Dual Role of the Histone Variant H2A.Z in Transcriptional Regulation of Stress-Response Genes

The influence of the histone variant H2A.Z on transcription remains a long-standing conundrum. Here, by analyzing the actin-related protein6 mutant, which is impaired in H2A.Z deposition, and by H2A.Z profiling in stress conditions, we investigated the impact of this histone variant on gene expressi...

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Published in:The Plant cell 2017-04, Vol.29 (4), p.791-807
Main Authors: Sura, Weronika, Kabza, Michał, Karlowski, Wojciech M., Bieluszewski, Tomasz, Kus-Slowinska, Marta, Pawełoszek, Łukasz, Sadowski, Jan, Ziolkowski, Piotr A.
Format: Article
Language:English
Subjects:
Actin
Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Arabidopsis thaliana
Drought
Droughts
Gene expression
Gene regulation
Genes
Histones - genetics
Histones - metabolism
Nucleosomes
Nucleosomes - genetics
Nucleosomes - metabolism
Osmotic stress
Promoter Regions, Genetic - genetics
Promoter Regions, Genetic - physiology
Stress
Stresses
Transcription activation
Transcription Initiation Site - physiology
Transcriptional Activation - genetics
Transcriptional Activation - physiology
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Summary:The influence of the histone variant H2A.Z on transcription remains a long-standing conundrum. Here, by analyzing the actin-related protein6 mutant, which is impaired in H2A.Z deposition, and by H2A.Z profiling in stress conditions, we investigated the impact of this histone variant on gene expression in Arabidopsis thaliana. We demonstrate that the arp6 mutant exhibits anomalies in response to osmotic stress. Indeed, stress-responsive genes are overrepresented among those hyperactive in arp6. In wild-type plants, these genes exhibit high levels of H2A.Z in the gene body. Furthermore, we observed that in droughtresponsive genes, levels of H2A.Z in the gene body correlate with transcript levels. H2A.Z occupancy, but not distribution, changes in parallel with transcriptional changes. In particular, we observed H2A.Z loss upon transcriptional activation and H2A.Z gain upon repression. These data suggest that H2A.Z has a repressive role in transcription and counteracts unwanted expression in noninductive conditions. However, reduced activity of some genes in arp6 is associated with distinct behavior of H2A.Z at their +1 nucleosome, which exemplifies the requirement of this histone for transcription. Our data support a model where H2A.Z in gene bodies has a strong repressive effect on transcription, whereas in +1 nucleosomes, it is important for maintaining the activity of some genes.
ISSN:1040-4651
1532-298X
DOI:10.1105/tpc.16.00573