Skip to main content
SpringerLink
Log in

Existence of two histone H3 variants in dicotyledonous plants and correlation between their acetylation and plant genome size

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Histone H3 proteins were purified to near homogeneity from callus cultures of dicotyledonous plants alfalfa, soybean, Arabidopsis, carrot and tobacco to determine the number of histone H3 variants. In every species two histone H3 variants were identified by gradient gel electrophoresis and reversed-phase chromatography. They were named H3.1 and H3.2 in order of increasing mobility in acid-urea-Triton gels. Co-electrophoresis of histone H3.2 proteins of all species in this gel system and HPLC cochromatography suggest that all histone H3.2 variants have a primary protein sequence identical to alfalfa H3.2. Two distinct H3.1 variant forms were identified, represented by alfalfa. and Arabidopsis H3.1 proteins which differ only at residue 90. Soybean H3.1 resembles H3.1 of alfalfa. Carrot and tobacco H3.1 appear identical to the Arabidopsis H3.1 histone variant. All H3 proteins were acetylated to multiple levels and in each plant the histone H3.2 forms were more highly acetylated. An inverse relationship was observed between plant genome size and the relative abundance of histone variant H3.2 and also with the level of acetylation of both histone H3 variants. This correlation matches the general tendency that in plants with smaller genomes a larger fraction of the genome is transcriptionally active.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Aleporou-Marinou V, Sekeri-Pataryas KT, Pataryas TA: Histone variants in diptera during metamorphosis. Comp Biochem Physiol B 88: 1027–1032 (1987).

    Google Scholar 

  2. Bennett MD, Smith JB: Nuclear DNA amounts in angiosperms. Phil Trans Roy Soc B 274: 227–274 (1976).

    Google Scholar 

  3. Chaboute ME, Chaubet N, Philipps G, Ehling M, Gigot C. Genomic organization and nucleotide sequences of two histone H3 and two histone H4 genes of Arabidopsis thaliana. Plant Mol Biol 8: 179–191 (1987).

    Google Scholar 

  4. Gabrielli F: Human histone variants. In: Hnilica LS, Stein GS, Stein IL (eds) Histones and Other Basic Proteins, pp. 4–16. CRC Press, Boca Raton, FL (1990).

    Google Scholar 

  5. Guzman P, Ecker JR: Development of large DNA methods for plants: molecular cloning of large segments of Arabidopsis and carrot DNA into yeast. Nucl Acids Res 16: 11091–11105 (1988).

    Google Scholar 

  6. Hayashi T, Hayashi H, Fusauchi Y, Iwai K: Tetrahymena histone H3. Purification and two variant sequences. J Biochem (Tokyo) 95: 1741–1749 (1984).

    Google Scholar 

  7. Hebbes TR, Thorne AW, Crane-Robinson C: A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J 7: 1395–1402 (1988).

    Google Scholar 

  8. Imschenetzky M, Puchi M, Massone R, Zepeda P, Inostroza D, Vega I: Characterization of histones from plutei larvae of the sea urchin Tetrapygus niger. Comp Biochem Physiol 94: 241–244 (1989).

    Google Scholar 

  9. Jackson V: In vivo studies on the dynamics of histone-DNA interaction. Evidence for nucleosome dissolution during replication and transcription and a low level of dissolution independent of both. Biochemistry 29: 719–731 (1990).

    Google Scholar 

  10. Kapros T, Bogre L, Nemeth K, Bako L, Gyorgyey J, Wu SC, Dudits D: Differential expression of histone H3 gene variants during cell cycle and somatic embryogenesis in alfalfa. Plant Physiol, in press.

  11. Karpenchuk KG, Klimyuk VI: Identification of plant histones by non-ionic detergent binding evolutionary argument. Mol Biol (Moscow) 21: 981–991 (1987).

    Google Scholar 

  12. Klyszejko-Stefanowicz L, Krajewska WM, Lipinska A: Histone occurrence, isolation, characterization, and biosynthesis. In: Hnilica LS, Stein GS, Stein JL (eds) Histones and Other Basic Proteins, pp. 269–317. CRC Press, Boca Raton, FL (1990).

    Google Scholar 

  13. Marzluff WF: Histone gene expression not coupled to DNA synthesis. In: Hnilica LS, Stein GS, Stein JL (eds) Histones and Other Basic Proteins, pp. 319–329. CRC Press, Boca Raton, FL (1990).

    Google Scholar 

  14. Matthews HR, Waterborg JH: Reversible modifications of nuclear proteins and their significance. In: Freedman RB, Hawkins HC (eds) The Enzymology of Post-Translational Modification of Proteins, vol 2, pp. 125–185. Academic Press, London (1985).

