Roles of dynamic and reversible histone acetylation in plant development and polyploidy

Abstract

Transcriptional regulation in eukaryotes is not simply determined by the DNA sequence, but rather mediated through dynamic chromatin modifications and remodeling. Recent studies have shown that reversible and rapid changes in histone acetylation play an essential role in chromatin modification, induce genome-wide and specific changes in gene expression, and affect a variety of biological processes in response to internal and external signals, such as cell differentiation, growth, development, light, temperature, and abiotic and biotic stresses. Moreover, histone acetylation and deacetylation are associated with RNA interference and other chromatin modifications including DNA and histone methylation. The reversible changes in histone acetylation also contribute to cell cycle regulation and epigenetic silencing of rDNA and redundant genes in response to interspecific hybridization and polyploidy.

Fig. 1

Post-translational modifications of core histones and cell cycle control. (A) The modifications include acetylation (Ac, red), methylation (Me, blue), phosphorylation (P in green circle), and ubiquitination (not shown) [13]. In plants, ZmHAT-B has been shown to acetylate specifically lysines (K) 5 and 12 of H4 [27], and the deacetylase ZmRpd3 can specifically deacetylate this distinct acetylation pattern [52,54]. Asterisks indicate plant-specific acetylation of H4 lysine 20 and plant-specific methylation of H3 lysines 14, 18, and 23. Histone H3 lysine-9 can be modified by acetylation and methylation in all plant species investigated. Specific sites of histone acetylation (+Ac) and deacetylation (−Ac) that have been characterized in plants are listed under the histone acetyltransferases and deacetylases, respectively. (B) Histones (marked as H in blue oval circle) are acetylated by type B HAT (e.g., ZmHAT-B) in cytoplasm and transported into nucleus for chromatin assembly. A small circular dashed line indicates the nuclear membrane. Each nucleosome (blue) is wrapped with a DNA strand (black line). The acetylated histones (with HAT in pink circles and Ac in small red circles) are associated with relaxed chromatin and can be subsequently modified by histone deacetylases (HDs, in yellow circles) (e.g., AtHD1 and ZmHDA101, below the arrows) to form condensed chromatin. Acetylation by type A or GCN5-like HATs (e.g., AtGCN5 and ZmGCN5, above the arrows) may revert the condensed chromatin to a relaxed form. ZmHAT-B is localized in nucleus as well as cytoplasm and may possess a function similar to that of type A HATs. Different acetylation patterns (e.g., H4K5Ac and H4K8Ac) and chromatin status may result in reversible changes in gene expression and alternate during cell cycle progression as discussed in the text.

Fig. 2

Model of how changes in environmental cues, developmental programs, and genome composition (e.g., polyploidy) induce molecular cascades that can lead to alteration of chromatin structure via histone modifications (acetylation in red circle and methylation in orange circles) and DNA methylation. Locus-specific changes in histone acetylation are mediated by the interactions between signal molecules and transcriptional activators or repressors and HATs or HDs, respectively. The relationships among histone modifications and DNA methylation are interactive and circular. The histone acetylation status works in combination with histone methylation and DNA methylation to maintain a relatively stable structure of chromatin-mediated gene repression. RNA interference (in red open circle) by short interfering RNAs, (siRNAs) may establish and reinforce heterochromatin formation via DNA methylation and histone methylation [142]. As a result, changes in DNA methylation and histone acetylation or histone methylation facilitate proper expression of target genes in response to light, temperatures, abiotic and biotic stresses, and polyploidy. There is also evidence for physiologically or stress-induced changes in DNA recombination and gene expression (dashed lines) [154,155], which may suggest epigenetic inheritance of induced memory. Dashed arrows indicate that the connections may be established with additional experimental data. ABA: abscisic acid; JA: jasmonic acid; HAT: histone acetyltransferase; HD (HDA, HDT): histone deacetylase; HDM: histone demethylase; HMT: histone methyltransferase; KYP: KRYPTONITE, a histone methyltransferase; DIM5: a SET domain protein for histone methyltransferase; MET1: DNA methyltransferase 1; DDM1: a SWI2/SNF2 chromatin protein affecting DNA methylation; MBD: methyl-binding domain; and MeCP: methyl CpG binding protein.