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. 1998 Apr;148(4):1973–1981. doi: 10.1093/genetics/148.4.1973

Paramutation of the r1 locus of maize is associated with increased cytosine methylation.

E L Walker 1
PMCID: PMC1460097  PMID: 9560410

Abstract

In paramutation two alleles of a gene interact so that one of the alleles is epigenetically silenced. The silenced state is then genetically transmissible for many generations. The large (220 kbp) multigenic complex R-r is paramutable: its level of expression is changed during paramutation. R-r was found to exhibit increases in its level of cytosine methylation (C-methylation) following paramutation. These C-methylation changes are localized to the 5' portions of the two genes in the complex that are most sensitive to paramutation. These methylation changes flank a small region called sigma that is thought to have been derived from a transposon named doppia. A mutant derivative of R-r that has a deletion of the sigma region fails to become methylated under conditions in which R-r is heavily methylated. This suggests that the presence of sigma sequences at the locus is required for the methylation changes that are observed following paramutation.

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Selected References

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  1. Assaad F. F., Tucker K. L., Signer E. R. Epigenetic repeat-induced gene silencing (RIGS) in Arabidopsis. Plant Mol Biol. 1993 Sep;22(6):1067–1085. doi: 10.1007/BF00028978. [DOI] [PubMed] [Google Scholar]
  2. BRINK R. A. Paramutation at the R locus in maize. Cold Spring Harb Symp Quant Biol. 1958;23:379–391. doi: 10.1101/sqb.1958.023.01.036. [DOI] [PubMed] [Google Scholar]
  3. Bender J., Fink G. R. Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell. 1995 Dec 1;83(5):725–734. doi: 10.1016/0092-8674(95)90185-x. [DOI] [PubMed] [Google Scholar]
  4. Brink R A. A Genetic Change Associated with the R Locus in Maize Which Is Directed and Potentially Reversible. Genetics. 1956 Nov;41(6):872–889. doi: 10.1093/genetics/41.6.872. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brink R. A. Paramutation. Annu Rev Genet. 1973;7:129–152. doi: 10.1146/annurev.ge.07.120173.001021. [DOI] [PubMed] [Google Scholar]
  6. Brown D. F. Paramutability of R and R mutant genes derived from an R allele in maize. Genetics. 1966 Sep;54(3):899–910. doi: 10.1093/genetics/54.3.899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cocciolone S. M., Cone K. C. Pl-Bh, an anthocyanin regulatory gene of maize that leads to variegated pigmentation. Genetics. 1993 Oct;135(2):575–588. doi: 10.1093/genetics/135.2.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Coe E. H. The properties, origin, and mechanism of conversion-type inheritance at the B locus in maize. Genetics. 1966 Jun;53(6):1035–1063. doi: 10.1093/genetics/53.6.1035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cone K. C., Cocciolone S. M., Moehlenkamp C. A., Weber T., Drummond B. J., Tagliani L. A., Bowen B. A., Perrot G. H. Role of the regulatory gene pl in the photocontrol of maize anthocyanin pigmentation. Plant Cell. 1993 Dec;5(12):1807–1816. doi: 10.1105/tpc.5.12.1807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Consonni G., Viotti A., Dellaporta S. L., Tonelli C. cDNA nucleotide sequence of Sn, a regulatory gene in maize. Nucleic Acids Res. 1992 Jan 25;20(2):373–373. doi: 10.1093/nar/20.2.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dooner H. K., Robbins T. P., Jorgensen R. A. Genetic and developmental control of anthocyanin biosynthesis. Annu Rev Genet. 1991;25:173–199. doi: 10.1146/annurev.ge.25.120191.001133. [DOI] [PubMed] [Google Scholar]
  12. Eggleston W. B., Alleman M., Kermicle J. L. Molecular organization and germinal instability of R-stippled maize. Genetics. 1995 Sep;141(1):347–360. doi: 10.1093/genetics/141.1.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gierl A., Lütticke S., Saedler H. TnpA product encoded by the transposable element En-1 of Zea mays is a DNA binding protein. EMBO J. 1988 Dec 20;7(13):4045–4053. doi: 10.1002/j.1460-2075.1988.tb03298.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Goff S. A., Klein T. M., Roth B. A., Fromm M. E., Cone K. C., Radicella J. P., Chandler V. L. Transactivation of anthocyanin biosynthetic genes following transfer of B regulatory genes into maize tissues. EMBO J. 1990 Aug;9(8):2517–2522. doi: 10.1002/j.1460-2075.1990.tb07431.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hollick J. B., Patterson G. I., Coe E. H., Jr, Cone K. C., Chandler V. L. Allelic interactions heritably alter the activity of a metastable maize pl allele. Genetics. 1995 Oct;141(2):709–719. doi: 10.1093/genetics/141.2.709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jorgensen R. A. Cosuppression, flower color patterns, and metastable gene expression States. Science. 1995 May 5;268(5211):686–691. doi: 10.1126/science.268.5211.686. [DOI] [PubMed] [Google Scholar]
