Plant Molecular Biology

, Volume 43, Issue 2–3, pp 121–145 | Cite as

Paramutation in maize

  • Vicki L. Chandler
  • William B. Eggleston
  • Jane E. Dorweiler


Paramutation is a heritable change in gene expression induced by allele interactions. This review summarizes key experiments on three maize loci, which undergo paramutation. Similarities and differences between the phenomenology at the three loci are described. In spite of many differences with respect to the stability of the reduced expression states at each locus or whether paramutation correlates with DNA methylation and repeated sequences within the loci, recent experiments are consistent with a common mechanism underlying paramutation at all three loci. Most strikingly, trans-acting mutants have been isolated that prevent paramutation at all three loci and lead to the activation of silenced Mutator transposable elements. Models consistent with the hypothesis that paramutation involves heritable changes in chromatin structure are presented. Several potential roles for paramutation are discussed. These include localizing recombination to low-copy sequences within the genome, establishing and maintaining chromatin domain boundaries, and providing a mechanism for plants to transmit an environmentally influenced expression state to progeny.

anthocyanins chromatin structure epigenetics gene silencing transcription 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Argon-Alcaide, L., Miller, T., Schwarzacher, T., Reader, S. and Moore, G. 1996. A cereal centromeric sequence. Chromosoma (Berlin) 105: 261–268.PubMedGoogle Scholar
  2. Axtell, J.D. and Brink, R.A. 1967. Chemically induced paramutation at the R locus in maize. Proc. Natl. Acad. Sci. USA 58: 181–187.PubMedGoogle Scholar
  3. Bennetzen, J.L., Schrick, K., Springer, P.S., Brown, W.E. and San-Miguel, P. 1994. Active maize genes are unmodified and flanked by diverse classes of modified, highly repetitive DNA. Genome 37: 565–576.PubMedGoogle Scholar
  4. Bray, R.A. and Brink, R.A. 1966. Mutation and paramutation at the R locus in maize. Genetics 54: 137–149.Google Scholar
  5. Brink, R.A. 1956. A genetic change associated with the R locus in maize which is directed and potentially reversible. Genetics 41: 872–889.Google Scholar
  6. Brink, R.A. 1958. Paramutation at the R locus in maize. Cold Spring Harbor Symp. Quant. Biol. 23: 379–391.PubMedGoogle Scholar
  7. Brink, R.A. 1973. Paramutation. Annu. Rev. Genet. 7: 129–152.PubMedGoogle Scholar
  8. Brink, R.A. and Mikula, B. 1958. Plant color effects of certain anomalous forms of the Rr allele in maize. Z. Ind. Abst. Vererb. 89: 94–102.Google Scholar
  9. Brink, R.A., Brown, D.F., Kermicle, J. and Weyers, W.H. 1960. Locus dependence of the paramutant R phenotype in maize. Genetics 45: 1297–1312.Google Scholar
  10. Brink, R.A., Kermicle, J.L. and Ziebur, N.K. 1970. Derepression in the female gametophyte in relation to paramutant R expression in maize endosperms, embryos and seedlings. Genetics 66: 87–96.Google Scholar
  11. Brink, R.A., Styles, E.C. and Axtell, J.D. 1968. Paramutation: directed genetic change. Science 159: 161–170.PubMedGoogle Scholar
  12. Brown, D.G. 1966. Paramutability of Rg and rr mutant genes derived from an Rr allele in maize. Genetics 54: 899–910.Google Scholar
  13. Brown, D.G. and Brink, R.A. 1960. Paramutagenic action of paramutant Rr and Rg alleles in maize. Genetics 45: 1313–1316.Google Scholar
