Genetic and epigenetic aspects of somaclonal variation: Flower colour bud sports in azalea, a case study

South African Journal of Botany

Volumn 69, Issue 2, 2003, Pages 117-128

  De Schepper, S ^a   Debergh, P ^a   Van Bockstaele, E ^a   De Loose, M ^b   Gerats, A ^c   Depicker, A ^a  

^a GHENT UNIVERSITY   (Belgium)

^b Centrum voor Landbouwkundig Onderzoek Gent CLO / Centre de Recherches Agronomiques Gand   (Belgium)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

HORTICULTURE; SPORT; VEGETATIVE REPRODUCTION;

EMBRYOPHYTA; EUKARYOTA;

EID: 0042286635     PISSN: 02546299     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0254-6299(15)30333-1     Document Type: Review

References (148)

1. Akhtar A, Zink D, Decker PB (2000) Chromodomain proteins are protein-RNA interaction modules. Nature 407: 405-409
2. Allshire R (2002) RNAi and heterochromatin - a hushed-up affair. Science 297: 1818-1818
3. Atkinson PW, Warren WD, O'Brochta DA (1993) The hobo transposable element of Drosophila can be cross-mobilized in house-flies and excises like the Ac element of maize. Proceedings of the National Academy of Sciences USA 90: 9693-9697
4. Attwood JT, Yung RL, Richardson BC (2002) DNA methylation and the regulation of gene transcription. Cellular and Molecular Life Sciences 59: 241-257
5. Bartee L, Bender J (2001) Two Arabidopsis methylation-deficiency mutations confer only partial effects on a methylated endogenous gene family. Nucleic Acids Research 29: 2127-2134
6. Bass BL (2000) Double-stranded RNA as a template for gene silencing. Cell 101: 235-238
7. Bauer H (1993) Identification of 'flower-sports' of pelargoniums and roses by phenolic compounds. Gartenbauwissenschaft 58: 82-89
8. Bennetzen JL, Schrick K, Springer PS, Brown WE, SanMiguel P (1994) Active maize genes are unmodified and flanked by diverse classes of modified, highly repetitive DNA. Genome 37: 565-576
9. Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363-366
10. Bino RJ, Bianchi F, Wijsman HJW (1984) Periclinal chimerism in Petunia demonstrated by regeneration of plants from the mutated epidermal layer. Heredity 52: 437-441
11. Bird AP (1995) Gene number, noise reduction and biological complexity. Trends in Genetics 11: 94-100
12. Bollmann J, Carpenter R, Coen ES (1991) Allelic interactions at the nivea locus of Antirrhinum. The Plant Cell 3: 1327-1336
13. Capy P, Vitalis R, Lagin T, Higuet D, Bazin C (1996) Relationships between transposable elements based upon the integrase-transposase domains: is there a common ancestor? Journal of Molecular Evolution 42: 359-368
14. Carpenter R, Coen ES (1995) Transposon induced chimeras show that floricaula, a meristem identity gene, acts non-autonomously between cell layers. Development 121: 19-26
15. Carthew (2001) Gene silencing by double-stranded RNA. Current Opinion in Cell Biology 13: 244-248
16. Chamberlain DF, Rae SJ (1990) A revision of Rhododendron IV sub-genus Tsutsusi. Edinburgh Journal of Botany 47: 89-200
17. Chen RZ, Pettersson U, Beard C, Jackson-Grusby L, Jaenisch R (1998) DNA hypomethylation leads to elevated mutation rates. Nature 395: 89-93
18. Chen ZJ, Pikaard CS (1997) Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. Genes and Development 11: 2124-2136
19. Coccilione SM, Cone KC (1993) PI-Bh, an anthocyanin regulatory gene of maize that leads to variegated pigmentation. Genetics 135: 575-588
20. Coen ES, Almeida J, Robbins TP, Hudson A, Carpenter R (1988) Molecular analysis of genes determining spatial patterns in Antirrhinum majus. In: Verma DPS, Goldberg RB (eds) Temporal and Spatial Regulation of Plant Genes. Springer-Verlag, Wien, pp 63-78
21. Coen ES, Carpenter R, Martin C (1986) Transposable elements generate novel patterns of gene expression in Antirrhinum majus. Cell 47: 285-296
