Beyond a dual role: how <i>Purpureocillium lilacinum</i> reprograms citrus metabolism for integrated biocontrol and growth promotion

BACKGROUND: Plants harbor complex microbial communities that are fundamental to their health and productivity. Among them, endophytic fungi such as Purpureocillium lilacinum establish mutualistic associations, offering dual benefits as plant growth promoters and biocontrol agents. However, the potential of this fungus in citrus cultivation and the metabolic dynamics of its interaction with citrus hosts remain unexplored. This study employed an integrated dual metabolomics approach to investigate the symbiosis between P. lilacinum and Citrus aurantium. It was hypothesized that the fungus would enhance plant performance through its own bioactive metabolites, and also by systemically reprogramming the host metabolism. To test this hypothesis, the in vitro fungal metabolome was characterized, plant growth promotion was evaluated in vivo, and metabolomic shifts in host tissues were analyzed. RESULTS: The results reveal a multilayered mode of action. Purpureocillium lilacinum stimulated plant growth directly through nutrient solubilization and phytohormone modulation. Concurrently, the fungus engaged in active metabolic cross-talk with the host, reprogramming primary metabolism, as exemplified by the spatial redistribution of amino acids like proline and arginine, and activating secondary defense pathways. The fungal metabolome also revealed a direct biocontrol arsenal, including insect-modulating acetophenone and the insecticidal alkaloid arecoline, underscoring its capacity for immediate antagonism. CONCLUSION: These findings provide novel insights into the biochemical mechanisms underlying P. lilacinum-citrus interactions. They confirm the role of the fungus in orchestrating a synergized growth-and-defense response in citrus, highlighting its strong potential as a sustainable, multi-functional bioinoculant for citrus production systems. © 2026 The Author(s). Journal of the Science of Food and Agriculture published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.