  14. Brown, J. and Sundaresen, V. 1991. A recombination hotspot in the maize a1 intragenic region. Theor. Appl. Genet. 81: 185–188.Google Scholar
  15. Cavalli, G. and Paro, R. 1998. The Drosophila Fab-7 chromosomal element conveys epigenetic inheritance during mitosis and meiosis. Cell 93: 505–518.PubMedGoogle Scholar
  16. Chandler, V.L., Kubo, K. M. and Hollick, J. B. 1996. b and pl paramutation in maize: heritable transcription states programmed during development. In: V. Russo, R. Martienssen and A.D. Riggs (Eds.) Epigenetic Mechanisms of Gene Regulation, Cold Spring Harbor Press, Cold Spring Harbor, NY, pp. 289–304.Google Scholar
  17. Civardi, L., Xia, Y., Edward, K.J., Schnable, P.S. and Nikolau, B.J. 1994. The relationship between genetic and physical distances in the cloned a1–sh2 interval of the Zea mays L. genome. Proc. Natl. Acad. Sci. USA 91: 8268–8272.PubMedGoogle Scholar
  18. Cocciolone, S.M. and Cone, K.C. 1993. Pl-Bh, an anthocyanin regulatory gene of maize that leads to variegated pigmentation. Genetics 135: 575–588.PubMedGoogle Scholar
  19. Coe, E.H., Jr. 1959. A regular and continuing conversion-type phenomenon at the B locus in maize. Proc. Natl. Acad. Sci. USA 45: 828–832.Google Scholar
  20. Coe, E.H., Jr. 1966. The properties, origin, and mechanism of conversion-type inheritance at the B locus in maize. Genetics 53: 1035–1063.Google Scholar
  21. Coe, E.H., Jr. 1979. Specification of the anthocyanin biosynthetic function by b and r in maize. Maydica 24: 49–58.Google Scholar
  22. Colot, V. and Rossignol, J.L. 1999. Eukaryotic DNA methylation as an evolutionary force. Bioessays 21: 402–411.PubMedGoogle Scholar
  23. Colot, V., Maloisel, L. and Rossignol, J.L. 1996. Interchromosomal transfer of epigenetic states in Ascobulus: transfer of DNA methylation is mechanistically related to homologous recombination. Cell 86: 855–864.Google Scholar
  24. Cone, K.C., Cocciolone, S. M., Burr, F.A. and Burr, B. 1993. Maize anthocyanin regulatory gene pl is a duplicate of c1 that functions in the plant. Plant Cell 5: 1795–1805.PubMedGoogle Scholar
  25. Csink, A.K. and Henikoff, S. 1996. Genetic modifications of heterochromatic associations and nuclear organization in Drosophila. Nature 381: 529–531.PubMedGoogle Scholar
  26. Das, O.P. and Messing, J. 1994. Variegated phenotype and developmental methylation changes of a maize allele originating from epimutation. Genetics 136: 1121–1141.PubMedGoogle Scholar
  27. DeCarvalho, F., Gheysen, G., Kushnir, S., Van Montagu, M., Inzé, D. and Castresana, C. 1992. Suppression of β-1,3–glucanase transgene expression in homozygous plants. EMBO J. 11: 2595–2602.PubMedGoogle Scholar
  28. Dooner, H.K. 1979. Identification of an R-locus region that controls the tissue specificity of anthocyanin formation inmaize. Genetics 93: 703–710.Google Scholar
  29. Dooner, H.K. and Kermicle, J.L. 1976. Displaced and tandem duplications in the long arm of chromosome 10 in maize. Genetics 82: 309–322.Google Scholar
  30. Dooner, H.K. and Martínez-Férez, I.M. 1997. Recombination occurs uniformly within the bronze gene, a meiotic recombination hotspot in the maize genome. Plant Cell 9: 1633–1646.PubMedGoogle Scholar
  31. Dooner, H.K., Weck, E., Adams, S., Ralston, E., Favreau, M. and English, J. 1985. A molecular genetic analysis of insertions in the bronze locus in maize. Mol. Gen. Genet. 200: 240–246.Google Scholar