22. Cogoni C, Macino G (2000) Post-transcriptional gene silencing across kingdoms. Current Opinion in Genetics and Development 10: 638-643
23. Colot V, Rossignol JL (1999) Eukaryotic DNA methylation as an evolutionary device. BioEssays 21: 402-411
24. Cullen J (1991) The logic of Rhododendron classification. Royal Horticultural Society London 44: 14-19
25. Dalmay T, Hamilton A, Meuller E, Baulcombe DC (2000) Potato virus X amplicons in Arabidopsis mediate genetic and epigenetic gene silencing. Plant Cell 12: 369-379
26. Dalmay T, Horsefield R, Braunstein TH, Baulcombe DC (2001) SDE3 encodes an RNA helicase required for posttranscriptional gene silencing in Arabidopsis. EMBO Journal 20: 2069-2078
27. De Cooman L, Everaert ESW, Fache P, Van de Casteele K, Van Sumere CF (1993) Flavonoid biosynthesis in petals of Rhododendron simsii. Phytochemistry 33: 1419-1426
28. De Keukeleire P (2000) Transposable Elements in Petunia hybrida. PhD Thesis, Ghent University, Belgium, 135pp
29. De Loose R (1969) The flower pigments of the Belgian hybrids of Rhododendron simsii and other species and varieties from Rhododendron subseries obtusum. Phytochemistry 8: 253-259
30. De Loose R (1979) Characterisation of Rhododendron simsii Planch. cultivars by flavonoid and isozyme markers. Scientia Horticulturae 11: 175-182
31. De Picker A, Van Montagu M (1997) Post-transcriptional gene silencing in plants. Current Opinion in Cell Biology 9: 373-382
32. De Riek J, Dendauw J, Mertens M, De Loose M, Heursel J, Van Bockstaele E (1999) Validation of criteria for the selection of AFLP markers to assess the genetic variation of a breeders' collection of evergreen azaleas. Theoretical and Applied Genetics 99: 1155-1165
33. De Schepper S (2001) Molecular Analysis of the Induction of Sports in Azalea (Rhododendron simsii hybrids). PhD Thesis, Ghent University, Belgium, 173pp
34. De Schepper S, Debergh P, Van Bockstaele E, De Loose M (2001a) Molecular analysis of sport induction in azalea (Rhododendron simsii hybrids). Acta Horticulturae 552: 143-149
35. De Schepper S, Leus L, Mertens M, Debergh P, Van Bockstaele E, De Loose M (2001b) Somatic polyploidy and its consequences for flower coloration and flower morphology in azalea. Plant Cell Reports 20: 583-590
36. De Schepper S, Leus L, Mertens M, Heursel J, Debergh P, Van Bockstaele E, De Loose M (2001c) Flow cytometric analysis of ploidy in Rhododendron subgenus Tsutsusi. HortScience 36: 125-127
37. De Vries H (1905) Species and Varieties: Their Origin by Mutation. Open Court Publishing, Chicago
38. Diégeuz MJ, Bellotto M, Afsar K, Mittelsten-Scheid O, Paszkowski J (1997) Methylation of cytosines in nonconventional methylation acceptor sites can contribute to reduced gene expression. Molecular Genetics and Genomics 253: 581-588
39. Dobosy JR, Selker EU (2001) Emerging connections between DNA methylation and histone acetylation. Cellular and Molecular Life Sciences 58: 721-727
40. Doerfler W (1983) DNA methylation and gene activity. Annual Reviews in Biochemistry 52: 93-124
41. Doodeman M, Bianchi F (1985) Genetic analysis of the instability in Petunia hybrids. 3. Periclinal chimeras resulting from frequent mutations of unstable alleles. Theoretical and Applied Genetics 69: 297-304
42. Dudley NR, Labbé JC, Goldstein B (2002) Using RNA interference to identify genes required for RNA interference. Proceedings National Academy of Sciences USA 99: 4191-4196
43. Fagard M, Boutet S, Morel JB, Bellini C, Vaucheret H (2000) AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proceedings National Academy of Sciences USA 97: 11650-11654
44. Finnegan EJ, Genger RK, Peacock WJ, Dennis ES (1998) DNA methylation in plants. Annual Review of Plant Physiology and Plant Molecular Biology 49: 223-247
