Upregulation of Three NAC Genes in Cucumber Grafted on Figleaf Gourd Contributes to Enhanced Resistance Against FOC Infection

Cucumber Fusarium wilt, which is induced by the soil-borne pathogen Fusarium oxysporum f. sp. Cucumerinum (FOC), represents a highly destructive disease. Cucumber seedling grafted onto figleaf gourd (Cucurbita ficifolia Bouché) rootstock (CFC) demonstrated better resistance to FOC. However, the molecular mechanism underlying this enhanced disease resistance capability is largely unknown. To elucidate this, we performed transcriptome, small RNA, and degradome sequencing for leaves from CFC and self-grafted cucumbers (SGC) as controls, with and without FOC infections, respectively. Our results indicated that three NAC genes, all predicted as targets of csa-miR164, were significantly up-regulated in CFC after FOC infection. Co-transformation assay in Nicotiana benthamiana confirmed that csa-miR164f directly inhibits NAC2, and transient overexpression of NAC2 in cucumber enhanced resistance to FOC, supporting its positive role in defense. Therefore, our results suggest that three NACs, upregulated in CFC, as an alternative pathway, enhance the reactive oxygen species burst and hypersensitive response, which further elevates the resistance to FOC infection. These results provide new insights into the molecular basis for improved FOC resistance in CFC.