    Google Scholar 

  15. Meyerowitz EM, Pruitt RE. Arabidopsis thaliana and plant molecular genetics. Science 229: 1214–1218 (1985).

    Google Scholar 

  16. Moehs CP, McElwain EF, Spiker S: Chromosomal proteins of Arabidopsis thaliana. Plant Mol Biol 11: 507–516 (1988).

    Google Scholar 

  17. Nagl W: Nuclear chromatin. In: Parthier B, Boulter D (eds) Nucleic Acids and Proteins in Plants II, vol 14B, pp. 1–45. Springer-Verlag, Berlin (1982).

    Google Scholar 

  18. Old RW, Woodland HR: Histone genes: not so simple after all. Cell 38: 624–626 (1984).

    Google Scholar 

  19. Pfaffle PK, Gerlach V, Bunzel L, Jackson VE: In vitro evidence that transcription-induced stress causes nucleosome dissolution and regeneration. J Biol Chem 265: 16830–16840 (1990).

    Google Scholar 

  20. Pfeffer U, Ferrari N, Tosetti F, Vidali G: Histone hyperacetylation is induced in chick erythrocyte nuclei during reactivation in heterokaryons. Exptl Cell Res 178: 25–30 (1988).

    Google Scholar 

  21. Pfeffer U, Ferrari N, Tosetti F, Vidali G: Histone acetylation in conjugating Tetrahymena thermophila. J Cell Biol 109: 1007–1014 (1989).

    Google Scholar 

  22. Rodrigo MI, Franco L: Histone variants from pea (Pisum sativum): Their differential presence in fractions obtained by DNase I digestion of nuclei. Physiol Plant 78: 602–608 (1990).

    Google Scholar 

  23. Schwager SLU, Brandt WF, Von Holt C: The isolation of isohistones by preparative gel electrophoresis from embryos of the sea urchin Parechinus angulosus. Biochim Biophys Acta 741: 315–321 (1983).

    Google Scholar 

  24. Turner BM, Fellows G: Specific antibodies reveal ordered and cell-cycle-related use of histone H4 acetylation sites in mammalian cells. Eur J Biochem 179: 131–139 (1989).

    Google Scholar 

  25. Vanfleteren JR, van Bun SM, van Beeumen JJ: The primary structure of histone H3 from the nematode Caenorhabditis elegans. FEBS Lett 211: 59–63 (1987).

    Google Scholar 

  26. Vanfleteren JR, van Bun SM, van Beeumen JJ: The histones of Caenorhabditis elegans. No evidence of stage specific isoforms. An overview. FEBS Lett 257: 233–237 (1989).

    Google Scholar 

  27. Waterborg JH, Winicov I, Harrington RE: Histone variants and acetylated species from the alfalfa plant Medicago sativa. Arch Biochem Biophys 256: 167–178 (1987).

    Google Scholar 

  28. Waterborg JH, Harrington RE, Winicov I: Differential histone acetylation in alfalfa (Medicago sativa) due to growth in NaCl. Plant Physiol 90: 237–245 (1989).

    Google Scholar 

  29. Waterborg JH, Harrington RE, Winicov I: Dynamic histone acetylation in alfalfa cells. Butyrate interference with acetate labeling. Biochim Biophys Acta 1049: 324–330 (1990).

    Google Scholar 

  30. Waterborg JH: Sequence analysis of acetylation and methylation in two histone H3 variants of alfalfa. J Biol Chem 265: 17157–17161 (1990).

    Google Scholar 

  31. Waterborg JH: Multiplicity of histone H3 variants in wheat, barley, rice, and maize. Plant Physiol 96: 453–458 (1991).

    Google Scholar 

  32. Wells D, McBride C: A comprehensive compilation and alignment of histones and histone genes. Nucl Acids Res 17: R311-R346 (1989).

    Google Scholar 

  33. Winicov I, Maki DH, Waterborg JH, Riehm MR, Harrington RE: Characterization of the alfalfa (Medicago sativa) genome by DNA reassociation. Plant Mol Biol 10: 369–371 (1988).

    Google Scholar 

  34. Wu RS, Panusz HT, Hatch CL, Bonner WM: Histones and their modifications. CRC Crit Rev Biochem 20: 201–263 (1986).

    Google Scholar 

  35. Wu SC, Gyorgyey J, Dudits D: Polyadenylated H3 histone transcripts and H3 histone variants in alfalfa. Nucl Acids Res 17: 3057–3063 (1989).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Cell Biology and Biophysics, School of Basic Life Sciences, University of Missouri-Kansas City, 5100 Rockhill Road, 64110-2499, Kansas City, MO, USA

    Jakob H. Waterborg

Authors
  1. Jakob H. Waterborg
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Waterborg, J.H. Existence of two histone H3 variants in dicotyledonous plants and correlation between their acetylation and plant genome size. Plant Mol Biol 18, 181–187 (1992). https://doi.org/10.1007/BF00034947

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00034947

Key words

Search

Navigation