Regulation of genes encoding subunits of the trehalose synthase complex inSaccharomyces cerevisiae: novel variations of STRE-mediated transcription control?

Abstract

Saccharomyces cerevisiae cells show under suboptimal growth conditions a complex response that leads to the acquisition of tolerance to different types of environmental stress. This response is characterised by enhanced expression of a number of genes which contain so-called stress-responsive elements (STREs) in their promoters. In addition, the cells accumulate under suboptimal conditions the putative stress protectant trehalose. In this work, we have examined the expression of four genes encoding subunits of the trehalose synthase complex, GGS1/TPS1, TPS2, TPS3 and TSL1. We show that expression of these genes is coregulated under stress conditions. Like for many other genes containing STREs, expression of the trehalose synthase genes is also induced by heat and osmotic stress and by nutrient starvation, and negatively regulated by the Ras-cAMP pathway. However, during fermentative growth only TSL1 shows an expression pattern like that of the STRE-controlled genes CTT1 and SSA3, while expression of the three other trehalose synthase genes is only transiently down-regulated. This difference in expression might be related to the known requirement of trehalose biosynthesis for the control of yeast glycolysis and hence for fermentative growth. We conclude that the mere presence in the promoter of (an) active STRE(s) does not necessarily imply complete coregulation of expression. Additional mechanisms appear to fine tune the activity of STREs in order to adapt the expression of the downstream genes to specific requirements.

Trehalose synthesis is important for the acquisition of thermotolerance in Schizosaccharomyces pombe

“…Synthesis of trehalose is mediated by the trehalose-6-phosphate (Tre6P) synthase-phosphatase complex, which, in S. cerevisiae, consists of at least four subunits carrying either Tre6P synthase (Tps1), Tre6P phosphatase (Tps2) or regulatory activities (Tps3 and Tsl1; Bell et al, 1992;De Virgilio et al, 1993;Vuorio et al, 1993;Reinders et al, 1997). In accordance with the observation that heat-induced accumulation of trehalose is partially dependent on protein synthesis in S. cerevisiae (De Virgilio et al, 1991), both catalytic subunits (Tps1 and Tps2) have been shown to be hsps, and expression of all four genes encoding the subunits of the Tre6P synthase complex (TPS1, TPS2, TPS3 and TSL1 ) has been found to be dramatically enhanced under heat-shock conditions (De Virgilio et al, 1993;Winderickx et al, 1996). Degradation of cytosolic trehalose is mainly mediated by the neutral trehalase (Londesborough and Varimo, 1984), which has attracted considerable attention because its potential activation by the cAMP-dependent protein kinase (cAPK) allows monitoring of the activation status of the Ras/cAMP pathway (for a review, see Thevelein, 1992).…”

“…The observation that unconditioned pka1 mutant cells had threefold to fourfold increased levels of Tre6P synthase activity indicates that cAPK may, as in S. cerevisiae (Winderickx et al, 1996), have a role in the negative regulation of tps1 þ transcription. As expected, tps1 þ was found to be essential for Tre6P synthase activity in wild-type and pka1 mutant cells.…”

Carbohydrate utilization and the lager yeast transcriptome during brewery fermentation

“…Trehalose is synthesised by the α,α-trehalose-phosphate synthase complex, made up of the products of TPS1, TPS2, TSL1 and TPS3 genes (Bell et al, 1992). Why the genes responded differently to the same conditions is not clear, as they are known to be regulated similarly by stress conditions and repressed via the RAS-cAMP pathway (Winderickx et al, 1996). Conversely, the three genes known to be involved in the hydrolysis of trehalose (ATH1, NTH1 and NTH2 ) showed highest transcription values at 60 and/or 80 h. Trehalose accumulates in brewing yeast cells towards the end of fermentation and this is most likely a response to nutrient or fermentable carbohydrate limitation and/or ethanol toxicity (Boulton and Quain, 2001).…”

Structural analysis of the subunits of the trehalose‐6‐phosphate synthase/phosphatase complex in Saccharomyces cerevisiae and their function during heat shock

“…In accordance with such a model, TPS3 and TSL1 have been reported to be differentially expressed in S. cerevisiae. While TPS3 is expressed at a constant rate in exponentially growing and stationaryphase cells, TSL1 expression is greatly enhanced upon entrance into stationary phase (Winderickx et al, 1996). Thus, the two proteins may indeed mediate, to some extent, differential regulation of the Tre6P synthase complex according to their relative abundance under different physiological conditions (e.g.…”

“…Thus, Tsl1 may be involved in modification of the kinetic properties of Tre6P synthase activity. Recent studies on TPS3 and TSL1 expression levels suggest that Tsl1 and Tps3 may to some extent act as interchangeable regulators of the Tre6P synthase/phosphatase complex, but that they also may exert different regulation under specific growth conditions (Winderickx et al, 1996). The precise function of both proteins, however, is not clear.…”