DOI: 10.3390/biom16101533 ISSN: 2218-273X

Schizophyllum commune Enhances Dendrobine Accumulation in Dendrobium nobile in Association with Induced Fungal Cellulolytic Activity and Host Jasmonate Biosynthesis

Yongxia Zhao, Yonglin Ouyang, Nian Xiong, Xiaolong Ji, Qi Jia, Lin Qin, Jian Xie, Yuqi He

Objective: To explore the mechanism by which Schizophyllum commune elevates dendrobine accumulation in Dendrobium nobile, and verify whether cellulase derived from this fungus triggers jasmonate biosynthesis to mediate the regulation of alkaloid production. Methods: Endophytic fungi were isolated from D. nobile stems via tissue block isolation and identified by ITS sequencing. A plant–fungus symbiotic system was established with axenic plantlets. Dual RNA seq transcriptomic analysis, RT qPCR, pharmacological interventions with methyl jasmonate (MeJA) and the JA biosynthesis inhibitor salicylhydroxamic acid (SHAM) and Extracellular cellulase activities assays was performed. Results: In this study, none of 29 endophytic fungal strains from D. nobile stems produced dendrobine independently. Symbiotic screening subsequently identified Schizophyllum commune CY01 1H (SC) as the best strain that significantly increased dendrobine accumulation in D. nobile plantlets. Dual RNA seq revealed that SC colonization substantially activated jasmonic acid (JA) biosynthesis, accompanied by marked upregulation of the key biosynthetic gene DnLOX2. In contrast, downstream JA-signaling components exhibited an atypical transcriptional pattern, DnJAR was downregulated, whereas DnJAZ was upregulated. These results suggest that SC colonization induces a reconfiguration of JA signaling that may contribute to the maintenance of symbiotic homeostasis. In the fungus, cellulase-encoding genes were significantly induced. Experimental verification that MeJA promoted dendrobine accumulation, whereas SHAM suppressed it, and SC symbiosis partially mitigated this suppression. Stem section assays showed dynamic increases in extracellular cellulase activities (endoglucanase, cellobiohydrolase, β glucosidase), peaking at day 19, with endoglucanase being the highest. Conclusions: These findings support a cross-regulatory model in which S. commune CY01-1H induces cellulolytic enzyme production during colonization, coinciding with host JA-biosynthetic activation and JA-signaling reprogramming, ultimately enhancing dendrobine accumulation. This study provides integrated evidence from fungal and host transcriptomes and enzymatic assays, expanding our understanding of endophyte-mediated regulation of medicinal plant metabolism. S. commune CY01 1H represents a promising biostimulant for sustainable improvement of dendrobine yield in cultivated D. nobile.

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