Abstract
The chromosomal distribution of seven histone methylation marks (H3K4me2, H3K9me1,2,3 and H3K27me1,2,3) was analysed in the gymnosperm species Pinus sylvestris and Picea abies. Similarly to the situation in other investigated eukaryotes, dimethylation of lysine 4 of histone H3 is restricted to euchromatin in gymnosperms. Surprisingly, also H3K9me1—a mark classified as heterochromatin-specific in angiosperms—labels the euchromatin in P. sylvestris and P. abies. The other investigated methylation marks are either equally distributed along the chromosomes, as H3K9me2 and H3K27me1 (in both species) and H3K9me3 (in P. abies), or enriched at specific types of heterochromatin, as H3K9me3 (in P. sylvestris) and H3K27me2 and H3K27me3 in both species. Although the methylation marks themselves are apparently conserved, their functional specificity within the frame of the ‘epigenetic code’ might have diverged during evolution.
Similar content being viewed by others
References
Bennett MD, Leitch IJ (2004) Angiosperm DNA C-values database (release 5.0, Dec. 2004) http://www.kew.org/cvalues/homepage.html. Accessed 11.07.08.
Bogunic F, Muratovic E, Brown SC, Siljak-Yakovlev S (2003) Genome size and base composition of five Pinus species from the Balkan region. Plant Cell Rep 22: 59–63.
Brown GR, Newton CH, Carlson JE (1998) Organization and distribution of a Sau3A tandem repeated DNA sequence in Picea (Pinaceae) species. Genome 41: 560–565.
Carchilan M, Delgado M, Ribeiro T et al. (2007) Transcriptionally active heterochromatin in rye B chromosomes. Plant Cell 19: 1738–1749.
Dhillon SS (1987) DNA in tree species. In: Bonga JM, Durzan DJ, eds. Cell and Tissue Culture in Forestry. Marinus Nijhoff, pp. 289–296.
Ebert A, Schotta G, Lein S et al. (2004) Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. Genes Dev 18: 2973–2983.
Ebert A, Lein S, Schotta G, Reuter G (2006) Histone modification and the control of heterochromatic gene silencing in Drosophila. Chromosome Res 14: 377–392.
Fuchs J, Schubert I (2008) Chromosomal distribution and functional interpretation of epigenetic histone marks in plants. In: Bass H, Birchler JA, eds. Plant Cytogenetics, Vol. 1: Genome Structure and Chromosome Function. Springer-Verlag, in press.
Fuchs J, Brandes A, Schubert I (1995) Telomere sequence localization and karyotype evolution in higher-plants. Plant Syst Evol 196: 227–241.
Fuchs J, Demidov D, Houben A, Schubert I (2006) Chromosomal histone modification patterns—from conservation to diversity. Trends Plant Sci 11: 199–208.
Galbraith DW, Harkins RK, Maddox MJ, Ayres MN, Sharma PD, Firoozabady E (1983) Rapid flow cytometry analysis of the cell cycle in intact plant tissues. Science 220: 1049–1051.
Greilhuber J (1986) Severely distorted Feulgen-DNA amounts in Pinus (Coniferophytina) after nonadditive fixations as a result of meristematic self-tanning with vacuole contents. Can J Genet Cytol 28: 409–415.
Heard E (2005) Delving into the diversity of facultative heterochromatin: the epigenetics of the inactive X chromosome. Curr Opin Genet Dev 15: 482–489.
Hizume M (1988) Karyomorphological studies in the family Pinaceae. Mem Fac Educ Ehime Univ Nat Sci 8: 1–108.
Hizume M, Shibata F, Matsusaki Y, Garajova Z (2002) Chromosome identification and comparative karyotypic analyses of four Pinus species. Theor Appl Genet 105: 491–497.
Houben A, Demidov D, Gernand D, Meister A, Leach CR, Schubert I (2003) Methylation of histone H3 in euchromatin of plant chromosomes depends on basic nuclear DNA content. Plant J 33: 967–973.
Jackson JP, Johnson L, Jasencakova Z et al. (2004) Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112: 308–315.
