Skip to main content
Genetics logoLink to Genetics
. 1998 May;149(1):307–318. doi: 10.1093/genetics/149.1.307

A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis.

S Henikoff 1, L Comai 1
PMCID: PMC1460135  PMID: 9584105

Abstract

Chromodomains are thought to mediate protein-protein interactions between chromatin components. We have detected a chromodomain embedded within the catalytic region of a predicted Arabidopsis DNA methyltransferase that is diverged from other eukaryotic enzymes. The 791 residue "chromomethylase" (CMT1) is encoded by a floral transcript that is spliced from 20 exons and is present at only approximately 1/10(-7) of total mRNA. Genomic sequencing reveals an ancient haplotype split at CMT1 between Col-0 + Metz and the other ecotypes examined. In the Col-0 + Metz haplotype, alternative mRNA processing at intron 13 truncates the coding region. In Ler, RLD, and No-0, similar truncation is caused by insertion of an intact retrotransposon, Evelknievel, which is present as a single copy in Ler and RLD and is currently methylated and inactive. Evelknievel is found at this site on a single branch that connects the Ler, RLD, and No-0 ecotypes but is absent from the genomes of all other ecotypes examined. A stop codon within exon 6 of the Metz ecotype confirms that CMT1 is nonessential. Nevertheless, comparison to CMT1 of Cardaminopsis arenosa, an outcrossing relative, indicates conservation for DNA methyltransferase function. We discuss how allelic diversity of CMT1 may reflect loosened selective constraints in a self-fertilizing species such as Arabidopsis thaliana.

Full Text

The Full Text of this article is available as a PDF (338.2 KB).

