Initiation of the transcriptional response to hyperosmotic shock correlates with the potential for volume recovery

Abstract

The control of activity and localization of transcription factors is critical for appropriate transcriptional responses. In eukaryotes, signal transduction components such as mitogen-activated protein kinase (MAPK) shuttle into the nucleus to activate transcription. It is not known in detail how different amounts of nuclear MAPK over time affect the transcriptional response. In the present study, we aimed to address this issue by studying the high osmolarity glycerol (HOG) system in Saccharomyces cerevisiae. We employed a conditional osmotic system, which changes the period of the MAPK Hog1 signal independent of the initial stress level. We determined the dynamics of the Hog1 nuclear localization and cell volume by single-cell analysis in well-controlled microfluidics systems and compared the responses with the global transcriptional output of cell populations. We discovered that the onset of the initial transcriptional response correlates with the potential of cells for rapid adaptation; cells that are capable of recovering quickly initiate the transcriptional responses immediately, whereas cells that require longer time to adapt also respond later. This is reflected by Hog1 nuclear localization, Hog1 promoter association and the transcriptional response, but not Hog1 phosphorylation, suggesting that a presently uncharacterized rapid adaptive mechanism precedes the Hog1 nuclear response. Furthermore, we found that the period of Hog1 nuclear residence affects the amplitude of the transcriptional response rather than the spectrum of responsive genes.

Rewiring yeast osmostress signalling through the MAPK network reveals essential and non-essential roles of Hog1 in osmoadaptation

“…2f). This observation is consistent with recent reports showing that glycerol accumulation is essential for cell volume recovery3031. Taken together, glycerol accumulation by upregulating expression of two genes, GPD1 and GPP2 , is sufficient for synthetic osmoadaptation.…”

Metabolic profiling of wheat rachis node infection by Fusarium graminearum – decoding deoxynivalenol‐dependent susceptibility

“…ROS metabolism in F. graminearum is partially governed by the high‐osmolarity glycerol (HOG) related MAP‐kinase FgOS‐2 (Nguyen et al ., ). FgOS‐2, like the S. cerevisiae HOG1p (Geijer et al ., ) activated through the polyol pathway, influences gene expression and activity of H 2 O 2 ‐decomposing catalases and links osmotic and oxidative stress (Nguyen et al ., ). Mannitol is a typical polyol in F. graminearum (Abebe et al ., ; Ramirez et al ., ) not synthesized by T. aestivum and with specific functions in host–pathogen interactions (Meena et al ., ).…”

Yeast AMP-activated Protein Kinase Monitors Glucose Concentration Changes and Absolute Glucose Levels

“…Changes in the subcellular localization of signaling proteins as a consequence of signal progression offer the opportunity to observe signaling as it occurs. In the yeast Saccharomyces cerevisiae, signaling has been monitored employing cytoplasmic-nuclear shuttling of protein kinases and transcription factors for the osmo-sensing High Osmolarity Glycerol (HOG) pathway (the Hog1 MAP kinase) (1)(2)(3)(4)(5), the calcineurin pathway (the Crz1 transcriptional activator) (6), the protein kinase A pathway (the Msn2 transcriptional activator) (7)(8)(9), and oxidative stress signaling through Yap1 (10). Several interesting system properties have been observed, including perfect adaptation of the Hog1 signaling system (1), slowdown of protein movements as a consequence of molecular crowding in compressed cells following osmostress (3,5), the potential benefits of nuclear accumulation bursts to coordinate multigene responses to external signals or for the survival of cell populations (8,9), and how coupling of dynamic phenomena may establish a rate of change sensor (7).…”