Trehalose alleviates high\u2010temperature stress in Pleurotus ostreatus by affecting central carbon metabolism

Zhi-Yu Yan,Chen-Yang Huang,Li-Jiao Zhang,Jin-Xia Zhang,Meng-Ran Zhao

doi:10.1186/s12934-021-01572-9

Abstract

BackgroundTrehalose, an intracellular protective agent reported to mediate defense against many stresses, can alleviate high-temperature-induced damage in Pleurotus ostreatus. In this study, the mechanism by which trehalose relieves heat stress was explored by the addition of exogenous trehalose and the use of trehalose-6-phosphate synthase 1 (tps1) overexpression transformants.ResultsThe results suggested that treatment with exogenous trehalose or overexpression of tps1 alleviated the accumulation of lactic acid under heat stress and downregulated the expression of the phosphofructokinase (pfk) and pyruvate kinase (pk) genes, suggesting an ameliorative effect of trehalose on the enhanced glycolysis in P. ostreatus under heat stress. However, the upregulation of hexokinase (hk) gene expression by trehalose indicated the involvement of the pentose phosphate pathway (PPP) in heat stress resistance. Moreover, treatment with exogenous trehalose or overexpression of tps1 increased the gene expression level and enzymatic activity of glucose-6-phosphate dehydrogenase (g6pdh) and increased the production of both the reduced form of nicotinamide adenine dinucleotide phosphate (NADPH) and glutathione (GSH), confirming the effect of trehalose on alleviating oxidative damage by enhancing PPP in P. ostreatus under heat stress. Furthermore, treatment with exogenous trehalose or overexpression of tps1 ameliorated the decrease in the oxygen consumption rate (OCR) caused by heat stress, suggesting a relationship between trehalose and mitochondrial function under heat stress.ConclusionsTrehalose alleviates high-temperature stress in P. ostreatus by inhibiting glycolysis and stimulating PPP activity. This study may provide further insights into the heat stress defense mechanism of trehalose in edible fungi from the perspective of intracellular metabolism.

Highlights

Trehalose, an intracellular protective agent reported to mediate defense against many stresses, can alleviate high-temperature-induced damage in Pleurotus ostreatus
Trehalose accumulates under high‐temperature stress We performed one LC-MS metabonomic assay on the intracellular metabolites of P. ostreatus mycelia under heat stress (40 °C) for 0–48 h and found a significant change in the trehalose content
The accumulation of trehalose in P. ostreatus mycelia under heat stress may indicate a role for trehalose in the P. ostreatus heat stress defense [2]

Summary

Introduction

An intracellular protective agent reported to mediate defense against many stresses, can alleviate high-temperature-induced damage in Pleurotus ostreatus. Pleurotus ostreatus is cultivated worldwide and is widely studied due to its high nutritional, economic, medical, and ecological value [1]. Trehalose accumulation increases the resistance of Salmonella enterica to high salt, low pH, and hydrogen peroxide [6] and increases thermal and osmotic stress resistance in Listeria monocytogenes [5]. Mutants of the plant pathogen Ustilago maydis that do not produce trehalose show increased sensitivity to oxidative, heat, acid, ionic, and osmotic stresses [10]. Trehalose can ameliorate the radial growth defects in P. ostreatus under heat stress [2]

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