  17. Kermicle J. L. Dependence of the R-mottled aleurone phenotype in maize on mode of sexual transmission. Genetics. 1970 Sep;66(1):69–85. doi: 10.1093/genetics/66.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ludwig S. R., Habera L. F., Dellaporta S. L., Wessler S. R. Lc, a member of the maize R gene family responsible for tissue-specific anthocyanin production, encodes a protein similar to transcriptional activators and contains the myc-homology region. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7092–7096. doi: 10.1073/pnas.86.18.7092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Martienssen R. Epigenetic phenomena: paramutation and gene silencing in plants. Curr Biol. 1996 Jul 1;6(7):810–813. doi: 10.1016/s0960-9822(02)00601-2. [DOI] [PubMed] [Google Scholar]
  20. Matzke A. J., Neuhuber F., Park Y. D., Ambros P. F., Matzke M. A. Homology-dependent gene silencing in transgenic plants: epistatic silencing loci contain multiple copies of methylated transgenes. Mol Gen Genet. 1994 Aug 2;244(3):219–229. doi: 10.1007/BF00285449. [DOI] [PubMed] [Google Scholar]
  21. Matzke M. A., Matzke AJM. How and Why Do Plants Inactivate Homologous (Trans)genes? Plant Physiol. 1995 Mar;107(3):679–685. doi: 10.1104/pp.107.3.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Meyer P., Heidmann I., Niedenhof I. Differences in DNA-methylation are associated with a paramutation phenomenon in transgenic petunia. Plant J. 1993 Jul;4(1):89–100. doi: 10.1046/j.1365-313x.1993.04010089.x. [DOI] [PubMed] [Google Scholar]
  23. Meyer P., Saedler H. HOMOLOGY-DEPENDENT GENE SILENCING IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):23–48. doi: 10.1146/annurev.arplant.47.1.23. [DOI] [PubMed] [Google Scholar]
  24. Patterson G. I., Kubo K. M., Shroyer T., Chandler V. L. Sequences required for paramutation of the maize b gene map to a region containing the promoter and upstream sequences. Genetics. 1995 Aug;140(4):1389–1406. doi: 10.1093/genetics/140.4.1389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Robbins T. P., Walker E. L., Kermicle J. L., Alleman M., Dellaporta S. L. Meiotic instability of the R-r complex arising from displaced intragenic exchange and intrachromosomal rearrangement. Genetics. 1991 Sep;129(1):271–283. doi: 10.1093/genetics/129.1.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Robbins T. P., Walker E. L., Kermicle J. L., Alleman M., Dellaporta S. L. Meiotic instability of the R-r complex arising from displaced intragenic exchange and intrachromosomal rearrangement. Genetics. 1991 Sep;129(1):271–283. doi: 10.1093/genetics/129.1.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ronchi A., Petroni K., Tonelli C. The reduced expression of endogenous duplications (REED) in the maize R gene family is mediated by DNA methylation. EMBO J. 1995 Nov 1;14(21):5318–5328. doi: 10.1002/j.1460-2075.1995.tb00216.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schläppi M., Raina R., Fedoroff N. Epigenetic regulation of the maize Spm transposable element: novel activation of a methylated promoter by TnpA. Cell. 1994 May 6;77(3):427–437. doi: 10.1016/0092-8674(94)90157-0. [DOI] [PubMed] [Google Scholar]
  29. Styles E. D., Brink R. A. The Metastable Nature of Paramutable R Alleles in Maize. IV. Parallel Enhancement of R Action in Heterozygotes with r and in Hemizygotes. Genetics. 1969 Apr;61(4):801–811. doi: 10.1093/genetics/61.4.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Styles E. D., Brink R. A. The metastable nature of paramutable R alleles in maize. I. Heritable enhancement in level of standard R action. Genetics. 1966 Aug;54(2):433–439. doi: 10.1093/genetics/54.2.433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Trentmann S. M., Saedler H., Gierl A. The transposable element En/Spm-encoded TNPA protein contains a DNA binding and a dimerization domain. Mol Gen Genet. 1993 Apr;238(1-2):201–208. doi: 10.1007/BF00279548. [DOI] [PubMed] [Google Scholar]
  32. WEYERS W. H. Expression and stability of the marbled allele in maize. Genetics. 1961 Aug;46:1061–1067. doi: 10.1093/genetics/46.8.1061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Walker E. L., Robbins T. P., Bureau T. E., Kermicle J., Dellaporta S. L. Transposon-mediated chromosomal rearrangements and gene duplications in the formation of the maize R-r complex. EMBO J. 1995 May 15;14(10):2350–2363. doi: 10.1002/j.1460-2075.1995.tb07230.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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