Effects of various types of stress on the metabolism of reserve carbohydrates in Saccharomyces cerevisiae: genetic evidence for a stress-induced recycling of glycogen and trehalose.
It is well known that glycogen and trehalose accumulate in yeast under nutrient starvation or entering into the stationary phase of growth, and that high levels of trehalose are found in heat-shocked cells. However, effects of various types of stress on trehalose, and especially on glycogen, are poorly documented. Taking into account that almost all genes encoding the enzymes involved in the metabolism of these two reserve carbohydrates contain between one and several copies of the stress-responsive element (STRE), an investigation was made of the possibility of a link between the potential transcriptional induction of these genes and the accumulation of glycogen and trehalose under different stress conditions. Using transcriptional fusions, it was found that all these genes were induced in a similar fashion, although to various extents, by temperature, osmotic and oxidative stresses. Experiments performed with an msn2/msn4 double mutant proved that the transcriptional induction of the genes encoding glycogen synthase (GSY2) and trehalose-6-phosphate synthase (TPS1) was needed for the small increase in glycogen and trehalose upon exposure to a mild heat stress and salt shock. However, the extent of transcriptional activation of these genes upon stresses in wild-type strains was not correlated with a proportional rise in either glycogen or trehalose. The major explanation for this lack of correlation comes from the fact that genes encoding the enzymes of the biosynthetic and of the biodegradative pathways were almost equally induced. Hence, trehalose and glycogen accumulated to much higher levels in cells lacking neutral trehalose or glycogen phosphorylase exposed to stress conditions, which suggested that one of the major effects of stress in yeast is to induce a wasteful expenditure of energy by increasing the recycling of these molecules. We also found that transcriptional induction of STRE-controlled genes was abolished at temperatures above 40 degree C, while induction was still observed for a heat-shock-element regulated gene. Remarkably, trehalose accumulated to very high levels under this condition. This can be explained by a stimulation of trehalose synthase and inhibition of trehalose by high temperature.
Parrou
Jean Luc
JL
Centre de Bioingenierie Gilbert Durand, UMR CNRS 5504, Laboratoire Associé INRA, Complexe Scientifique de Rangeuil, 31077 Toulouse Cedex 04, France.
Teste
Marie-Ange
MA
Centre de Bioingenierie Gilbert Durand, UMR CNRS 5504, Laboratoire Associé INRA, Complexe Scientifique de Rangeuil, 31077 Toulouse Cedex 04, France.
François
Jean
J
Centre de Bioingenierie Gilbert Durand, UMR CNRS 5504, Laboratoire Associé INRA, Complexe Scientifique de Rangeuil, 31077 Toulouse Cedex 04, France.
D050260:Carbohydrate Metabolism; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism; D004789:Enzyme Activation; D004798:Enzymes / Q000378:metabolism; D005656:Fungal Proteins / Q000235:genetics / Q000378:metabolism; D005800:Genes, Fungal / Q000235:genetics; D006003:Glycogen / Q000235:genetics / Q000378:metabolism; D006361:Heating / Q000379:methods; D008840:Microfilament Proteins; D009154:Mutation / Q000235:genetics; D011506:Proteins / Q000235:genetics; D012441:Saccharomyces cerevisiae / Q000737:chemistry* / Q000235:genetics / Q000378:metabolism; D029701:Saccharomyces cerevisiae Proteins; D014157:Transcription Factors; D015533:Transcriptional Activation / Q000235:genetics / Q000502:physiology; D014199:Trehalose / Q000235:genetics / Q000378:metabolism; D016335:Zinc Fingers / Q000235:genetics / Q000502:physiology
D004268:DNA-Binding Proteins; D004798:Enzymes; D005656:Fungal Proteins; C081935:MSN2 protein, S cerevisiae; C081937:MSN4 protein, S cerevisiae; D008840:Microfilament Proteins; D011506:Proteins; D029701:Saccharomyces cerevisiae Proteins; D014157:Transcription Factors; C071058:moesin; D006003:Glycogen; D014199:Trehalose