Global transcriptional and metabolic reprogramming underlies Fusarium wilt resistance in figleaf gourd (Cucurbita ficifolia)

Fusarium wilt, caused by Fusarium oxysporum f. sp. cucumerinum (FOC), poses a major threat to economically important crops worldwide. Figleaf gourd (Cucurbita ficifolia) has been widely adopted as a rootstock for FOC-susceptible cucumber (Cucumis sativus) due to its strong resistance, although the underlying molecular mechanisms remain elusive. In this study, we leveraged the contrasting FOC resistance between C. ficifolia and C. sativus to perform a comparative analysis aimed at elucidating the molecular basis of Fusarium wilt resistance in C. ficifolia. Compared to C. sativus, resistant C. ficifolia exhibited milder wilting, enhanced antioxidant enzyme activities, and reduced oxidative damage. Transcriptome profiling revealed 1,599 species-specific expressed genes and 3,379 orthologous genes with interspecies expression divergence. Several key defense-related pathways, such as MAPK signaling and plant–pathogen interaction, contained critical node genes that exhibited species-specific regulation, potentially contributing to the enhanced resistance of C. ficifolia. This global divergence in gene expression was associated with distinct metabolic shifts, leading to the specific activation of defense-related metabolic pathways in C. ficifolia and the subsequent accumulation of protective compounds such as brassinosteroids, phenylpropanoids, and flavonoids. These findings indicate that C. ficifolia's superior FOC resistance is not attributable to a single factor but emerges from a sophisticated orchestration of gene expression and metabolic output. This study provides novel molecular insights into Fusarium wilt resistance and offers candidate genes and metabolic targets for breeding disease-resistant cucurbit crops.