  32. Dooner, H.K., Robbins, T.P. and Jorgensen, R.A. 1991. Genetic and developmental control of anthocyanin biosynthesis. Annu. Rev. Genet. 25: 173–199.Google Scholar
  33. Dreesen, T.D., Henikoff, S. and Loughney, K. 1991. A pairingsensitive element that mediates trans-inactivation associated with the Drosophila brown gene. Genes Dev. 5: 331–340.PubMedGoogle Scholar
  34. Eggleston, W., Alleman, M. and Kermicle, J.L. 1995. Molecular organization and germinal instability of R-stippled maize. Genetics 141: 347–360.PubMedGoogle Scholar
  35. Ekwall, K., Olsson, T., Turner, B.M., Cranston, G. and Allshire, R.C. 1997. Transient inhibition of histone deacetylation alters the structural and functional imprint at fission yeast centromeres. Cell 91: 1021–1032.PubMedGoogle Scholar
  36. Finnegan, E.J., Peacock, W.J. and Dennis, E.S. 1996. Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc. Natl. Acad. Sci. USA 93: 8449–8454.PubMedGoogle Scholar
  37. Gaut, B.S. and Doebley, J.F. 1997. DNA sequence evidence for the segmental allotetraploid origin of maize. Proc. Natl. Acad. Sci. USA 94: 6809–6814.PubMedGoogle Scholar
  38. Geyer, P.K., Green, M.M. and Corces, V.G. 1990. Tissue-specific transcriptional enhancers may act in trans on the gene located in the homologous chromsome: the molecular basis of transvection in Drosophila. EMBO J. 9: 2247–2256.PubMedGoogle Scholar
  39. Goff, S.A., Klein, T.M., Roth, B.A., Fromm, M.E., Cone, K.C. and Chandler, V.L. 1990. Trans-activation of anthocyanin biosynthetic genes following transfer of b regulatory genes into maize tissues. EMBO J. 9: 2517–2522.PubMedGoogle Scholar
  40. Goff, S.A., Cone, K.C. and Chandler, V.L. 1992. Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. Genes Dev. 6: 864–875.PubMedGoogle Scholar
  41. Grewal, S.I.S. and Klar, A.J.S. 1996. Chromosomal inheritance of epigenetic states in fission yeast during mitosis and meiosis. Cell 86: 95–101.PubMedGoogle Scholar
  42. Grotewold, E., Athma, P. and Peterson, T. 1991. Alternatively spliced products of the maize P gene encode proteins with homology to the DNA binding domain of Myb-like transcription factors. Proc. Natl. Acad. Sci. USA 88: 4587–4591.PubMedGoogle Scholar
  43. Grotewold, E., Drummond, B., Bowen, B. and Peterson, T. 1994. The Myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76: 543–553.CrossRefPubMedGoogle Scholar
  44. Heard, E., Clerc, P. and Avner, P. 1997. X-chromosome inactivation in mammals. Annu. Rev. Genet. 31: 571–610.PubMedGoogle Scholar
  45. Henikoff, S. 1998. Conspiracy of silence among repeated transgenes. BioEssays 20: 532–535.PubMedGoogle Scholar
  46. Henikoff, S. and Comai, L. 1998. Trans-sensing effects: the ups and downs of being together. Cell 93: 329–332.PubMedGoogle Scholar
  47. Hoekenga, O. 1998. Epigenetic regulation of Pl-Blotched. Ph.D. dissertation, University of Missouri, Columbia, MO.Google Scholar
  48. Hollick, J.B. and Chandler, V.L. 1998. Epigenetic allelic states of a maize transcriptional regulatory locus exhibit overdominant gene action. Genetics 150: 891–897.PubMedGoogle Scholar
  49. Hollick, J.B., Patterson, G.I., Coe, E.H. Jr., Cone, K.C. and Chandler, V. L. 1995. Allelic interactions heritably alter the activity of a metastable maize pl1 allele. Genetics 141: 709–719.PubMedGoogle Scholar
