Activation of mycelial defense mechanisms in the oyster mushroom Pleurotus ostreatus induced by Tyrophagus putrescentiae

Abstract

Fungal chemicals are vital in processes recognizing damage- and microbe-associated molecules (DAMPs/MAMPs) that trigger defense responses in fungi. Pleurotus ostreatus is a widely cultivated edible fungus that is prone to attack from fungivorous insects and mites. Yet P. ostreatus has evolved an elegant defense system against fungivore attacks. In this study, we investigated how the oyster mushroom responds to the fungivory and mechanical wounding by conducting transcriptome, proteome, and secondary metabolic analyses. The profiling analysis revealed a total of 11,495 transcripts and 866 proteins, 4416 differentially expressed genes (DEGs), and 62 differentially expressed proteins (DEPs) were identified in response to the mite Tyrophagus putrescentiae feeding and mechanical wounding. In comparing the responses induced by mechanical wounding, some genes, proteins, and metabolites were uniquely induced or repressed by the mite. At the transcript level, nine pathways were activated by the mite feeding, including those of "MAPK signaling pathway-yeast", "Phenylalanine metabolism", and "Biotin metabolism", among others, while both enrichment of "Ribosome", "Ribosome biogenesis in eukaryotes", and "Regulation of Mitophagy in Yeast" demonstrated the common effects upon fungal secretory protein synthesis and processing induced by fungivory and mechanical wounding. Fungivory also stimulated the synthesis of C₈-aryl compounds and sesquiterpenes (especially1-octen-3-ol and α-/β-bisabolene), and these compounds repellent to T. putrescentiae. Both jasmonic acid (JA) and jasmonic acid methyl ester (MeJA) were specifically regulated by mite feeding and mechanical wounding. The terpene synthase gene transcription was significantly increased induced by the exogenous addition of MeJA, resulting in defensive sesquiterpene production against the mite. These findings are the first to demonstrate that the reactive oxygen species (ROS)/MAPK signaling pathway, JA regulation, specific gene expression, and protein synthesis, and anti-mite substance metabolism are all involved in coordinated inducible chemical-based defense responses in P. ostreatus, which could be especially effective the mite T. putrescentiae.

Keywords: Bisabolene; Edible fungi; Fungal chemical defense; Fungivore; Mushroom; Pleurotus; Sesquiterpene.