Dual Role of the Histone Variant H2A.Z in Transcriptional Regulation

RESEARCH ARTICLE 1 Dual Role of the Histone Variant H2A.Z in Transcriptional Regulation 2 of Stress-Response Genes 3 4 Weronika Sura, Michał Kabza, Wojciech M. Karlowski, Tomasz Bieluszewski, Marta 5 Kuś-Slowinska, Łukasz Pawełoszek†, Jan Sadowski and Piotr A. Ziolkowski* 6 7 1 Department of Biotechnology, Adam Mickiewicz University, Poznan, Poland 8 2 Department of Bioinformatics, Adam Mickiewicz University, Poznan, Poland 9 3 Department of Computational Biology, Adam Mickiewicz University, Poznan, Poland 10 † Deceased 8 March 2012 11 * Corresponding author: [email protected] 12 13 Short title: Changes of H2A.Z levels in stress response 14 One-sentence summary: H2A.Z is removed from nucleosomes localized in genes upon 15 transcriptional activation in response to drought stress conditions in Arabidopsis thaliana. 16 17 The author responsible for distribution of materials integral to the findings presented in this 18 article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) 19 is: Weronika Sura ([email protected]). 20 21 ABSTRACT 22 The influence of the histone variant H2A.Z on transcription remains a long-standing 23 conundrum. Here, by analyzing the actin-related protein6 mutant, which is impaired in 24 H2A.Z deposition, and by H2A.Z profiling in stress conditions, we investigated the 25 impact of this histone variant on gene expression in Arabidopsis thaliana. We 26 demonstrate that the arp6 mutant exhibits anomalies in response to osmotic stress. 27 Indeed, stress-responsive genes are overrepresented amongst those hyperactive in 28 arp6. In wild-type plants, these genes exhibit high levels of H2A.Z in the gene body. 29 Furthermore, we observed that in drought-responsive genes, levels of H2A.Z in the gene 30 body correlate with transcript levels. H2A.Z occupancy, but not distribution, changes in 31 parallel with transcriptional changes. In particular, we observed H2A.Z loss upon 32 transcriptional activation and H2A.Z gain upon repression. This data suggest that H2A.Z 33 has a repressive role in transcription and counteracts unwanted expression in non34 inductive conditions. However, reduced activity of some genes in arp6 is associated with 35 distinct behavior of H2A.Z at their +1 nucleosome, which exemplifies the requirement of 36 this histone for transcription. Our data support a model where H2A.Z in gene bodies has 37 a strong repressive effect on transcription, whereas in +1 nucleosomes it is important for 38 maintaining the activity of some genes. 39 40 4