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

Abstract

SummaryYeast cells show an adaptive response to a mild heat shock, resulting in thermotolerance acquisition. This is accompanied by induction of heat-shock protein (hsp) synthesis and rapid accumulation of trehalose. Genetic approaches to determine the specific role of trehalose in heat-induced thermotolerance in Saccharomyces cerevisiae have been hampered by the finding that deletion of TPS1, the gene encoding trehalose-6-phosphate synthase, causes a variety of pleiotropic effects, including inability to grow on glucose-containing media. Here, we have studied a tps1 mutant of the yeast Schizosaccharomyces pombe that reportedly has no such growth defects. We show that tps1 mutants have a serious defect in heat shock-induced acquisition of thermotolerance if conditioned at highly elevated temperatures (40-42.5ЊC), which, in wild-type cells, prevent hsp but not trehalose synthesis. In contrast, hsp synthesis appears to become particularly important under conditions in which trehalose synthesis is either absent (in tps1 mutant strains) or not fully induced (conditioning at moderately elevated temperatures, i.e. 35ЊC). In addition, pka1 mutants deficient in cAMP-dependent protein kinase were examined. Unconditioned pka1 cells had low levels of trehalose but a high basal level of thermotolerance. It was found that pka1 mutant cells, contrary to wild-type cells, accumulated large amounts of trehalose, even during a 50ЊC treatment. pka1 tps1 double mutants lacked this ability and showed reduced intrinsic thermotolerance, indicating a particularly important role for trehalose synthesis, which takes place during the challenging heat shock.

Trehalose is required for the acquisition of tolerance to a variety of stresses in the filamentous fungus Aspergillus nidulans The GenBank accession number for the sequence reported in this paper is AF043230.

“…This is in agreement with the previous observations that germlings of A. nidulans maintaining a high level of trehalose due to a defect in the TreB neutral trehalase are less sensitive to heat stress than wild-type germlings (d 'Enfert et al, 1999) and that viability of the conidia of an A. niger tpsA mutant is reduced (Wolschek and Kubicek, 1997). This is also consistent with the role of trehalose in the acquisition of thermotolerance and halotolerance demonstrated in S. cerevisiae (Hounsa et al, 1998 ;Lewis et al, 1995) and in Schizosaccharomyces pombe (Ribeiro et al, 1998). Results presented in Fig.…”

Signaling via cAMP in fungi: interconnections with mitogen-activated protein kinase pathways

“…Mutants defective in pka1 have higher thermotolerance, and this may be partially due to increased trehalose synthesis. However, a pka1 tps1 double mutant is more thermotolerant than a wildtype strain or a tps1 mutant, suggesting that cAMP has another effect on thermotolerance that is independent of trehalose synthesis (Ribeiro et al 1997). The level of tps1 mRNA is approximately threefold higher in a pka1 mutant than in a wild-type strain, suggesting that Pka1 also has a role in the expression of genes involved in thermotolerance ).…”

Hsp16p Is Required for Thermotolerance in Nuclear mRNA Export in Fission Yeast Schizosaccharomyces pombe

“…Mild heat pretreatments of cells induce adaptation to high temperatures, that is, thermotolerance. After acquisition of thermotolerance, cells can survive even at high temperatures which otherwise would be lethal to them (Ribeiro et al, 1997). In S. cerevisiae, large heat shock proteins, such as Hsp104p and Hsp70p, were thought to contribute to the acquisition of thermotolerance for growth by promoting the resolubilization of aggregated proteins (Parsell et al, 1994).…”

“…The non-reducing disaccharide trehalose was also shown to be involved in acquisition of thermotolerance in yeast cells (Ribeiro et al, 1997). tps1, a mutant for trehalose synthesis shows a serious defect in induction of thermotolerance in S. pombe (Ribeiro et al, 1997).…”

“…tps1, a mutant for trehalose synthesis shows a serious defect in induction of thermotolerance in S. pombe (Ribeiro et al, 1997). Trehalose accumulated in cells is thought to protect cells by enhancing the thermal stability of proteins and reducing the heat-induced formation of protein aggregates (for a review, see Wiemken, 1990).…”