Review
Chromatin remodeling in plants

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Abstract

In the past two years, a variety of forward genetic screens have revealed predicted plant chromatin remodeling components that are involved in either differential histone acetylation or ATP-dependent SWI2/SNF2-related complexes. Combined with the results of recent reverse genetic studies, these findings have begun to provide the groundwork for determining the function of chromatin-based control in plants.

Introduction

The phrase ‘chromatin remodeling’ is commonly used as a catchall to describe the reconfiguration of protein–DNA interactions that accompany or potentiate changes in genomic activity (e.g. gene expression or recombination) [1]. Chromatin remodeling encompasses a diverse array of mechanisms, which are beginning to be defined—largely through genetic and biochemical studies in fungi and animals (see 2., 3.). In this review, we explore recent work in plants concerning two of the best-understood chromatin remodeling mechanisms: first, differential core histone acetylation, and second, the action of ATP-hydrolyzing protein complexes. In addition, we discuss the interaction of chromatin remodeling and cytosine methylation, the most basic level of modification superimposed on eukaryotic genomes as epigenetic information. In the process, we consider the novel contributions of both forward and reverse genetics studies in plants connecting chromatin remodeling to gene silencing and development.

Section snippets

Plant chromatin

Plant chromatin organization closely resembles that of other organisms, being based upon the packaging of approximately 145 base pairs of DNA into core nucleosomes. Like many multicellular eukaryotes, plants express a diverse repertoire of genes encoding the core histones H2A, H2B, H3 and H4 (e.g. Arabidopsis has 45 core histone genes; URL http://www.chromdb.org), as well as multiple linker histones. The positions of nucleosomes surrounding the upstream regions of particular plant genes, and

Plant histone acetylation

Core histones are subject to post-translational modifications, including acetylation, phosphorylation, and methylation [10]. The most-studied histone modification is the acetylation of conserved lysine residues, primarily in their amino-terminal tails. Histone acetylation levels are determined by the competing action of histone acetyltransferases (HAT or HAC) and histone deacetylases (HDAs). Elevated acetylation of lysines in the core histone tails is often associated with increased gene

ATP-dependent chromatin remodeling in plants

An alphabet soup of chromatin remodeling machines capable of disrupting and reordering nucleosome–DNA interactions has been biochemically defined in Drosophila, yeast and mammalian cells (e.g. SWITCH [SWI]/SUCROSE NON-FERMENTING [SNF], CHRAC [chromatin accessibility complex], and NURF [nucleosome remodeling factor]) [2]. The engines of these remodeling machines are DNA-dependent ATPases in the SWI2/SNF2 superfamily 34., 35.. In many cases, the chromatin remodeling machines function as

Interactions between chromatin remodeling and DNA methylation

Methylation of cytosine residues has been implicated in the control or reinforcement of epigenetic gene expression states for a number of years. The mechanisms by which DNA methylation can influence gene expression are now becoming clearer through recent work connecting cytosine methylation and chromatin remodeling [50]. An important breakthrough was the demonstration that mammalian methylcytosine-binding proteins can recruit histone deacetylase complexes 51., 52., 53., 54., 55.. In this way,

Conclusions

This brief review touches upon emerging areas in the study of chromatin remodeling in plants. Although the biochemistry of plant chromatin remodeling remains in its infancy, an expanding set of chromatin modification mutants promises to make plants important experimental systems for the study of chromatin-mediated regulation at the whole-organism level. In addition, plants offer a diverse palette of epigenetic phenomena and developmental plasticity with which to gauge the effects of

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

References (64)

  • J.D. Aalfs et al.

    What does ‘chromatin remodeling’ mean?

    Trends Biochem Sci

    (2000)
  • C.J. Fry et al.

    Chromatin remodeling enzymes: who's on first?

    Curr Biol

    (2001)
  • K. Havas et al.

    ATP-dependent chromatin remodeling activities

    Cell Mol Life Sci

    (2001)
  • A.L. Paul et al.

    Permeabilized Arabidopsis protoplasts provide new insight into the chromatin structure of plant alcohol dehydrogenase genes

    Dev Genet

    (1998)
  • G. Li et al.

    Chromatin structure and phaseolin gene regulation

    Plant Mol Biol

    (2001)
  • J. Goodrich et al.

    A Polycomb-group gene regulates homeotic gene expression in Arabidopsis

    Nature

    (1997)
  • C. Spillane et al.

    Interaction of the Arabidopsis polycomb group proteins FIE and MEA mediates their common phenotypes

    Curr Biol

    (2000)
  • M. Luo et al.

    Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds

    Proc Natl Acad Sci USA

    (2000)
  • R. Yadegari et al.

    Mutations in the FIE and MEA genes that encode interacting polycomb proteins cause parent-of-origin effects on seed development by distinct mechanisms

    Plant Cell

    (2000)
  • A.P. Wolffe et al.

    Chromatin disruption and modification

    Nucleic Acids Res

    (1999)
  • J. Wu et al.

    25 years after the nucleosome model: chromatin modifications

    Trends Biochem Sci

    (2000)
  • B.E. Bernstein et al.

    Genome wide studies of histone deacetylase function in yeast

    Proc Natl Acad Sci USA

    (2000)
  • K. Luger et al.

    Crystal structure of the nucleosome core particle at 2.8 Å resolution

    Nature

    (1997)
  • A. Lusser et al.

    Histone acetylation: lessons from the plant kingdom

    Trends Plant Sci

    (2001)
  • G. Brosch et al.

    Inhibition of maize histone deacetylases by HC toxin, the host-selective toxin of Cochliobolus carbonum

    Plant Cell

    (1995)
  • Z.J. Chen et al.

    Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance

    Genes Dev

    (1997)
  • J.P. Murphy et al.

    Histone deacetylase inhibitors and cell proliferation in pea root meristems

    Phytochemistry

    (2000)
  • A. Lusser et al.

    Identification of maize histone deacetylase HD2 as an acidic nucleolar phosphoprotein

    Science

    (1997)
  • E.J. Stockinger et al.

    Transcriptional adaptor and histone acetyltransferase proteins in Arabidopsis and their interactions with CBF1, a transcriptional activator involved in cold-regulated gene expression

    Nucleic Acids Res

    (2001)
  • L. Bordoli et al.

    Plant orthologs of p300/CBP: conservation of a core domain in metazoan p300/CBP acetyltransferase-related proteins

    Nucleic Acids Res

    (2001)
  • Z. Jasencakova et al.

    Histone H4 acetylation of euchromatin and heterochromatin is cell cycle dependent and correlated with replication rather than with transcription

    Plant Cell

    (2000)
  • Z. Jasencakova et al.

    Chromatin organization and its relation to replication and histone acetylation during the cell cycle in barley

    Chromosoma

    (2001)
  • A. Lusser et al.

    Analysis of the histone acetyltransferase B complex of maize embryos

    Nucleic Acids Res

    (1999)
  • K. Wu et al.

    Functional analysis of HD2 histone deacetylase homologues in Arabidopsis thaliana

    Plant J

    (2000)
  • K. Wu et al.

    Functional analysis of a RPD3 histone deacetylase homologue in Arabidopsis thaliana

    Plant Mol Biol

    (2000)
  • L. Tian et al.

    Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development

    Proc Natl Acad Sci USA

    (2001)
  • J. Murfett et al.

    Identification of Arabidopsis histone deacetylase HDA6 mutants that affect transgene expression

    Plant Cell

    (2001)
  • E.J. Finnegan et al.

    Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development

    Proc Natl Acad Sci USA

    (1996)
  • T. Kakutani et al.

    Developmental abnormalities and epimutations associated with DNA hypomethylation mutations

    Proc Natl Acad Sci USA

    (1996)
  • M.J. Ronemus et al.

    Demethylation-induced developmental pleiotropy in Arabidopsis

    Science

    (1996)
  • S.E. Jacobsen et al.

    Ectopic hypermethylation of flower-specific genes in Arabidopsis

    Curr Biol

    (2000)
  • W.J. Soppe et al.

    The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene

    Mol Cell

    (2000)

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