  50. Hollick, J.B., Dorweiler, J.E. and Chandler, V.L. 1997. Paramutation and related allelic interactions. Trends Genet. 13: 302–308PubMedGoogle Scholar
  51. Hollick, J.B., Patterson, G.I., Asmundsson, I.M. and Chandler, V.L. 2000. Paramutation alters regulatory control of the maize pl1 locus. Genetics, 154: 1827–1838.PubMedGoogle Scholar
  52. Ingelbrecht, I., Van Houdt, H., Van Montagu, M. and Depicker, A. 1994. Post-transcriptional silencing of reporter transgenes in tobacco correlates with DNA methylation. Proc. Natl. Acad. Sci. USA 91: 10502–10506.PubMedGoogle Scholar
  53. Jeddeloh, J.A., Stokes, T.L. and Richards, E.J. 1999. Maintenance of genomic methylation requires a SWI2/SNF2–like protein. Nature Genet. 22: 94–97.PubMedGoogle Scholar
  54. Jorgensen, R.A. 1995. Cosuppression, flower color patterns, and metastable gene expression states. Science 268: 686–691.Google Scholar
  55. Kermicle, J. L. 1996. Epigenetic silencing and activation of a maize r gene. In: V.E.A. Russo, R.A. Martienssen and A.D. Riggs (Eds) Epigenetic Mechanisms of Gene Regulation, Cold Spring Harbor Laboratory Press, Plainview, NY, pp. 267–287.Google Scholar
  56. Kermicle, J.L. and Axtell, J.D. 1981. Modification of chlorophyll striping by the R region. Maydica 26: 185–197.Google Scholar
  57. Kermicle, J.L., Eggleston W.B. and Alleman, M. 1995. Organization of paramutagenicity in R-stippled maize. Genetics 141: 361–372.PubMedGoogle Scholar
  58. Klar, A.J.S. 1998. Propagating epigenetic states through meiosis: where Mendel's gene is more than a DNA moiety. Trends Genet. 14: 299–301.PubMedGoogle Scholar
  59. Krebbers, E., Hehl, R., Piotrowiak, R., Lonnig, W., Sommer, H. and Saedler, H. 1987. Molecular analysis of paramutant plants of Antirrhinum majus and the involvement of transposable elements. Mol. Gen. Genet. 214: 325–327.Google Scholar
  60. Lechelt, C., Peterson, T., Laird, A., Chen, J., Dellaporta, S., Dennis, E., Peacock, W.J. and Starlinger, P. 1989. Isolation and molecular analysis of the maize P locus. Mol. Gen. Genet. 219: 225–234.PubMedGoogle Scholar
  61. Lee, J.T. and Jaenisch, R. 1997. Long-range cis effects of ectopic Xinactivation centers on a mouse autosome. Nature 386: 275–279.PubMedGoogle Scholar
  62. Lee, J.T., Strauss, W.M., Dausman, J.A. and Jaenisch, R. 1996. A 450 kb transgene displays properties of the mammalian X-inactivation center. Cell 86: 83–94.PubMedGoogle Scholar
  63. Ludwig, S.R., Bowen, B., Beach, L. and Wessler, S. 1990. A regulatory gene as a novel visible marker for maize transformation. Science 247: 449–450.Google Scholar
  64. Ludwig, S.R. and Wessler, S.R. 1990. Maize R gene family: tissuespecific helix-loop-helix proteins. Cell 62: 849–851.PubMedGoogle Scholar
  65. Lund, G., Das, O.P. and Messing, J. 1995. Tissue-specific DNaseIsensitive sites of the maize P gene and their changes upon epimutation. Plant J. 7: 797–807.Google Scholar
  66. Maloisel, L. and Rossignol, J.L. 1998. Suppression of crossing-over by DNA methylation in Ascobolus. Genes Dev. 12: 1381–1389.PubMedGoogle Scholar
  67. Martienssen, R.A. 1996. Epigenetic silencing of Mu transposable elements in maize. In: V.E.A. Russo, R.A. Martienssen and A.D. Riggs (Eds) Epigenetic Mechanisms of Gene Regulation, Cold Spring Harbor Laboratory Press, Plainview, NY, pp. 593–608.Google Scholar
  68. Matzke, M.A., Matzke, A.J.M. and Eggleston, W.B. 1996. Paramutation and transgene silencing: a common response to invasive DNA? Trends Plant Sci. 1: 382–388.Google Scholar
