Abstract
Cells have the ability to sense, respond and adapt to environmental fluctuations. Stress causes a massive reorganization of the transcriptional program. Many examples of histone post-translational modifications (PTMs) have been associated with transcriptional activation or repression under steady-state growth conditions. Comparatively less is known about the role of histone PTMs in the cellular adaptive response to stress. Here, we performed high-throughput genetic screenings that provide a novel global map of the histone residues required for transcriptional reprogramming in response to heat and osmotic stress. Of note, we observed that the histone residues needed depend on the type of gene and/or stress, thereby suggesting a ‘personalized’, rather than general, subset of histone requirements for each chromatin context. In addition, we identified a number of new residues that unexpectedly serve to regulate transcription. As a proof of concept, we characterized the function of the histone residues H4-S47 and H4-T30 in response to osmotic and heat stress, respectively. Our results uncover novel roles for the kinases Cla4 and Ste20, yeast homologs of the mammalian PAK2 family, and the Ste11 MAPK as regulators of H4-S47 and H4-T30, respectively. This study provides new insights into the role of histone residues in transcriptional regulation under stress conditions.
Highlights
IntroductionIn this context, the regulation of gene expression is one of the most important cell responses to achieve rapid adaptation to stress [1,2]
To quantify the transcriptional output induced by stress, we used a reporter system based on quadruple Venus fluorescent protein expressed under the control of three specific stressresponsive promoters dependent on different transcription factors: ALD3, induced in response to heat and osmostress and regulated by Msn2/4 transcription factors; HSP82, induced in response to heat stress and controlled by Hsf1; and STL1, induced in response to osmostress and regulated by Hot1 and Sko1 [8,9,47]
Histone post-translational modifications (PTMs) play a crucial role in regulating gene expression, thereby facilitating such transcriptional reprogramming [20,32,60,61]
Summary
In this context, the regulation of gene expression is one of the most important cell responses to achieve rapid adaptation to stress [1,2]. Transcriptome changes have common features, some aspects of the response triggered by specific transcription factors are unique to each individual stress [7,8,9]. Several layers of regulatory elements control such dynamic response, from the combinatorial network of transcription factors binding [8,9] to the activity of specific chromatin remodelers, which shape the duration and intensity of the transcriptional response (e.g. SWI/SNF, RSC and SAGA) [11,14,15,17] or attenuate it (INO80 and ISWI) [12,18], according to the cellular requirements
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