Jasencakova Z, Soppe WJ, Meister A, Gernand D, Turner BM, Schubert I (2003) Histone modifications in Arabidopsis—high methylation of H3 lysine 9 is dispensable for constitutive heterochromatin. Plant J 33: 471–480.
Joyner KL, Wang, X-R, Johnston, JS, Price HJ, Williams CG (2001) DNA content for Asian pines parallels New World relatives. Can J Bot 79: 192–196.
Kamm A, Doudrick RL, Heslop-Harrison JS, Schmidt T (1996) The genomic and physical organization of Ty1-copia-like sequences as a component of large genomes in Pinus elliottii var. elliottii and other gymnosperms. Proc Natl Acad Sci U S A 93: 2708–2713.
Lachner M, Sengupta R, Schotta G, Jenuwein T (2004) Trilogies of histone lysine methylation as epigenetic landmarks of the eukaryotic genome. Cold Spring Harb Symp Quant Biol 69: 209–218.
Lindroth AM, Shultis D, Jasencakova Z et al. (2004) Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J 23: 4286–4296.
Loidl P (2004) A plant dialect of the histone language. Trends Plant Sci 9: 84–90.
Lubaretz O, Fuchs J, Ahne R, Meister A, Schubert I (1996) Karyotyping of three Pinaceae species via fluorescent in situ hybridization and computer-aided chromosome analysis. Theor Appl Genet 92: 411–416.
Lysak M, Fransz P, Schubert I (2006) Cytogenetic analyses of Arabidopsis. Methods Mol Biol 323: 173–186.
Marschner S, Kumke K, Houben A (2007) B chromosomes of B. dichromosomatica show a reduced level of euchromatic histone H3 methylation marks. Chromosome Res 15: 215–222.
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.
Naumann K, Fischer A, Hofmann I et al. (2005) Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis. EMBO J 24: 1418–1429.
Noma K, Allis CD, Grewal SI (2001) Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293: 1150–1155.
Peters AH, Kubicek S, Mechtler K et al. (2003) Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 12: 1577–1589.
Rice JC, Briggs SD, Ueberheide B et al. (2003) Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol Cell 12: 1591–1598.
Schmidt A, Doudrick RL, Heslop-Harrison JS, Schmidt T (2000) The contribution of short repeats of low sequence complexity to large conifer genomes. Theor Appl Genet 101: 7–14.
Schotta G, Lachner M, Sarma K et al. (2004) A silencing pathway to induce H3–K9 and H4–K20 trimethylation at constitutive heterochromatin. Genes Dev 18: 1251–1262.
Shi J, Dawe RK (2006) Partitioning of the maize epigenome by the number of methyl groups on histone H3 lysines 9 and 27. Genetics 173: 1571–1583.
Siljak-Yakovlev S, Cerbah M, Coulaud J et al. (2002) Nuclear DNA content, base composition, heterochromatin and rDNA in Picea omorika and Picea abies. Theor Appl Genet 104: 505–512.
Soppe WJ, Jasencakova Z, Houben A et al. (2002) DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21: 6549–6559.
Tamaru H, Selker EU (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414: 277–283.
Tamaru H, Zhang X, McMillen D et al. (2003) Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet 34: 75–79.
Tariq M, Saze H, Probst AV, Lichota J, Habu Y, Paszkowski J (2003) Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc Natl Acad Sci U S A 100: 8823–8827.
Valkonen JPT, Nygren M, Ylonen A, Mannonen L (1994) Nuclear DNA content of Pinus sylvestris (L.) as determined by laser flow cytometry. Genetica 92: 203–207.
Yamada T, Fischle W, Sugiyama T, Allis CD, Grewal SI (2005) The nucleation and maintenance of heterochromatin by a histone deacetylase in fission yeast. Mol Cell 20: 173–185.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Fuchs, J., Jovtchev, G. & Schubert, I. The chromosomal distribution of histone methylation marks in gymnosperms differs from that of angiosperms. Chromosome Res 16, 891–898 (2008). https://doi.org/10.1007/s10577-008-1252-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10577-008-1252-4