The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi

Gancedo, Carlos; Flores, Carmen‐Lisset

doi:10.1016/s1567-1356(03)00222-8

Cited by 196 publications

(159 citation statements)

References 66 publications

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“…Recent studies show that the precursor of trehalose, T6P, is an indispensable regulator of sugar utilization in eukaryotic organisms as different as yeasts and plants (18,20,22). However, apart from regulating glycolysis by inhibiting hexokinase in some yeast species, other sites of T6P action have until now not been known (20,(25)(26)(27).…”

Section: Discussionmentioning

confidence: 99%

“…Hexokinase and SnRK1 are both implicated in a regulatory network that controls the expression and phosphorylation of cytosolic enzymes in response to sugars (17). How they are linked to reductive activation of AGPase and starch synthesis in the plastid remains unresolved.Recently, trehalose metabolism has been implicated in the regulation of sugar utilization in yeast and plants (18)(19)(20). Trehalose, an ancient sugar consisting of two ␣-1,1-linked glucose molecules, is synthesized via the phosphorylated precursor This paper was submitted directly (Track II) to the PNAS office.…”

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confidence: 99%

“…Recently, trehalose metabolism has been implicated in the regulation of sugar utilization in yeast and plants (18)(19)(20). Trehalose, an ancient sugar consisting of two ␣-1,1-linked glucose molecules, is synthesized via the phosphorylated precursor trehalose 6-phosphate (T6P), with a trehalose phosphate synthase (TPS) and a trehalose phosphate phosphatase (TPP).…”

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Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase

Kolbe

Tiessen

Schluepmann³

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

351

320

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Trehalose is the most widespread disaccharide in nature, occurring in bacteria, fungi, insects, and plants. Its precursor, trehalose 6-phosphate (T6P), is also indispensable for the regulation of sugar utilization and growth, but the sites of action are largely unresolved. Here we use genetic and biochemical approaches to investigate whether T6P acts to regulate starch synthesis in plastids of higher plants. Feeding of trehalose to Arabidopsis leaves led to stimulation of starch synthesis within 30 min, accompanied by activation of ADP-glucose pyrophosphorylase (AGPase) via posttranslational redox modification. The response resembled sucrose but not glucose feeding and depended on the expression of SNF1-related kinase. We also analyzed transgenic Arabidopsis plants with T6P levels increased by expression of T6P synthase or decreased by expression of T6P phosphatase (TPP) in the cytosol. Compared with wild type, leaves of T6P synthase-expressing plants had increased redox activation of AGPase and increased starch, whereas TPP-expressing plants showed the opposite. Moreover, TPP expression prevented the increase in AGPase activation in response to sucrose or trehalose feeding. Incubation of intact isolated chloroplasts with 100 M T6P significantly and specifically increased reductive activation of AGPase within 15 min. Results provide evidence that T6P is synthesized in the cytosol and acts on plastidial metabolism by promoting thioredoxin-mediated redox transfer to AGPase in response to cytosolic sugar levels, thereby allowing starch synthesis to be regulated independently of light. The discovery informs about the evolution of plant metabolism and how chloroplasts of prokaryotic origin use an intermediate of the ancient trehalose pathway to report the metabolic status of the cytosol.SNF1 kinase ͉ sugar signaling ͉ thioredoxin S tarch is the major carbon store in plants consisting of an insoluble polymer of ␣-1,4-and ␣-1,6-linked glucose units (1). In the chloroplast of leaves, starch is synthesized during the day as a transient store, which is degraded during the night to support nonphotosynthetic leaf metabolism and sucrose export. In heterotrophic storage organs such as potato tubers, most of the incoming sucrose is converted to starch as a long-term carbon store for reproductive growth. In addition to its central role in carbon metabolism of plants, starch is also of great economical importance and is used for food and feed purposes and many industrial applications (2).ADP-glucose pyrophosphorylase (AGPase) catalyzes the first committed step of starch synthesis in the plastid, converting glucose 1-phosphate and ATP to ADP-glucose and PP i . ADP-glucose is subsequently used by starch synthases and branching enzymes to elongate the glucan chains of the starch granule. AGPase is a heterotetramer that contains two large (AGPS, 51 kDa) and two slightly smaller subunits (AGPB, 50 kDa) (3, 4). Work with Arabidopsis mutants (5) and potato tubers (6) showed that the enzyme catalyzes a near rate-limiting step in the pat...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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confidence: 99%

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Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase

Kolbe

Tiessen

Schluepmann³

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

351

320

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“…T6P is an intermediate in trehalose biosynthesis that has been shown to possess regulatory potential (5,26 (7,21,22,47,53,59) and give further insights into T6P. In C. albicans, the tps2 mutant flocculates during stationary growth, while in A. nidulans, the mutant produces nonviable germination of spores through a deficiency in chitin production.…”

Section: Discussionmentioning

confidence: 99%

Characterization and Regulation of the Trehalose Synthesis Pathway and Its Importance in the Pathogenicity of Cryptococcus neoformans

et al. 2006

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The disaccharide trehalose has been found to play diverse roles, from energy source to stress protectant, and this sugar is found in organisms as diverse as bacteria, fungi, plants, and invertebrates but not in mammals. Recent studies in the pathobiology of Cryptococcus neoformans identified the presence of a functioning trehalose pathway during infection and suggested its importance for C. neoformans survival in the host. Therefore, in C. neoformans we created null mutants of the trehalose-6-phosphate (T6P) synthase (TPS1), trehalose-6-phophate phosphatase (TPS2), and neutral trehalase (NTH1) genes. We found that both TPS1 and TPS2 are required for high-temperature (37°C) growth and glycolysis but that the block at TPS2 results in the apparent toxic accumulation of T6P, which makes this enzyme a fungicidal target. Sorbitol suppresses the growth defect in the tps1 and tps2 mutants at 37°C, which supports the hypothesis that these sugars (trehalose and sorbitol) act primarily as stress protectants for proteins and membranes during exposure to high temperatures in C. neoformans. The essential nature of this pathway for disease was confirmed when a tps1 mutant strain was found to be avirulent in both rabbits and mice. Furthermore, in the system of the invertebrate C. elegans, in which high in vivo temperature is no longer an environmental factor, attenuation in virulence was still noted with the tps1 mutant, and this supports the hypothesis that the trehalose pathway in C. neoformans is involved in more host survival mechanisms than simply high-temperature stresses and glycolysis. These studies in C. neoformans and previous studies in other pathogenic fungi support the view of the trehalose pathway as a selective fungicidal target for use in antifungal development.

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“…In retrospect we know that with our selection strategy it would have been quite impossible to get those mutants: there are several genes in yeast encoding for different glucose transporters and glucose phosphorylating kinases. Ironically, perhaps some of the mutants we isolated were affected in TPS1, a gene encoding trehalose-6-phosphate synthase, whose mutation leads, as we eventually established many years later (3), to the phenotype we were selecting for.…”

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2006

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The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi

Cited by 196 publications

References 66 publications

Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase

Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase

Characterization and Regulation of the Trehalose Synthesis Pathway and Its Importance in the Pathogenicity of Cryptococcus neoformans

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