Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2002 Sep;162(1):355–363. doi: 10.1093/genetics/162.1.355

The control of natural variation in cytosine methylation in Arabidopsis.

Nicole C Riddle 1, Eric J Richards 1
PMCID: PMC1462236  PMID: 12242246

Abstract

We explore the extent and sources of epigenetic variation in cytosine methylation in natural accessions of the flowering plant, Arabidopsis thaliana, by focusing on the methylation of the major rRNA gene repeats at the two nucleolus organizer regions (NOR). Our findings indicate that natural variation in NOR methylation results from a combination of genetic and epigenetic mechanisms. Genetic variation in rRNA gene copy number and trans-acting modifier loci account for some of the natural variation in NOR methylation. Our results also suggest that divergence and inheritance of epigenetic information, independent of changes in underlying nucleotide sequence, may play an important role in maintaining natural variation in cytosine methylation.

Full Text

The Full Text of this article is available as a PDF (154.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alonso-Blanco C., Koornneef M. Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. Trends Plant Sci. 2000 Jan;5(1):22–29. doi: 10.1016/s1360-1385(99)01510-1. [DOI] [PubMed] [Google Scholar]
  2. Alonso-Blanco C., Peeters A. J., Koornneef M., Lister C., Dean C., van den Bosch N., Pot J., Kuiper M. T. Development of an AFLP based linkage map of Ler, Col and Cvi Arabidopsis thaliana ecotypes and construction of a Ler/Cvi recombinant inbred line population. Plant J. 1998 Apr;14(2):259–271. doi: 10.1046/j.1365-313x.1998.00115.x. [DOI] [PubMed] [Google Scholar]
  3. Bestor T. H. The DNA methyltransferases of mammals. Hum Mol Genet. 2000 Oct;9(16):2395–2402. doi: 10.1093/hmg/9.16.2395. [DOI] [PubMed] [Google Scholar]
  4. Burn J. E., Bagnall D. J., Metzger J. D., Dennis E. S., Peacock W. J. DNA methylation, vernalization, and the initiation of flowering. Proc Natl Acad Sci U S A. 1993 Jan 1;90(1):287–291. doi: 10.1073/pnas.90.1.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Campell B. R., Song Y., Posch T. E., Cullis C. A., Town C. D. Sequence and organization of 5S ribosomal RNA-encoding genes of Arabidopsis thaliana. Gene. 1992 Mar 15;112(2):225–228. doi: 10.1016/0378-1119(92)90380-8. [DOI] [PubMed] [Google Scholar]
  6. Chen R. Z., Pettersson U., Beard C., Jackson-Grusby L., Jaenisch R. DNA hypomethylation leads to elevated mutation rates. Nature. 1998 Sep 3;395(6697):89–93. doi: 10.1038/25779. [DOI] [PubMed] [Google Scholar]
  7. Conconi A., Widmer R. M., Koller T., Sogo J. M. Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell. 1989 Jun 2;57(5):753–761. doi: 10.1016/0092-8674(89)90790-3. [DOI] [PubMed] [Google Scholar]
  8. Copenhaver G. P., Pikaard C. S. RFLP and physical mapping with an rDNA-specific endonuclease reveals that nucleolus organizer regions of Arabidopsis thaliana adjoin the telomeres on chromosomes 2 and 4. Plant J. 1996 Feb;9(2):259–272. doi: 10.1046/j.1365-313x.1996.09020259.x. [DOI] [PubMed] [Google Scholar]
  9. Copenhaver G. P., Pikaard C. S. Two-dimensional RFLP analyses reveal megabase-sized clusters of rRNA gene variants in Arabidopsis thaliana, suggesting local spreading of variants as the mode for gene homogenization during concerted evolution. Plant J. 1996 Feb;9(2):273–282. doi: 10.1046/j.1365-313x.1996.09020273.x. [DOI] [PubMed] [Google Scholar]
  10. Cubas P., Vincent C., Coen E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature. 1999 Sep 9;401(6749):157–161. doi: 10.1038/43657. [DOI] [PubMed] [Google Scholar]
  11. Dammann R., Lucchini R., Koller T., Sogo J. M. Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae. Nucleic Acids Res. 1993 May 25;21(10):2331–2338. doi: 10.1093/nar/21.10.2331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dennis K., Fan T., Geiman T., Yan Q., Muegge K. Lsh, a member of the SNF2 family, is required for genome-wide methylation. Genes Dev. 2001 Nov 15;15(22):2940–2944. doi: 10.1101/gad.929101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Doerge R. W., Churchill G. A. Permutation tests for multiple loci affecting a quantitative character. Genetics. 1996 Jan;142(1):285–294. doi: 10.1093/genetics/142.1.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Finnegan E. J., Peacock W. J., Dennis E. S. Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8449–8454. doi: 10.1073/pnas.93.16.8449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Flavell R. B., O'Dell M., Thompson W. F. Regulation of cytosine methylation in ribosomal DNA and nucleolus organizer expression in wheat. J Mol Biol. 1988 Dec 5;204(3):523–534. doi: 10.1016/0022-2836(88)90352-x. [DOI] [PubMed] [Google Scholar]
  16. Gibbons R. J., McDowell T. L., Raman S., O'Rourke D. M., Garrick D., Ayyub H., Higgs D. R. Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nat Genet. 2000 Apr;24(4):368–371. doi: 10.1038/74191. [DOI] [PubMed] [Google Scholar]
  17. Holliday R., Pugh J. E. DNA modification mechanisms and gene activity during development. Science. 1975 Jan 24;187(4173):226–232. [PubMed] [Google Scholar]
  18. Jackson James P., Lindroth Anders M., Cao Xiaofeng, Jacobsen Steven E. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature. 2002 Mar 17;416(6880):556–560. doi: 10.1038/nature731. [DOI] [PubMed] [Google Scholar]
  19. Jacobsen S. E., Meyerowitz E. M. Hypermethylated SUPERMAN epigenetic alleles in arabidopsis. Science. 1997 Aug 22;277(5329):1100–1103. doi: 10.1126/science.277.5329.1100. [DOI] [PubMed] [Google Scholar]
  20. Jacobsen S. E., Sakai H., Finnegan E. J., Cao X., Meyerowitz E. M. Ectopic hypermethylation of flower-specific genes in Arabidopsis. Curr Biol. 2000 Feb 24;10(4):179–186. doi: 10.1016/s0960-9822(00)00324-9. [DOI] [PubMed] [Google Scholar]
  21. Jeddeloh J. A., Bender J., Richards E. J. The DNA methylation locus DDM1 is required for maintenance of gene silencing in Arabidopsis. Genes Dev. 1998 Jun 1;12(11):1714–1725. doi: 10.1101/gad.12.11.1714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kakutani T., Jeddeloh J. A., Flowers S. K., Munakata K., Richards E. J. Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12406–12411. doi: 10.1073/pnas.93.22.12406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kakutani T., Munakata K., Richards E. J., Hirochika H. Meiotically and mitotically stable inheritance of DNA hypomethylation induced by ddm1 mutation of Arabidopsis thaliana. Genetics. 1999 Feb;151(2):831–838. doi: 10.1093/genetics/151.2.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Knox M. R., Ellis T. H. Stability and inheritance of methylation states at PstI sites in Pisum. Mol Genet Genomics. 2001 May;265(3):497–507. doi: 10.1007/s004380000438. [DOI] [PubMed] [Google Scholar]
  25. Lander E. S., Botstein D. Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics. 1989 Jan;121(1):185–199. doi: 10.1093/genetics/121.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Li E., Bestor T. H., Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell. 1992 Jun 12;69(6):915–926. doi: 10.1016/0092-8674(92)90611-f. [DOI] [PubMed] [Google Scholar]