Selected References

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

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Ball L. J., Murzina N. V., Broadhurst R. W., Raine A. R., Archer S. J., Stott F. J., Murzin A. G., Singh P. B., Domaille P. J., Laue E. D. Structure of the chromatin binding (chromo) domain from mouse modifier protein 1. EMBO J. 1997 May 1;16(9):2473–2481. doi: 10.1093/emboj/16.9.2473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bartolomei M. S., Webber A. L., Brunkow M. E., Tilghman S. M. Epigenetic mechanisms underlying the imprinting of the mouse H19 gene. Genes Dev. 1993 Sep;7(9):1663–1673. doi: 10.1101/gad.7.9.1663. [DOI] [PubMed] [Google Scholar]
  4. Bestor T. H. DNA methylation: evolution of a bacterial immune function into a regulator of gene expression and genome structure in higher eukaryotes. Philos Trans R Soc Lond B Biol Sci. 1990 Jan 30;326(1235):179–187. doi: 10.1098/rstb.1990.0002. [DOI] [PubMed] [Google Scholar]
  5. Bird A. P. Gene number, noise reduction and biological complexity. Trends Genet. 1995 Mar;11(3):94–100. doi: 10.1016/S0168-9525(00)89009-5. [DOI] [PubMed] [Google Scholar]
  6. Chandler V. L., Walbot V. DNA modification of a maize transposable element correlates with loss of activity. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1767–1771. doi: 10.1073/pnas.83.6.1767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cheng X., Kumar S., Posfai J., Pflugrath J. W., Roberts R. J. Crystal structure of the HhaI DNA methyltransferase complexed with S-adenosyl-L-methionine. Cell. 1993 Jul 30;74(2):299–307. doi: 10.1016/0092-8674(93)90421-l. [DOI] [PubMed] [Google Scholar]
  8. Edwards K., Johnstone C., Thompson C. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res. 1991 Mar 25;19(6):1349–1349. doi: 10.1093/nar/19.6.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Hanfstingl U., Berry A., Kellogg E. A., Costa J. T., 3rd, Rüdiger W., Ausubel F. M. Haplotypic divergence coupled with lack of diversity at the Arabidopsis thaliana alcohol dehydrogenase locus: roles for both balancing and directional selection? Genetics. 1994 Nov;138(3):811–828. doi: 10.1093/genetics/138.3.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hebsgaard S. M., Korning P. G., Tolstrup N., Engelbrecht J., Rouzé P., Brunak S. Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information. Nucleic Acids Res. 1996 Sep 1;24(17):3439–3452. doi: 10.1093/nar/24.17.3439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Henikoff J. G., Pietrokovski S., Henikoff S. Recent enhancements to the Blocks Database servers. Nucleic Acids Res. 1997 Jan 1;25(1):222–225. doi: 10.1093/nar/25.1.222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Henikoff S., Henikoff J. G. Embedding strategies for effective use of information from multiple sequence alignments. Protein Sci. 1997 Mar;6(3):698–705. doi: 10.1002/pro.5560060319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Henikoff S., Henikoff J. G. Protein family classification based on searching a database of blocks. Genomics. 1994 Jan 1;19(1):97–107. doi: 10.1006/geno.1994.1018. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Kamm A., Galasso I., Schmidt T., Heslop-Harrison J. S. Analysis of a repetitive DNA family from Arabidopsis arenosa and relationships between Arabidopsis species. Plant Mol Biol. 1995 Mar;27(5):853–862. doi: 10.1007/BF00037014. [DOI] [PubMed] [Google Scholar]
  18. Karreman C., de Waard A. Agmenellum quadruplicatum M.AquI, a novel modification methylase. J Bacteriol. 1990 Jan;172(1):266–272. doi: 10.1128/jb.172.1.266-272.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Klimasauskas S., Kumar S., Roberts R. J., Cheng X. HhaI methyltransferase flips its target base out of the DNA helix. Cell. 1994 Jan 28;76(2):357–369. doi: 10.1016/0092-8674(94)90342-5. [DOI] [PubMed] [Google Scholar]
  20. Konieczny A., Voytas D. F., Cummings M. P., Ausubel F. M. A superfamily of Arabidopsis thaliana retrotransposons. Genetics. 1991 Apr;127(4):801–809. doi: 10.1093/genetics/127.4.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Laird P. W., Jaenisch R. The role of DNA methylation in cancer genetic and epigenetics. Annu Rev Genet. 1996;30:441–464. doi: 10.1146/annurev.genet.30.1.441. [DOI] [PubMed] [Google Scholar]
  22. Lippuner V., Chou I. T., Scott S. V., Ettinger W. F., Theg S. M., Gasser C. S. Cloning and characterization of chloroplast and cytosolic forms of cyclophilin from Arabidopsis thaliana. J Biol Chem. 1994 Mar 18;269(11):7863–7868. [PubMed] [Google Scholar]
  23. Lucas H., Feuerbach F., Kunert K., Grandbastien M. A., Caboche M. RNA-mediated transposition of the tobacco retrotransposon Tnt1 in Arabidopsis thaliana. EMBO J. 1995 May 15;14(10):2364–2373. doi: 10.1002/j.1460-2075.1995.tb07231.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Martienssen R. A., Richards E. J. DNA methylation in eukaryotes. Curr Opin Genet Dev. 1995 Apr;5(2):234–242. doi: 10.1016/0959-437x(95)80014-x. [DOI] [PubMed] [Google Scholar]
  25. Nebendahl A., Bäumlein H. Analysis of overlapping cDNA clones specific for a putative second DNA methyltransferase-encoding gene in Arabidopsis thaliana. Gene. 1995 May 19;157(1-2):269–272. doi: 10.1016/0378-1119(95)00068-h. [DOI] [PubMed] [Google Scholar]
  26. Oakeley E. J., Jost J. P. Non-symmetrical cytosine methylation in tobacco pollen DNA. Plant Mol Biol. 1996 Jul;31(4):927–930. doi: 10.1007/BF00019481. [DOI] [PubMed] [Google Scholar]
  27. Pinarbasi E., Elliott J., Hornby D. P. Activation of a yeast pseudo DNA methyltransferase by deletion of a single amino acid. J Mol Biol. 1996 Apr 12;257(4):804–813. doi: 10.1006/jmbi.1996.0203. [DOI] [PubMed] [Google Scholar]
  28. Platero J. S., Hartnett T., Eissenberg J. C. Functional analysis of the chromo domain of HP1. EMBO J. 1995 Aug 15;14(16):3977–3986. doi: 10.1002/j.1460-2075.1995.tb00069.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pósfai J., Bhagwat A. S., Pósfai G., Roberts R. J. Predictive motifs derived from cytosine methyltransferases. Nucleic Acids Res. 1989 Apr 11;17(7):2421–2435. doi: 10.1093/nar/17.7.2421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Reinisch K. M., Chen L., Verdine G. L., Lipscomb W. N. The crystal structure of HaeIII methyltransferase convalently complexed to DNA: an extrahelical cytosine and rearranged base pairing. Cell. 1995 Jul 14;82(1):143–153. doi: 10.1016/0092-8674(95)90060-8. [DOI] [PubMed] [Google Scholar]
  31. Riggs A. D., Pfeifer G. P. X-chromosome inactivation and cell memory. Trends Genet. 1992 May;8(5):169–174. doi: 10.1016/0168-9525(92)90219-t. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Rossignol J. L., Faugeron G. MIP: an epigenetic gene silencing process in Ascobolus immersus. Curr Top Microbiol Immunol. 1995;197:179–191. doi: 10.1007/978-3-642-79145-1_12. [DOI] [PubMed] [Google Scholar]
  34. Rychlik W., Rhoads R. E. A computer program for choosing optimal oligonucleotides for filter hybridization, sequencing and in vitro amplification of DNA. Nucleic Acids Res. 1989 Nov 11;17(21):8543–8551. doi: 10.1093/nar/17.21.8543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wilkinson C. R., Bartlett R., Nurse P., Bird A. P. The fission yeast gene pmt1+ encodes a DNA methyltransferase homologue. Nucleic Acids Res. 1995 Jan 25;23(2):203–210. doi: 10.1093/nar/23.2.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wilson G. G., Murray N. E. Restriction and modification systems. Annu Rev Genet. 1991;25:585–627. doi: 10.1146/annurev.ge.25.120191.003101. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES