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Title: Characterizing the in vivo role of trehalose in Saccharomyces cerevisiae using the AGT1 transporter

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America

Trehalose is a highly stable, nonreducing disaccharide of glucose. A large body of research exists implicating trehalose in a variety of cellular phenomena, notably response to stresses of various kinds. However, in very few cases has the role of trehalose been examined directly in vivo. Here, we describe the development and characterization of a system in Saccharomyces cerevisiae that allows us to manipulate intracellular trehalose concentrations independently of the biosynthetic enzymes and independently of any applied stress. We found that many physiological roles heretofore ascribed to intracellular trehalose, including heat resistance, are not due to the presence of trehalose per se. We also found that many of the metabolic and growth defects associated with mutations in the trehalose biosynthesis pathway are not abolished by providing abundant intracellular trehalose. Instead, we made the observation that intracellular accumulation of trehalose or maltose (another disaccharide of glucose) is growth-inhibitory in a carbon source-specific manner. We conclude that the physiological role of the trehalose pathway is fundamentally metabolic: i.e., more complex than simply the consequence of increased concentrations of the sugar and its attendant physical properties (with the exception of the companion paper where demonstrate a direct role for trehalose in protecting cells against desiccation).

Research Organization:
Princeton Univ., NJ (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
SC0012461
OSTI ID:
1347586
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, Issue 19; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 58 works
Citation information provided by
Web of Science

References (47)

Effect of trehalose on protein structure journal January 2008
Two Distinct Pathways for Trehalose Assimilation in the Yeast Saccharomyces cerevisiae journal May 2004
Trehalose Metabolism and Signaling journal June 2008
Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli. journal June 1988
Immunological Properties of Trehalose Dimycolate (Cord Factor) and Other Mycotic Acid-Containing Glycolipids--A Review journal December 2001
Trehalose: Current Use and Future Applications journal June 2011
Kinetics of active α-glucoside transport in Saccharomyces cerevisiae journal April 2001
Can Trehalose Prevent Neurodegeneration? Insights from Experimental Studies journal April 2014
Trehalose 6-phosphate phosphatase is required for development, virulence and mycotoxin biosynthesis apart from trehalose biosynthesis in Fusarium graminearum journal February 2014
Deletion of the ATH1 gene in Saccharomyces cerevisiae prevents growth on trehalose journal May 1996
Multiple Effects of Trehalose on Protein Folding In Vitro and In Vivo journal April 1998
Trehalose synthase: guard to the gate of glycolysis in yeast? journal January 1995
Yeast metabolic and signaling genes are required for heat-shock survival and have little overlap with the heat-induced genes journal October 2013
Relevance of Trehalose in Pathogenicity: Some General Rules, Yet Many Exceptions journal August 2013
Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli. journal December 1991
Lost in Transition: Start-Up of Glycolysis Yields Subpopulations of Nongrowing Cells journal January 2014
Trehalose reserve in Saccharomyces cerevisiae: phenomenon of transport, accumulation and role in cell viability journal April 2000
Sugar signals and molecular networks controlling plant growth journal June 2010
Trehalose in yeast, stress protectant rather than reserve carbohydrate journal October 1990
Characterization of AGT1 encoding a general alpha-glucoside transporter from Saccharomyces journal September 1995
Disruption of the Candida albicans TPS1Gene Encoding Trehalose-6-Phosphate Synthase Impairs Formation of Hyphae and Decreases Infectivity journal August 1998
Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae journal January 2001
Genome-wide identification of genes involved in tolerance to various environmental stresses inSaccharomyces cerevisiae journal September 2009
The First Prokaryotic Trehalose Synthase Complex Identified in the Hyperthermophilic Crenarchaeon Thermoproteus tenax journal April 2013
Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. journal January 1995
A temperature-sensitive mutant of Sacchromyces cerevisiae defective in the specific phosphatase of trehalose biosynthesis journal February 1988
Autonomous oscillations in Saccharomyces cerevisiae during batch cultures on trehalose: Oscillating batch cultures on trehalose journal March 2005
Preservation of Membranes in Anhydrobiotic Organisms: The Role of Trehalose journal February 1984
The role of trehalose synthesis for the acquisition of thermotolerance in yeast. II. Physiological concentrations of trehalose increase the thermal stability of proteins in vitro journal January 1994
The Chemistry of Insect Hemolymph: ii. Trehalose and Other Carbohydrates journal July 1957
Growth-limiting Intracellular Metabolites in Yeast Growing under Diverse Nutrient Limitations journal January 2010
Revisiting yeast trehalose metabolism journal September 2014
Oscillatory metabolism of Saccharomyces cerevisiae: an overview of mechanisms and models journal May 2003
Trehalose synthesis and metabolism are required at different stages of plant infection by Magnaporthe grisea journal January 2003
Characterization and Regulation of the Trehalose Synthesis Pathway and Its Importance in the Pathogenicity of Cryptococcus neoformans journal September 2006
New insights on trehalose: a multifunctional molecule journal January 2003
Composition and Functional Analysis of the Saccharomyces cerevisiae Trehalose Synthase Complex journal December 1998
Rapid Expansion and Functional Divergence of Subtelomeric Gene Families in Yeasts journal May 2010
The role of trehalose synthesis for the acquisition of thermotolerance in yeast. I. Genetic evidence that trehalose is a thermoprotectant journal January 1994
Evidence for trehalose-6-phosphate-dependent and -independent mechanisms in the control of sugar influx into yeast glycolysis journal June 1996
Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose journal November 1998
Growth Arrest by Trehalose-6-Phosphate: An Astonishing Case of Primary Metabolite Control over Growth by Way of the SnRK1 Signaling Pathway journal July 2011
The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi journal January 2004
Increasing intracellular trehalose is sufficient to confer desiccation tolerance to Saccharomyces cerevisiae journal April 2015
Molecular Biology of Trehalose and the Trehalases in the Yeast Saccharomyces cerevisiae book January 1997
Large-Scale Functional Genomic Analysis of Sporulation and Meiosis in Saccharomyces cerevisiae journal January 2003
Slow Growth Induces Heat-Shock Resistance in Normal and Respiratory-deficient Yeast journal February 2009