45. Finnegan EJ, Peacock WJ, Dennis ES (1996) Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proceedings of the National Academy of Sciences USA 93: 8449-8454
46. Finnegan EJ, Peacock WJ, Dennis ES (2000) DNA methylation a key regulator of plant development and other processes. Current Opinion in Genetics and Development 10: 217-223
47. Fire A (1999) RNA-triggered gene silencing. Trends in Genetics 15: 358-363
48. Flavell RB (1994) Inactivation of gene expression in plants as a consequence of specific sequence duplication. Proceedings of the National Academy of Sciences USA 91: 3490-3496
49. Galitski T, Saldanha AJ, Style, CA, Lander ES, Fink GR (1999) Ploidy regulation of gene expression. Science 28: 251-254
50. Gastony GJ (1991) Gene silencing in a polyploid homosporous fern: paleopolyploidy revised. Proceedings of the National Academy of Sciences USA 88: 1602-1605
51. Gendrel AV, Lippman Z, Yordan C, Colot V, Martienssen RA (2002) Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297: 1871-1873
52. Gibbons RJ, McDowell TL, Raman S, O'Rourke DM, Garrick D, Ayyub H, Higgs DR (2000) Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nature Genetics 24: 368-371
53. Grunewaldt J, Duneman F (1991) Variation and selection in vitro. Gartenbauwissenschaft 56: 1-5
54. Habu Y, Kakutani T, Paszkowski J (2001) Epigenetic developmental mechanisms in plants: molecules and targets of plant epigenetic regulation. Current Opinion in Genetics and Development 11: 215-220
55. Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286: 950-952
56. Hammond SM, Bernstein E, Beach D, Hannon GJ (2000)An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404:293-296
57. Hammond SM, Boettcher S, Caudy AA, Kobayashi R, Hannon GJ (2001) Argonaute2, a link between genetic and biochemical analyses of RNAi. Nature 293: 1146-1150
58. Henikoff S, Comai L (1998) A DNA methyltransferase homologue with a chromodomain exists in multiple polymorphic forms in Arabidopsis. Genetics 149: 307-318
59. Heursel J (1999) Azalea's Oorsprong, Veredeling en Cultivars. Lannoo-Terra, Tielt, Belgium, 194pp
60. Heursel J, Horn W (1977) A hypothesis on the inheritance of flower colours and flavonoids in Rhododendron simsii Planch. Zeitschrift für Pflanzenzücht 79: 238-249
61. Holliday R (1990) Mechanisms for the control of gene activity during development. Biological Reviews 65: 431-471
62. Horn W (1968) Genetische Ursachen der Variation bei Zierpflanzen. Gartenbauwissenschaft 33: 317-333
63. Imai Y (1934) On the mutable genes Pharbitis, with special reference to their bearing on the mechanism of bud-variation. Journal of the College of Agriculture Imperial University Tokyo 12: 479-523
64. Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556-560
65. Jacobsen SE (1999) Gene silencing: maintaining methylation patterns. Current Biology 9: 617-619
66. Jacobsen SE, Meyerowitz EM (1997) Hypermethylated Superman epigenetic alleles in Arabidopsis. Science 277: 1100-1103
67. Jaligot E, Rival A, Beulé T, Dussert S, Verdeil JL (2000) Somaclonal variation in oil palm (Elaeis guineensis Jacq.): the DNA methylation hypothesis. Plant Cell Reports 19: 684-690
68. mCCG methylation in angiosperms. Plant Journal 9: 579-586
69. Jeddeloh JA, Stokes TL, Richards EJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nature Genetics 22: 94-97
70. Jenuwein T (2002) An RNA-guided pathway for the epigenome. Science 297: 2215-2218
71. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293: 1074-1080
72. Jones L, Hamilton AJ, Voinnet O, Thomas CL, Maule AJ, Baulcombe DC (1999) RNA-DNA interactions and DNA methylation in post-transcriptional gene silencing. The Plant Cell 11: 2291-2301
