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• Heat stress response mechanism of Grifola frondosa is proposed by multiomics analysis. • Heat shock proteins play a central role in heat stress response in Grifola frondosa. • Polyamines serve as protection agents in response to heat stress in Grifola frondosa. • Grifola frondosa uses mTOR and Ca2+ pathways to sense and transmit heat-stress signal. High temperature can lead to severe retardation in the growth and development of mushrooms, which influence the quality of fruiting bodies. Grifola frondosa is a popular and wide-cultivated mushroom in Asia; however, little information about the heat response mechanism in this commercially cultivated mushroom has been reported. The growth test was performed to determine the heat tolerance of different strains. Then, the TMT-based proteome and transcriptome analysis of major G. frondosa cultivar Qinghui-151 under different temperatures were performed. High temperature seriously affected the growth and recovery growth of mycelia. Thirty-four heat shock proteins (HSPs) were identified in the multiomics data and the expressions of most HSPs were induced by high temperature. The accumulation of HSPs under the control of HSFs is assumed to play a central role in the heat stress response (HSR) in G. frondosa. mTOR and Ca2+ signaling pathways were found to be activated under high temperature and might involved in heat stress signaling transduction. Polyamines synthesis enzymes were also up-regulated, suggesting the accumulation of stress protector polyamines under heat stress. In addition, expression of an L-phenylalanine ammonia-lyase (GfPAL) gene was significantly up-regulated under high temperature, which might be related to secondary metabolites synthesis. Taken together, these findings improve our understanding of the molecular mechanisms underlying the response to heat stress in G. frondosa , which could promote the breeding of new heat-tolerant G. frondosa cultivars. [Display omitted] [ABSTRACT FROM AUTHOR]