Cuminal-triggered mitophagy induces mitochondrial dysfunction, resulting in decreased vegetative growth and...

Trichothecium roseum (T. roseum) is a significant postharvest pathogen that infects a wide range of fruits and vegetables. This study investigated the antifungal activity of cuminal (CA), the major active component of cumin essential oil, against T. roseum. The results showed that CA notably inhibited spore germination, germ tube elongation, mycelial growth, and pathogenicity in T. roseum. Mechanistic analyses revealed that CA induced excessive intracellular reactive oxygen species (ROS) accumulation in T. roseum, despite antioxidant elicitation, leading to oxidative stress. This stress triggered mitochondrial dysfunction, characterized by ultrastructural damage, membrane depolarization, cytochrome c release, and disturbance of Ca²⁺ homeostasis. Further examination showed that CA altered mitochondrial dynamics and activated TrAtg8-mediated mitophagy, as evidenced by upregulated autophagy-related genes and the definite colocalization of GFP-TrAtg8 with mitochondria and vacuoles. Excessive mitophagy impaired mitochondrial function, resulting in a 44.14% decrease in energy charge in CA-treated spores compared to the untreated control. This energy deficit led to the suppression of gene expression of cell wall-degrading enzymes, required for pathogenic attack, and to impaired environmental alkalization capability, which is crucial for successful host colonization. Consequently, this led to a significant reduction in T. roseum's pathogenicity. Taken together, this study establishes that CA disrupts T. roseum's energy metabolism via a cascade initiated by oxidative stress, which dysregulates mitochondria and traps the cell in a futile cycle of excessive mitophagy, ultimately decreasing its pathogenic capacity. This multi-target mechanism highlights CA's potential as a natural postharvest preservative for fruits and vegetables against T. roseum.