Trade-offs between different defense traits exist commonly in plants. However, no evidence suggests that symbiotic microbes can drive a trade-off between plant pathogen and herbivore defense. The present study aims to investigate whether the mixture of epiphytic Fusarium oxysporum and Fusarium fujikuroi can drive the trade-off between the two defense traits in invasive Ipomoea cairica. Surface-sterilized I. cairica cuttings pre-inoculated with the epiphytic fungal mixture served as an epiphyte-inoculated (E+) group, while cuttings sprayed with sterile PDB served as an epiphyte-free (E−) group. After 3 days of incubation, E+ and E− cuttings were subjected to the challenge from a fungal pathogen and an insect herbivore, respectively. The results suggested that E+ cuttings had less rotted and yellowed leaf rates per plant than E− cuttings after Colletotrichum gloeosporioides infection. On the contrary, E+ cuttings had higher absolute and relative fresh weight losses per leaf than E− cuttings after Taiwania circumdata introduction. In the absence of challenges from the two natural enemies, salicylic acid and H2O2 accumulation occurred in E+ cuttings, which activated their SA-dependent pathogen defense and resulted in an increase in chitinase and β-1,3-glucanase activities. Although jasmonic acid accumulation also occurred in E+ cuttings, their JA-dependent herbivore defense responses were antagonized by SA signaling, leading to a decrease in total phenol content and phenylalanine ammonia-lyase activity. The activity of generalized defense enzymes, including superoxide dismutase, peroxidase, and catalase, did not differ between E+ and E− cuttings. Together, our findings indicate that a trade-off between pathogen and herbivore defense in I. cairica had already been driven by the epiphytic fungal mixture before the challenge by the two natural enemies. This study provides a novel insight into biocontrol strategies for I. cairica.
