Bikaverin as a molecular weapon: enhancing Fusarium oxysporum pathogenicity in bananas via rhizosphere microbiome manipulation.

BACKGROUND: Fusarium wilt, caused by Fusarium oxysporum f. sp. cubense Tropical Race 4 (Foc TR4), poses a severe threat to global banana production. Secondary metabolites are critical tools employed by pathogens to interact with their environment and modulate host-pathogen dynamics. Bikaverin, a red-colored polyketide pigment produced by several Fusarium species, has been studied for its pharmacological properties, but its ecological roles and impact on pathogenicity remain unclear. RESULTS: This study investigated the role of bikaverin in Foc TR4, focusing on its contribution to pathogenicity and its interaction with the rhizosphere microbiome. Pathogenicity assays under sterile and autoclaved conditions demonstrated that bikaverin does not directly contribute to pathogenicity by affecting the infection process or damaging host tissues. Instead, bikaverin indirectly enhances Foc TR4's pathogenicity by reshaping the rhizosphere microbiome. It suppresses beneficial plant growth-promoting rhizobacteria, such as Bacillus, while promoting the dominance of fungal genera, thereby creating a microbial environment beneficial for pathogen colonization and infection. Notably, bikaverin biosynthesis was found to be tightly regulated by environmental cues, including acidic pH, nitrogen scarcity, and microbial competition. Co-culture with microbes such as Bacillus velezensis and Botrytis cinerea strongly induced bikaverin production and upregulated expression of the key bikaverin biosynthetic gene FocBik1. In addition, the identification of bikaverin-resistant Bacillus BR160, a strain with broad-spectrum antifungal activity, highlights its potential as a biocontrol agent for banana wilt management, although its stability and efficiency under field conditions require further validation. CONCLUSIONS: Bikaverin plays an indirect yet important role in the pathogenicity of Foc TR4 by manipulating the rhizosphere microbiome. This ecological function underscores its potential as a target for sustainable disease management strategies. Future research should focus on elucidating the molecular mechanisms underlying bikaverin-mediated microbial interactions, using integrated approaches such as transcriptomics and metabolomics. Together, these findings provide a foundation for novel approaches to combat banana wilt disease and enhance crop resistance. Video Abstract.