferences for specific sites of insertion. Eukaryot. Cell 1: 44-55.
83. Slotkin, R.K. and Martienssen, R. 2007. Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet. 8: 272-285.
84. Tamaru, H. and Selker, E.U. 2001. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414: 277-283.
85. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. 1997. The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
86. Thon, M.R., Martin, S.L., Goff, S., Wing, R.A., and Dean, R.A. 2004. BAC end sequences and a physical map reveal transposable element content and clustering patterns in the genome of Magnaporthe grisea. Fungal Genet. Biol. 41: 657-666.
87. Turck, F., Roudier, F., Farrona, S., Martin-Magniette, M.L., Guillaume, E., Buisine, N., Gagnot, S., Martienssen, R.A., Coupland, G., and Colot, V. 2007. Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet. 3: e86. doi: 10.1371/journal.pgen.0030086.
88. Vagin, V.V., Sigova, A., Li, C., Seitz, H., Gvozdev, V., and Zamore, P.D. 2006. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313: 320-324.
89. Vastenhouw, N.L. and Plasterk, R.H. 2004. RNAi protects the Caenorhabditis elegans germline against transposition. Trends Genet. 20: 314-319.
90. Wang, G.P., Ciuffi, A., Leipzig, J., Berry, C.C., and Bushman, F.D. 2007. HIV integration site selection: Analysis by massively parallel pyrosequencing reveals association with epigenetic modifications. Genome Res. 17: 1186-1194.
91. Wood, V., Gwilliam, R., Rajandream, M.A., Lyne, M., Lyne, R., Stewart, A., Sgouros, J., Peat, N., Hayles, J., Baker, S., et al. 2002. The genome sequence of Schizosaccharomyces pombe. Nature 415: 871-880.
92. Wu, X., Li, Y., Crise, B., and Burgess, S.M. 2003. Transcription start regions in the human genome are favored targets for MLV integration. Science 300: 1749-1751.
93. Xie, W., Gai, X., Zhu, Y., Zappulla, D.C., Sternglanz, R., and Voytas, D.F. 2001. Targeting of the yeast Ty5 retrotransposon to silent chromatin is mediated by interactions between integrase and Sir4p. Mol. Cell. Biol. 21: 6606-6614.
94. Yieh, L., Kassavetis, G., Geiduschek, E.P., and Sandmeyer, S.B. 2000. The Brf and TATA-binding protein subunits of the RNA polymerase III transcription factor IIIB mediate position-specific integration of the gypsy-like element, Ty3. J. Biol. Chem. 275: 29800-29807.
95. Yieh, L., Hatzis, H., Kassavetis, G., and Sandmeyer, S.B. 2002. Mutational analysis of the transcription factor IIIB-DNA target of Ty3 retroelement integration. J. Biol. Chem. 277: 25920-25928.
96. Yuan, Q., Ouyang, S., Wang, A., Zhu, W., Maiti, R., Lin, H., Hamilton, J., Haas, B., Sultana, R., Cheung, F., et al. 2005. The institute for genomic research Osa1 rice genome annotation database. Plant Physiol. 138: 18-26.
97. Zemach, A., Li, Y., Ben-Meir, H., Oliva, M., Mosquna, A., Kiss, V., Avivi, Y., Ohad, N., and Grafi, G. 2006. Different domains control the localization and mobility of LIKE HETEROCHROMATIN PROTEIN1 in Arabidopsis nuclei. Plant Cell 18: 133-145.
98. Zhang, X., Germann, S., Blus, B.J., Khorasanizadeh, S., Gaudin, V., and Jacobsen, S.E. 2007. The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat. Struct. Mol. Biol. 14: 869-871.
99. Zou, S., Ke, N., Kim, J.M., and Voytas, D.F. 1996. The Saccharomyces retrotransposon Ty5 integrates preferentially into regions of silent chromatin at the telomeres and mating loci. Genes & Dev. 10: 634-645.