Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation

Abstract

SummaryThe accumulation of compatible solutes, such as glycerol, in the yeast Saccharomyces cerevisiae, is a ubiquitous mechanism in cellular osmoregulation. Here, we demonstrate that yeast cells control glycerol accumulation in part via a regulated, Fps1p-mediated export of glycerol. Fps1p is a member of the MIP family of channel proteins most closely related to the bacterial glycerol facilitators. The protein is localized in the plasma membrane. The physiological role of Fps1p appears to be glycerol export rather than uptake. Fps1⌬ mutants are sensitive to hypo-osmotic shock, demonstrating that osmolyte export is required for recovery from a sudden drop in external osmolarity. In wild-type cells, the glycerol transport rate is decreased by hyperosmotic shock and increased by hypo-osmotic shock on a subminute time scale. This regulation seems to be independent of the known yeast osmosensing HOG and PKC signalling pathways. Mutants lacking the unique hydrophilic N-terminal domain of Fps1p, or certain parts thereof, fail to reduce the glycerol transport rate after a hyperosmotic shock. Yeast cells carrying these constructs constitutively release glycerol and show a dominant hyperosmosensitivity, but compensate for glycerol loss after prolonged incubation by glycerol overproduction. Fps1p may be an example of a more widespread class of regulators of osmoadaptation, which control the cellular content and release of compatible solutes.

Integrative model of the response of yeast to osmotic shock

“…Another feature emerging from our simulations concerns the crucial role of the Fps1 aquaglyceroporin 33 in controlling glycerol accumulation and therefore also controlling signaling through the HOG pathway. The basal glycerol production level combined with rapid closure of Fps1 is sufficient to explain an initial glycerol accumulation after osmotic shock, which in turn accounts for HOG pathway downregulation.…”

“…The osmo-regulated aquaglyceroporin Fps1 contributes to the control of intracellular glycerol level 33,42 . We assume that the channel is open when the turgor pressure assumes its original value and that transport is downregulated with fading P t , reaching zero when turgor pressure is completely lost.…”

Genome‐wide screen of Saccharomyces cerevisiae for killer toxin HM‐1 resistance

“…Fps1p is phosphorylated by Hog1p MAPK and is degraded in vacuoles under acetate stress; lack of Fps1p further activates the CWI pathway MAPK Slt2p (Beese et al, 2009;Davenport et al, 1995;Mollapour and Piper, 2007;Mollapour et al, 2009;Philips and Herskowitz, 1997;Tamas et al, 1999;Tong and Boone, 2006). Table 4 shows that in this study hog1 and slt2 mutants had HM-1-sensitive phenotypes, whose IC 50 values were half that of the wild-type.…”

“…Fps1p participates in the efflux of glycerol to regulate the intracellular glycerol level together with glycerol production enzymes, which are stimulated by mitogen-activated protein kinase (MAPK) Hog1p and the HOG pathway (Hohmann, 2002;Luyten et al, 1995;Tamas et al, 1999). Fps1p is phosphorylated by Hog1p MAPK and is degraded in vacuoles under acetate stress; lack of Fps1p further activates the CWI pathway MAPK Slt2p (Beese et al, 2009;Davenport et al, 1995;Mollapour and Piper, 2007;Mollapour et al, 2009;Philips and Herskowitz, 1997;Tamas et al, 1999;Tong and Boone, 2006).…”

Analysis of osmoadaptation system in budding yeast suggests that regulated degradation of glycerol synthesis enzyme is key to near-perfect adaptation

“…Figure 2a shows the mRNA profiles for the wild type and a mutant in which FPS1, a glycerol transporter membrane protein (Tamás et al 1999), is made putatively open, for cells in a 0.5 M NaCl solution, (re-plotted from the data in Klipp et al (2005)). Note that the unregulated expression of FPS1 increases leakage of glycerol thereby reducing the ability of the cell to adapt.…”