  27. Malagnac F., Wendel B., Goyon C., Faugeron G., Zickler D., Rossignol J. L., Noyer-Weidner M., Vollmayr P., Trautner T. A., Walter J. A gene essential for de novo methylation and development in Ascobolus reveals a novel type of eukaryotic DNA methyltransferase structure. Cell. 1997 Oct 17;91(2):281–290. doi: 10.1016/s0092-8674(00)80410-9. [DOI] [PubMed] [Google Scholar]
  28. Martienssen R. A., Colot V. DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science. 2001 Aug 10;293(5532):1070–1074. doi: 10.1126/science.293.5532.1070. [DOI] [PubMed] [Google Scholar]
  29. Miao V. P., Freitag M., Selker E. U. Short TpA-rich segments of the zeta-eta region induce DNA methylation in Neurospora crassa. J Mol Biol. 2000 Jul 7;300(2):249–273. doi: 10.1006/jmbi.2000.3864. [DOI] [PubMed] [Google Scholar]
  30. Miura A., Yonebayashi S., Watanabe K., Toyama T., Shimada H., Kakutani T. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature. 2001 May 10;411(6834):212–214. doi: 10.1038/35075612. [DOI] [PubMed] [Google Scholar]
  31. Monk M., Boubelik M., Lehnert S. Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development. 1987 Mar;99(3):371–382. doi: 10.1242/dev.99.3.371. [DOI] [PubMed] [Google Scholar]
  32. Oakeley E. J., Podestà A., Jost J. P. Developmental changes in DNA methylation of the two tobacco pollen nuclei during maturation. Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11721–11725. doi: 10.1073/pnas.94.21.11721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Okano M., Bell D. W., Haber D. A., Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell. 1999 Oct 29;99(3):247–257. doi: 10.1016/s0092-8674(00)81656-6. [DOI] [PubMed] [Google Scholar]
  34. Pruitt R. E., Meyerowitz E. M. Characterization of the genome of Arabidopsis thaliana. J Mol Biol. 1986 Jan 20;187(2):169–183. doi: 10.1016/0022-2836(86)90226-3. [DOI] [PubMed] [Google Scholar]
  35. Pélissier T., Tutois S., Tourmente S., Deragon J. M., Picard G. DNA regions flanking the major Arabidopsis thaliana satellite are principally enriched in Athila retroelement sequences. Genetica. 1996 Mar;97(2):141–151. doi: 10.1007/BF00054621. [DOI] [PubMed] [Google Scholar]
  36. Richards Eric J., Elgin Sarah C. R. Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell. 2002 Feb 22;108(4):489–500. doi: 10.1016/s0092-8674(02)00644-x. [DOI] [PubMed] [Google Scholar]
  37. Ronemus M. J., Galbiati M., Ticknor C., Chen J., Dellaporta S. L. Demethylation-induced developmental pleiotropy in Arabidopsis. Science. 1996 Aug 2;273(5275):654–657. doi: 10.1126/science.273.5275.654. [DOI] [PubMed] [Google Scholar]
  38. Schmitt F., Oakeley E. J., Jost J. P. Antibiotics induce genome-wide hypermethylation in cultured Nicotiana tabacum plants. J Biol Chem. 1997 Jan 17;272(3):1534–1540. doi: 10.1074/jbc.272.3.1534. [DOI] [PubMed] [Google Scholar]
  39. Soppe W. J., Jacobsen S. E., Alonso-Blanco C., Jackson J. P., Kakutani T., Koornneef M., Peeters A. J. The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell. 2000 Oct;6(4):791–802. doi: 10.1016/s1097-2765(05)00090-0. [DOI] [PubMed] [Google Scholar]
  40. Tamaru H., Selker E. U. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature. 2001 Nov 15;414(6861):277–283. doi: 10.1038/35104508. [DOI] [PubMed] [Google Scholar]
  41. Vongs A., Kakutani T., Martienssen R. A., Richards E. J. Arabidopsis thaliana DNA methylation mutants. Science. 1993 Jun 25;260(5116):1926–1928. doi: 10.1126/science.8316832. [DOI] [PubMed] [Google Scholar]
  42. Yates P. A., Burman R. W., Mummaneni P., Krussel S., Turker M. S. Tandem B1 elements located in a mouse methylation center provide a target for de novo DNA methylation. J Biol Chem. 1999 Dec 17;274(51):36357–36361. doi: 10.1074/jbc.274.51.36357. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES