Contribution of the histone variant H2A.Z to expression of responsive genes in plants

Abstract

The histone variant H2A.Z plays a critical role in chromatin-based processes such as transcription, replication, and repair in eukaryotes. Although many H2A.Z-associated processes and features are conserved in plants and animals, a distinguishing feature of plant chromatin is the enrichment of H2A.Z in the bodies of genes that exhibit dynamic expression, particularly in response to differentiation and the environment. Recent work sheds new light on the plant machinery that enables dynamic changes in H2A.Z enrichment and identifies additional chromatin-based pathways that contribute to transcriptional properties of H2A.Z-enriched chromatin. In particular, analysis of a variety of responsive loci reveals a repressive role for H2A.Z in expression of responsive genes and identifies roles for SWR1 and INO80 chromatin remodelers in enabling dynamic regulation of H2A.Z levels and transcription. These studies lay the groundwork for understanding how this ancient histone variant is harnessed by plants to enable responsive and dynamic gene expression (Graphical Abstract).

Keywords: Chromatin; H2A.Z; H3K27me3; INO80 subfamily of remodelers; Stress response; Transcriptional repression.

Figure 1:. Identification of the subunits of the plant SWR1 complex reveals multiple opportunities for functional and/or biochemical interactions.

A) 11 subunits of the plant SWR1 complex are conserved in yeast and animals. The ovals are assigned different colors based on identified role(s) for the subunits. Blue indicates core subunits of the remodeling complex. Green subunits are shared between SAGA and SWR1 complexes. Subunits that are present in both INO80 and SWR1 complexes are indicated by orange. The two subunits that are associated all three complexes (SWR1, INO80, and SAGA) are indicated by ovals that are colored green and orange. The H2A.Z/H2B dimer is depicted as a purple octagon. B) A number of plant-specific components of the SWR1 complex have been identified in Arabidopsis that expand opportunities for functional crosstalk and recruitment of SWR1, as indicated. The dashed lines around CHR11/17 denote identification of this interaction by only one of three groups, as described in the text. Double-headed arrows denote interactions between subunits of SWR1 whereas single-headed arrows denote interactions/activities identified for specific subunits.

Figure 2:. H2A.Z-enriched chromatin is also associated with transcriptionally repressive histone modifications promoted by PRC1 and PRC2.

The PRC1 component BMI1 promotes ubiquitylation of H2A.Z (b) and ChIP-seq and genetic analyses suggest that H2A.Z nucleosomes can also be modified by PRC2 to promote H3K27me3 (c). Analysis of RNA-seq and ChIP-seq data raise the possibility (dashed line) that all three epigenetic marks may be present at some loci (d). These three modification states and unmodified nucleosomes incorporating H2A.Z (a) are linked to transcriptional repression.

Figure 3:. The presence of H2A.Z enables transcriptional regulation of stress-responsive loci.

Both drought-responsive and heat shock-responsive loci have been identified at which H2A.Z is present at the locus, necessary for transcriptional repression of the locus, and relative depletion of H2A.Z at the locus is associated with expression [31, 94] (top). In addition, numerous loci for which expression is strongly induced by drought stress that are also enriched for H2A.Z prior to induction [31] (bottom). Given that the presence of H2A.Z at a locus does not appear to be sufficient to confer repression, nucleosomes are outlined in red or green to indicate expression status of the locus (repressed and active respectively) which may reflect additional modifications of chromatin (see Conclusions). Observation of relatively reduced enrichment of H2A.Z in nucleosomes at loci in a given stress-dependent transcriptional response is indicated by purple and blue stripes.

Figure 4:. SWR1 and INO80 complexes contribute to altered levels of H2A.Z at distinct light-responsive loci.

Light-responsive loci have been identified at which the SWR1 remodeling complex promotes incorporation of H2A.Z and transcriptional repression in response to light and for which recruitment of the complex is likely directly mediated by transcription factors (ELF3 and HY5) [97, 99] (top). Similarly, other responsive loci have been identified in which recruitment of the INO80 remodeling complex by a PIF transcription factor (e.g. PIF4 or PIF7) facilitates depletion of H2A.Z and transcriptional activation [66, 103] (bottom). Observation of relatively reduced enrichment of H2A.Z in nucleosomes at loci in a given stress-dependent transcriptional response is indicated by purple and blue stripes. TSS denotes transcription start site.