Transcriptional regulation of virulence and stress adaptation in Akanthomyces attenuatus JEF-147 during mite pathogenesis.

Although Akanthomyces attenuatus JEF-147 exhibits high virulence against the two-spotted spider mite (Tetranychus urticae), its molecular mechanisms remain poorly understood. This study investigated fungal gene expression during early pathogenesis to elucidate how JEF-147 overcomes host defenses. Treatment on adults significantly suppressed descendant nymph populations. RNA-sequencing revealed time-dependent transcriptomic shifts: at 36-h after treatment, DEGs were primarily associated with transcription and translation, whereas 72-h samples showed activation of genes related to pathogenesis and stress management. Pathway analysis indicated that 72-h DEGs were enriched in metabolic pathways, suggesting JEF-147 maximizes energy production (TCA cycle and oxidative phosphorylation) and reinforces cell walls (glucan biosynthesis). The fungus actively utilizes host-derived fatty acids and proteins while maintaining homeostasis via the glutathione pathway. Furthermore, enrichment in vacuolar degradation pathways including autophagy and endocytosis in 72-h samples suggests active digestion of host nutrients. It was partially supported via LC-MS/MS analysis of fungal supernatants from a saprophytic culture. Our results suggest a two-stage infection strategy: an initial 36-h phase focused on hyphal growth and penetration, followed by a 72-h transition to counteracting host defenses through up-regulation of virulence and stress management-related genes. This work provides critical insights into the infection mechanisms of mite-pathogenic fungi.