Genistein Mediates Beauveria bassiana-Induced Resistance Against Bemisia tabaci Reproduction in Tomato.

Endophytic colonization by entomopathogenic fungi Beauveria bassiana enhances plant resistance to herbivores; however, the underlying molecular mechanisms, particularly those involving hormonal disruption of pests, remain poorly understood. This study examined whether root inoculation of tomato with B. bassiana suppresses whitefly Bemisia tabaci fitness via flavonoid modulation. Metabolomic profiling of leaf tissues showed a 3.5-fold accumulation of the isoflavonoid genistein in B. bassiana-inoculated plants. KEGG enrichment analysis indicated significant upregulation of the isoflavonoid biosynthesis pathway. Virus-induced gene silencing of SlHIDH (2-hydroxyisoflavanone dehydratase), a key gene in genistein biosynthesis, reversed the fungal-mediated protection: it increased whitefly ovariole number by 20.5% and oviposition by 23.5% compared with the control. Correspondingly, B. bassiana inoculation downregulated seven whitefly reproduction-related genes (BtPLA, BtJHAMT, BtFPPS, BtPER, BtSPN, BtELOVL, BtAPN), whereas SlHIDH silencing abolished this effect and led to their upregulation. In artificial feeding assays, dietary genistein reduced oviposition by 32.9% and ovariole formation by 19.6%. Our findings demonstrate that B. bassiana elevates genistein levels in tomato, which impairs whitefly ovarian development and reproduction via endocrine disruption. These results reveal a tripartite interaction in which EPF enhances plant defense through specific secondary metabolites that target insect reproductive physiology, providing molecular insights for improving biocontrol strategies against sap-sucking pests.