  69. Matzke, A.J.M., Neuhuber, F., Park, Y.-D., Ambros, D.F. and Matzke, M.A. 1994. Homology-dependent gene silencing in transgenic plants, epistatic silencing loci contain multiple copies of methylated transgenes. Mol. Gen. Genet. 244: 219–229.PubMedGoogle Scholar
  70. McClintock, B. 1965. The control of gene action in maize. Brookhaven Symp. Biol. 18: 162–184.Google Scholar
  71. McWhirter, K.S. and Brink, R.A. 1962. Continuous variation in level of paramutation at the R locus in maize. Genetics 47: 1053–1074.Google Scholar
  72. Meyer, P., Heidmann, I. and Niedenhoff, I. 1993. Differences in DNA methylation are associated with a paramutation phenomenon in transgenic petunia. Plant J. 4: 89–100.PubMedGoogle Scholar
  73. Meyer, P., Linn, F., Heidmann, I., Meyer, Z.A.H., Niedenhof, I. and Saedler, H. 1992. Endogenous and environmental factors influence 35S promoter methylation of a maize A1-gene construct in transgenic petunia and its colour phenotype. Mol. Gen. Genet. 231: 345–352.PubMedGoogle Scholar
  74. Mikula, B.C. 1961. Progressive conversion of R-locus expression in maize. Proc. Natl. Acad. Sci. USA 47: 566–571.PubMedGoogle Scholar
  75. Mikula, B.C. 1967. Heritable changes in R-locus expression in maize is responsive to environment. Genetics 56: 733–742.Google Scholar
  76. Mikula, B.C. 1995. Environmental programming of heritable epigenetic changes in paramutant r-gene expression using temperature and light at a specific stage of early development in maize seedlings. Genetics 140: 1379–1387.PubMedGoogle Scholar
  77. Neal, K.C. 1998. Characterization of the organization and paramutagenicity of the maize R-marbled allele. M.S. dissertation, Virginia Commonwealth University, Richmond, VA.Google Scholar
  78. Panavas, T., Weir, J. and Walker, E.L. 1999. The structure and paramutagenicity of the R-marbled haplotype in Zea mays. Genetics 153: 979–991.PubMedGoogle Scholar
  79. Panning, B. and Jaenisch, R. 1998. RNA and the epigenetic regulation of X chromosome inactivation. Cell 93: 305–308.PubMedGoogle Scholar
  80. Patterson, G.I. and Chandler, V.L. 1995. Timing of b locus paramutation. Maydica 40: 35–41.Google Scholar
  81. Patterson, G.I., Harris, L.J., Walbot, V. and Chandler, V.L. 1991. Genetic analysis of B-Peru, a regulatory gene in maize. Genetics 126: 205–220.Google Scholar
  82. Patterson, G.I., Thorpe, C.J. and Chandler, V.L. 1993. Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize b regulatory gene. Genetics 135: 881–894.PubMedGoogle Scholar
  83. Patterson, G.I., Kubo, K.M., Shroyer, T. and Chandler, V.L. 1995. Sequences required for paramutation of the maize b gene map to a region containing the promoter and upstream sequences. Genetics 140: 1389–1406.PubMedGoogle Scholar
  84. Penny, G.D., Kay, G.F., Sheardown, S.A., Rastan, S. and Brockdorff, N. 1996. Requirement for Xist in X chromosome inactivation. Nature 379: 131–137.CrossRefPubMedGoogle Scholar
  85. Pirrotta, V. 1997. PcG complexes and chromatin silencing. Curr. Opin. Genet. Dev. 7: 249–258.PubMedGoogle Scholar
  86. Pirrotta, V. 1998. Polycombing the genome: PcG, trxG and chromatin silencing. Cell 93: 333–336.PubMedGoogle Scholar
  87. Quinn, A.R. 1999. Characterization of the transposable element responsible for germinal and somatic instability of the maize R-marbled allele. M.S. dissertation, Virginia Commonwealth University, Richmond, VA.Google Scholar