73. Jorgensen RA (1995) Cosuppression, flower colour patterns and metastable gene expression states. Science 268: 686-691
74. Jorgensen RA, Cluster PD, English J, Que Q, Napoli CA (1996) Chalcone synthase cosuppression phenotypes in petunia flowers: comparison of sense vs. antisense constructs and single copy vs. complex T-DNA sequences. Plant Molecular Biology 31: 957-973
75. Jost JP, Saluz HP (eds) (1993) DNA Methylation: Molecular Biology and Biological Significance, Birkhäuser Verlag, Basel, 572pp
76. Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Molecular Biology 43: 179-188
77. Kaeppler SM, Phillips RL, Olhoft P (1998) Molecular basis of heritable tissue culture-induced variation in plants. In: Jain SM, Brar DS Ahloowalia BS (eds) Somaclonal Variation and Induced Mutations in Crop Improvement. Kluwer Academic Publishers, Dordrecht, pp 465-484
78. Kakutani T, Munakata K, Richards EJ, Hirochika H (1999) Meiotically and mitotically stable inheritance of DNA hypomethylation induced by ddm1 mutation of Arabidopsis thaliana. Genetics 151: 831-838
79. Kempken F, Windhofer F (2001) The hAT family: a versatile transposon group common to plants, fungi, animals and man. Chromosoma Focus 110: 1-9
80. Ketting RF, Haverkamp TH, Van Luenen HG, Plasterk RH (1999) mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RnaseD. Cell 99: 133-141
81. Lister C, Jackson D, Martin C (1993) Transposon-induced inversion in Anthirrinum modifies nivea gene expression to give a novel flower color pattern under the control of Cyclodea radialis. The Plant Cell 5: 1541-1553
82. Luff B, Paszkowski J, Bender J (1999) An inverted repeat triggers cytosine methylation of identical sequences in Arabidopsis. Molecular Cell 3: 505-511
83. Marcotrigiano M (1997) Chimeras and variegation: patterns of deceit. HortScience 32: 773-784
84. Marcotrigiano M, Stewart RN (1984) All variegated plants are not chimeras. Science 23: 505
85. Martienssen RA (1996) Epigenetic phenomena: paramutation and gene silencing in plants. Current Biology 6: 810-813
86. Martienssen RA (1998) Transposons, DNA methylation and gene control. Trends in Genetics 14: 12-13
87. Martienssen RA, Colot V (2001) DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293: 1070-1074
88. Martin C, Gerats AGM (1993) Control of pigment biosynthesis genes during petal development. The Plant Cell 5: 1253-1264
89. Matzke MA, Matzke AJM, Eggleston W (1996) Trans-gene silencing and paramutation: a common response to invasive DNA? Trends in Plant Sciences 1: 382-388
90. Matzke MA, Matzke AJM, Pruss G, Vance VB (2001) RNA-based silencing in plants. Current Opinion in Genetics and Development 11: 221-227
91. Matzke MA, Mette MF, Matzke AJM (2000) Transgenic silencing by the host genome defense: implications for the evolution of epigenetic control mechanisms in plants and vertebrates. Plant Molecular Biology 43: 401-415
92. Matzke MA, Mittelsten-Scheid O, Matzke AJM (1999) Rapid structural and epigenetic changes in polyploid and aneuploid genomes. BioEssays 21: 761-767
93. May BP, Dellaporta SL (1998) Transposon sequences drive tissue-specific expression of the maize regulatory gene R-s. Plant Journal 13: 241-247
94. McClintock B (1947) Cytogenetic studies of maize and Neurospora. Carnegie Institute Washington Yearbook 46: 146-152
95. Melquist S, Luff B Bender J (1999) Arabidopsis PAI gene rearrangements, cytosine methylation and expression. Genetics 153: 401-413
96. Mertens M, Werbrouck S, Samyn G, Botelho dos Santhos Moreira de Silva H, Debergh P (1996) In vitro regeneration of evergreen azalea from leaves. Plant Cell Tissue Organ Culture 45: 231-236
97. Mette MF, Aufsatz W, Van der Winden J, Matzke MA, Marzke AJ (2000) Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO Journal 19: 5194-5201