Cited By (19)

Osmolytes ameliorate the effects of stress in the absence of the heat shock protein Hsp104 in Saccharomyces cerevisiae journal September 2019
Synergy between the small intrinsically disordered protein Hsp12 and trehalose sustain viability after severe desiccation journal July 2018
Antifreeze proteins govern the precipitation of trehalose in a freezing-avoiding insect at low temperature journal May 2016
Discrete roles of trehalose and Hsp104 in inhibition of protein aggregation in yeast cells journal May 2018
Selection and subsequent physiological characterisation of industrial Saccharomyces cerevisiae strains during continuous growth at sub- and- supra optimal temperatures posted_content January 2020
The trehalose protective mechanism during thermal stress in Saccharomyces cerevisiae: the roles of Ath1 and Agt1 journal June 2018
Ongoing resolution of duplicate gene functions shapes the diversification of a metabolic network journal September 2016
Comprehensive molecular characterization of Methylobacterium extorquens AM1 adapted for 1-butanol tolerance journal April 2016
Cross-stress resistance in Saccharomyces cerevisiae yeast—new insight into an old phenomenon journal January 2016
Common and divergent features of galactose-1-phosphate and fructose-1-phosphate toxicity in yeast journal April 2018
Trehalose induced by reactive oxygen species relieved the radial growth defects of Pleurotus ostreatus under heat stress journal May 2019
Dynamics of Storage Carbohydrates Metabolism in Saccharomyces cerevisiae text January 2015
The SEB-1 Transcription Factor Binds to the STRE Motif in Neurospora crassa and Regulates a Variety of Cellular Processes Including the Stress Response and Reserve Carbohydrate Metabolism journal March 2016
Molecular characterization of Tps1 and Treh genes in Drosophila and their role in body water homeostasis journal July 2016
A Single-Nucleotide Insertion in a Drug Transporter Gene Induces a Thermotolerance Phenotype in Gluconobacter frateurii by Increasing the NADPH/NADP + Ratio via Metabolic Change journal March 2018
Cloning, purification and characterization of trehalose-6-phosphate synthase from Pleurotus tuoliensis journal January 2018
Trehalose synthesis inhibitor: A molecular in silico drug design
  • Gonçalves, Lucas Machado; Trevisol, Eduardo Thomaz Vasconcelos; Azevedo Abrahim Vieira, Bárbara
  • Journal of Cellular Biochemistry, Vol. 121, Issue 2 https://doi.org/10.1002/jcb.29347
journal September 2019
Quantitative Operating Principles of Yeast Metabolism during Adaptation to Heat Stress journal February 2018
Nutritional and Meiotic Induction of Heritable Stress Resistant States in Budding Yeast posted_content August 2018

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