Endophytic colonization by Beauveria bassiana induces steroidal glycoalkaloids accumulation in tomato and suppresses Tuta absoluta performance

Abstract Beauveria bassiana is widely used as an entomopathogen in sustainable pest management, and its endophytic colonization has been increasingly recognized as a potential means of priming plant defence against herbivores. Here we show that root drenching of tomato with B. bassiana substantially reduced the fitness of Tuta absoluta : larval development was prolonged by 2.1 days, fourth-instar larval weight dropped by 34%, pupal weight by 22%, and pupation rate, emergence rate and female fecundity all declined significantly. Foliar spray application produced weaker effects, affecting only pupal weight and emergence rate. No B. bassiana was re-isolated from insect bodies, ruling out direct infection and pointing to a plant-mediated mechanism. Transcriptomic profiling of T. absoluta larvae feeding on colonized plants revealed the upregulation of detoxification-related metabolic pathways, particularly cytochrome P450 genes. To test whether this response was triggered by steroidal glycoalkaloids (SGAs), we fed larvae on tomato mutants with reduced or elevated SGA content. Larvae feeding on SGA-knockout mutants showed no changes in detoxification enzyme activity or development relative to controls, whereas those feeding on SGA-overexpressing mutants exhibited strong developmental inhibition and a marked increase in cytochrome P450 activity. These results demonstrate that endophytic B. bassiana primes tomato defence against T. absoluta specifically through SGA induction. Our findings establish a mechanistic basis for integrating entomopathogenic fungi with plant innate immunity in pest management.