98. Meyer P (2001) Chromatin remodelling. Current Opinion in Plant Biology 4: 457-462
99. Mittelsten-Scheid O, Jakovleva L, Afsar K, Maluszynska J, Paszkowski J (1996) A change of ploidy can modify epigenetic silencing. Proceedings of the National Academy of Sciences USA 93: 7114-7119
100. Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411: 212-214
101. Mol JNM, Schram AW, De Vlaming P, Gerats AGM, Kreuzaler F, Hahlbrock K, Reif HJ, Veltkamp E (1983) Regulation of flavonoid gene expression in Petunia hybrida: description and partial characterisation of a conditional mutant in chalcone synthase gene expression. Molecular Genomics and Genetics 129: 424-429
102. Morel JB, Mourrain P, Béclin C, Vaucheret H (2000) DNA methylation and chromatin structure affect transcriptional and post-transcriptional transgene silencing in Arabidopsis. Current Biology 10: 1591-1594
103. Mourrain P, Béclin C, Elmayan T, Feuerbach F, Godon C, Morel JB, Jouette D, Lacombe AM, Nikic S, Picault N, Remoue K, Sanial M, Vo TA, Vaucheret H (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101: 533-542
104. Muskens MWM, Vissers APA, Mol JNM, Kooter JM (2000) Role of inverted DNA repeats in transcriptional and post-transcriptional gene silencing. Plant Molecular Biology 43: 243-260
105. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SIS (2001) Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292: 110-113
106. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird AP (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393: 386-389
107. Napoli CA, Lemieux C, Jorgensen RA (1990) Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. The Plant Cell 2: 279-289
108. Nevers P, Shepherd NS, Saedler H (1986) Plant transposable elements. Advances in Botanical Research 12: 103-203
109. Ng H, Bird AP (1999) DNA methylation and chromatin configuration. Current Opinion in Genetics and Development 9: 158-163
110. Noma K, Allis CD, Grewal SIS (2001) Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293: 1150-1155
111. Nykänen A, Haley B, Zamore PD (2001) ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 107: 309-321
112. Paszkowski J, Whitham SA (2001) Gene silencing and DNA methylation processes. Current Opinion in Plant Biology 4: 123-129
113. Patterson GI, Kubo KM, Shroyer T, Chandler VL (1995) Sequences required for paramutation of the maize b gene to a region containing the promoter and upstream sequences. Genetics 141: 1389-1406
114. Peterson CL, Workman JL (2000) Promoter targeting and chromatin remodelling by the SWI/SNF complex. Current Opinion in Genetics and Development 10: 187-192
115. Phillips RL, Kaeppler SM, Olhof P (1994) Genetic instability of plant tissue cultures: breakdown of normal controls. Proceedings of the National Academy of Sciences USA 91: 5222-5226
116. Plasterk RHA (2002) RNA silencing: The genome's immune system. Science 296: 1263-1269
117. Razin A, Riggs AD (1980) DNA methylation and gene function. Science 210: 604-610
118. Rea S, Eisenhaber F, O'Carroll N, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases Nature 406: 593-599
119. Rice JC, Allis CD (2001) Histone methylation versus histone acetylation: new insights into epigenetic regulation. Current Opinion in Cell Biology 13: 263-273
120. Richards EJ (1997) DNA methylation and plant development. Trends in Genetics 13: 319-322
121. Ronchi A, Petroni K, Tonelli C (1995) The reduced expression of endogenous duplications (REED) in the maize R gene family is mediated by DNA methylation. EMBO Journal 14: 5318-5328
122. Ronemus MJ, Galbiati M, Ticknor C, Chen J, Dellaporta SL (1996) Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273: 654-657