  88. Radicella, J.P., Turks, D. and Chandler, V.L. 1991. Cloning and nucleotide sequence of a cDNA encoding B-Peru, a regulatory protein of the anthocyanin pathway in maize. Plant Mol. Biol. 17: 127–130.PubMedGoogle Scholar
  89. Radicella, J.P., Brown, D., Tolar, L.A. and Chandler, V.L. 1992. Allelic diversity of the maize b regulatory gene: different leader and promoter sequences of two b alleles determine distinct tissue specificities of anthocyanin production. Genes Dev. 6: 2152–2164.PubMedGoogle Scholar
  90. Robbins, T.P., Walker, E.L., Kermicle, J.L., Alleman, M. and Dellaporta, S.L. 1991. Meiotic instability of the R-r complex arising from displaced intragenic exchange and intrachromosomal rearrangement. Genetics 129: 217–283.Google Scholar
  91. Sastry, G.R.K., Cooper, H.B., Jr. and Brink, R.A. 1965. Paramutation and somatic mosaicism in maize. Genetics 52: 407–424.PubMedGoogle Scholar
  92. Schwartz, D.C. and Cantor, C.R. 1984. Separation of yeast chromosome-sized DNAs by pulsed-field gel gradient electrophoresis. Cell 37: 67–75.CrossRefPubMedGoogle Scholar
  93. Selinger, D.A. and Chandler, V.L. 1999. Major recent and independent changes in levels and patterns of expression have occurred at the b gene, a regulatory locus in maize. Proc. Natl. Acad. Sci. USA 96: 15007–15012.PubMedGoogle Scholar
  94. Selinger, D.A., Lisch, D. and Chandler, V.L. 1998. The maize regulatory gene, B-Peru, contains a DNA rearrangement that specifies tissue-specific expression through both positive and negative promoter elements. Genetics 149: 1125–1138.PubMedGoogle Scholar
  95. Selker, E.U. 1997. Epigenetic phenomena in filamentous fungi: useful paradigms or repeat-induced confusion? Trends Genet. 13: 293–341.PubMedGoogle Scholar
  96. Sherman, J. M. and Pillus, L. 1997. An uncertain silence. Trends Genet. 13: 308–313.PubMedGoogle Scholar
  97. Shih, K.L. and Brink, R.A. 1969. Effects of X-irradiation on aleurone pigmenting potential of standard Rr and a paramutant form of Rr in maize. Genetics 61: 167–177.PubMedGoogle Scholar
  98. Shore, D. 1995. Telomere position effects and transcriptional silencing in the yeast Saccharomyces cerevisiae. In: E.H. Blackburn and C.W. Greider (Eds) Telomeres, Cold Spring Harbor Laboratory Press, Plainview, NY, pp. 139–191.Google Scholar
  99. Sidorenko, L., Li, X., Tagliani, L., Bowen, B. and Peterson, T. 1999. Characterization of the regulatory elements of the maize P-rr gene by transient expression assays. Plant Mol. Biol. 39: 11–19.PubMedGoogle Scholar
  100. Smolik-Utlaut, S. and Gelbart, W.M. 1987. The effects of chromosomal rearrangements on zeste-white interaction in Drosophila melanogaster. Genetics 116: 285–298.PubMedGoogle Scholar
  101. Stam, M., Lavin, M.T. and Chandler, V.L. 2000. Npi402 and ncsu1 are identical; inra1(tmp) maps upstream of the b promoter. Maize Genet. Coop. Newsl. 74, in press.Google Scholar
  102. Stam, M., de Bruin, R., Kenter, S., van der Hoorn, R.A.L., van Blokland, R., Mol, J.N.M. and Kooter, J.M. 1997. Post-transcriptional silencing of chalcone synthase in Petunia by inverted transgene repeats. Plant J. 12: 63–82.Google Scholar
  103. Steinmuller, K. and Apel, K. 1986. A simple and efficient procedure for isolating plant chromatin which is suitable for studies of DNase I sensitive domains and hypersensitive sites. Plant Mol. Biol. 7: 87–94.Google Scholar
