Abstract
Histone H1, a major structural component of chromatin fiber, is believed to act as a general repressor of transcription. To investigate in vivo the role of this protein in transcription regulation during development of a multicellular organism, we made transgenic tobacco plants that overexpress the gene for Arabidopsis histone H1. In all plants that overexpressed H1 the total H1-to-DNA ratio in chromatin increased 2.3-2.8 times compared with the physiological level. This was accompanied by 50-100% decrease of native tobacco H1. The phenotypic changes in H1-overexpressing plants ranged from mild to severe perturbations in morphological appearance and flowering. No correlation was observed between the extent of phenotypic change and the variation in the amount of overexpressed H1 or the presence or absence of the native tobacco H1. However, the severe phenotypic changes were correlated with early occurrence during plant growth of cells with abnormally heterochromatinized nuclei. Such cells occurred considerably later in plants with milder changes. Surprisingly, the ability of cells with highly heterochromatinized nuclei to fulfill basic physiological functions, including differentiation, was not markedly hampered. The results support the suggestion that chromatin structural changes dependent on H1 stoichiometry and on the profile of major H1 variants have limited regulatory effect on the activity of genes that control basal cellular functions. However, the H1-mediated chromatin changes can be of much greater importance for the regulation of genes involved in control of specific developmental programs.
MeSH Terms
Arabidopsis/metabolism
Cell Nucleus/ultrastructure
Chromatin/ultrastructure
DNA, Plant/metabolism
Genes, Plant
Heterochromatin/ultrastructure
Histones/biosynthesis,genetics
Nucleosomes/ultrastructure
Phenotype
Plants, Genetically Modified
Plants, Toxic
Tobacco/growth & development,physiology
Chemicals
Chromatin
DNA, Plant
Heterochromatin
Histones
Nucleosomes
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Prymakowska-Bosak M
Laboratory of Plant Molecular Biology, Warsaw University, Poland.
Przewłoka M R
Iwkiewicz J
Egierszdorff S
Kuraś M
Chaubet N
Gigot C
Spiker S
Jerzmanowski A
References (22)
22 references, click to expand
-
A preference of histone H1 for methylated DNA.
EMBO J. 1996 Apr 1;15(7):1705-14
PMID: 8612595
-
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
Nature. 1970 Aug 15;227(5259):680-5
PMID: 5432063
-
Flanking sequences of Xenopus 5 S RNA genes determine differential inhibition of transcription by H1 histone in vitro. Mitotic phosphorylation of H1 decreases its inhibitory power.
J Biol Chem. 1990 Jun 25;265(18):10726-32
PMID: 2355019
-
Rapid and efficient site-specific mutagenesis without phenotypic selection.
Methods Enzymol. 1987;154:367-82
PMID: 3323813
-
The pFF plasmids: cassettes utilising CaMV sequences for expression of foreign genes in plants.
J Biotechnol. 1990 Jun;14(3-4):333-44
PMID: 1369289
-
The interaction of histone H5 and its globular domain with core particles, depleted chromatosomes, polynucleosomes, and a DNA decamer.
J Biol Chem. 1991 Jan 25;266(3):1502-8
PMID: 1988433
-
Analysis of pre-mRNA processing in transfected plant protoplasts.
Methods Enzymol. 1990;181:148-61
PMID: 1696344
-
Mice develop normally without the H1(0) linker histone.
Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6434-8
PMID: 7604008
-
Linker histones are not essential and affect chromatin condensation in vivo.
Cell. 1995 Jul 14;82(1):47-56
PMID: 7606784
-
Arabidopsis thaliana H1 histones. Analysis of two members of a small gene family.
Eur J Biochem. 1991 Dec 18;202(3):1029-39
PMID: 1765064
-
Low levels of exogenous histone H1 in yeast cause cell death.
Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11567-70
PMID: 7972103
-
Immunoblotting.
Methods Cell Biol. 1993;37:105-17
PMID: 7504778
-
Binary Agrobacterium vectors for plant transformation.
Nucleic Acids Res. 1984 Nov 26;12(22):8711-21
PMID: 6095209
-
Molecular characterization and expression of a tobacco histone H1 cDNA.
Plant Mol Biol. 1995 Feb;27(3):597-605
PMID: 7894022
-
The use of lead citrate at high pH as an electron-opaque stain in electron microscopy.
J Cell Biol. 1963 Apr;17:208-12
PMID: 13986422
-
A modification of the acetic acid-urea system for use in microslab polyacrylamide gel electrophoresis.
Anal Biochem. 1980 Nov 1;108(2):263-5
PMID: 7457868
-
Conserved epitopes on plant H1 histones recognized by monoclonal antibodies.
Eur J Biochem. 1989 Jan 2;178(3):779-87
PMID: 2463917
-
Differential repression of transcription factor binding by histone H1 is regulated by the core histone amino termini.
EMBO J. 1994 Dec 15;13(24):6031-40
PMID: 7813441
-
A simple and general method for transferring genes into plants.
Science. 1985 Mar 8;227(4691):1229-31
PMID: 17757866
-
Histone H1 expressed in Saccharomyces cerevisiae binds to chromatin and affects survival, growth, transcription, and plasmid stability but does not change nucleosomal spacing.
Mol Cell Biol. 1994 Apr;14(4):2822-35
PMID: 8139579
-
Mechanisms of heritable gene repression during development of Drosophila.
Curr Opin Cell Biol. 1993 Dec;5(6):999-1005
PMID: 7907493
-
Replacement of histone H1 by H5 in vivo does not change the nucleosome repeat length of chromatin but increases its stability.
EMBO J. 1990 May;9(5):1651-8
PMID: 2328730