123. Rubin E, Lithwick G, Levy AA (2001) Structure and evolution of the hAT transposon superfamily. Genetics 158: 949-957
124. Samyn G, De Schepper S, Van Bockstaele E (2002) Regeneration of explants of several azalea (Rhododendron simsii) cultivars in view of the appearance of sports. Plant Cell Tissue Organ Culture 70: 223-227
125. Satina S, Blakeslee AF, Avery AG (1940) Demonstrations of the three germ layers in the shoot apex of Datura by means of induced polyploidy in periclinal chimeras. American Journal of Botany 27: 895-905
126. Schmitt F, Oakeley E, Jost JP (1997) Antibiotics induced genome wide hypermethylation in cultured Nicotiana tabacum plants. Journal Biological Chemistry 272: 1534-1540
127. Schwartz D, Dennis ES (1986) Transposase activity of the Ac controlling element in maize is regulated by its degree of methylation. Molecular Genomics and Genetics 205: 476-482
128. Selinger DA, Chandler VL (2001) B-Bolivia, an allele of the maize b1 gene with variable expression, contains a high copy retrotransposon-related sequence immediately upstream. Plant Physiology 125: 1363-1379
129. Sharp PA (2001) RNA interference. Genes and development 15: 485-490
130. Sudarsanam P, Winston F (2000) The SWI/SNF family of nucleosomes-remodelling complexes and transcriptional control. Trends in Genetics 16: 345-351
131. Tian L, Chen ZJ (2001) Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. Proceedings of the National Academy of Sciences USA 2: 200-205
132. Tilney-Bassett RA (1963) The structure of periclinal chimeras. Heredity 18: 265-285
133. Tilney-Bassett RA (1986) Plant Chimeras. Edward Arnold Publishers, London. 199pp
134. Urnov FD, Wolffe AP (2001) Above and within the genome: Epigenetics past and present. Journal Mammary Gland Biology Neoplasia 6: 153-167
135. Vaistij FE, Jones L, Baulcombe DC (2002) Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. The Plant Cell 14: 857-867
136. Vanderwiel P, Voytas DF, Wendel JF (1993) Copia-like retrotransposable element evolution in diploid and polyploid cotton (Gossypium L). Journal of Molecular Evolution 36: 429-447
137. Vaucheret H, Beclin C, Elmayan T, Feuerbach F, Godon C, Morel JB, Mourrain P, Palauqui JC, Vernhettes S (1998) Transgene-induced gene silencing in plants. Plant Journal 16: 651-659
138. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SIS, Martienssen RA (2002) Regulation of heterochromatic silencing and histone H3 Lysine-9 methylation by RNAi. Science 297: 1833-1837
139. Wade PA (2001) Methyl CpG binding proteins: coupling chromatin architecture to gene regulation. Oncogene 20: 3166-3173
140. Wassenegger M (2000) RNA-directed DNA methylation. Plant Molecular Biology 43: 203-220
141. Wessler SR (1998) Transposable elements associated with normal plant genes. Physiologia Plantarum 103: 581-586
142. Wiebauer K, Nedderman P, Hughes M, Jiricny J (1993) The repair of 5-methylcytosine-deamination damage. In: Jost JP, Saluz P (eds) DNA Methylation: Molecular Biology and Biological Significance, Birkhäuser Verlag, Basel, pp 510-568
143. Wolffe AP, Guschin D (2000) Review: chromatin structural features and targets that regulate transcription. Journal of Structural Biology 129: 102-122
144. Wolffe AP, Hayes JJ (1999) Chromatin disruption and modification. Nucleic Acids Research 27: 711-720
145. Wolffe AP, Matzke MA (1999) Epigenetics: regulation through repression. Science 286: 481-486
146. Wu-Scharf D, Jeong B, Zhang C, Cerutti H (2000) Transgene and transposon silencing in Chlamydomonas reinhardtii by a DEAH-Box RNA helicase. Science 290: 1159-1162
147. Yoder JA, Walsh CP, Bestor TH (1997) Cytosine methylation and the ecology of intragenomic parasites. Trends in Genetics 13: 335-340
148. Zamore PD (2002) Ancient pathways programmed by small RNAs. Science 296: 1265-1269