  104. Styles, E.D. and Brink, R.A. 1966. The metastable nature of paramutable R alleles in maize. I. Heritable enhancement in level of standard Rr action. Genetics 54: 433–439.Google Scholar
  105. Styles, E.D. and Brink, R.A. 1969. The metastable nature of paramutable R alleles in maize. IV. Parallel enhancement of R action in heterozygotes with r and in hemizygotes. Genetics 61: 801–811.Google Scholar
  106. Styles, E.D. and Ceska, O. 1977. The genetic control of flavonoid synthesis in maize. Can. J. Genet. Cytol. 19: 3019–3021.Google Scholar
  107. Styles, E.D., Ceska, O. and Seah, K.T. 1973. Developmental differences in action of r and b alleles in maize. Can. J. Genet. Cytol. 15: 59–72.Google Scholar
  108. Thuriax, P. 1977. Is recombination confined to structural genes on the eukaryotic genome? Nature 268: 460–462.PubMedGoogle Scholar
  109. van Blokland, R., ten Lohuis, M. and Meyer, P. 1997. Condensation of chromatin in transcriptional regions of an inactivated plant transgene: evidence for an active role of transcription in gene silencing. Mol. Gen. Genet. 257: 1–13.PubMedGoogle Scholar
  110. van Houwelingen, A., Souer, E., Mol, J. and Koes, R. 1999. Epigenetic interactions among three dTph1 transposons in two homologous chromosomes activate a new excision-repair mechanism in Petunia. Plant Cell 11: 1319–1336.PubMedGoogle Scholar
  111. van West, P., Kamoun, S., van 't Klooster, J.W. and Govers, F. 1999. Internuclear gene silencing in Phytophthora infestans. Mol. Cell 3: 339–348.PubMedGoogle Scholar
  112. Vaucheret, H. 1993. Identification of a general silencer for 19S and 35S promoters in a transgenic tobacco plant: 90 bp of homology in the promoter sequences are sufficient for trans-inactivation. C. R. Acad. Sci. Paris: 317: 310–323.Google Scholar
  113. Vaucheret, H., Beclin, C., Elmayan, T., Feuerbach, F., Godon, C., Morel, J.-B., Mourrain, P., Palauqui, J.-C. and Vernhetter, S. 1998. Transgene-induced gene silencing in plants. Plant J: 651–659.Google Scholar
  114. Vongs, A., Kakutani, T., Martienssen, R., and Richards, E.J. 1993. Arabidopsis thaliana DNA methylation mutants. Science 260: 926–1928.PubMedGoogle Scholar
  115. Wakimoto, B.T. 1998. Beyond the nucleosome: epigenetic aspects of position-effect variegation in Drosophila. Cell 93: 321–324.PubMedGoogle Scholar
  116. Walker, E.L., Robbins, T.P., Bureau, T.E., Kermicle, J. and Dellaporta, S.L. 1995. Transposon-mediated chromosomal rearrangements and gene duplications in the formation of the maize R-r complex. EMBO J. 14: 2350–2363.PubMedGoogle Scholar
  117. Walker, E. 1998. Paramutation of the r1 locus of maize is associated with increased cytosine methylation. Genetics 148: 1973–1981.PubMedGoogle Scholar
  118. Williams, W.M. 1972. Variability of the R-stippled gene in maize. Ph.D. dissertation, University of Wisconsin, Madison, WI.Google Scholar
  119. Wolffe, A.P. and Matzke, M. A. 1999. Epigenetics: regulation through repression. Science 286: 481–486.PubMedGoogle Scholar
  120. Yoder, J.A., Walsh, C.P. and Bestor, T.H. 1997. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 13: 335–340.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Vicki L. Chandler
    • 1
  • William B. Eggleston
    • 2
  • Jane E. Dorweiler
    • 1
  1. 1.Department of Plant SciencesUniversity of ArizonaTucsonUSA
  2. 2.Department of BiologyVirginia Commonwealth UniversityRichmondUSA

Personalised recommendations