Epiphytic Fungi Can Drive a Trade-Off Between Pathogen and Herbivore Resistance in Invasive Ipomoea cairica

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 <i>Fusarium oxysporum</i> and <i>Fusarium fujikuroi</i> can drive the trade-off between the two defense traits in invasive <i>Ipomoea cairica</i>. Surface-sterilized <i>I. cairica</i> 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 <i>Colletotrichum gloeosporioides</i> infection. On the contrary, E+ cuttings had higher absolute and relative fresh weight losses per leaf than E- cuttings after <i>Taiwania circumdata</i> 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>I. cairica</i> 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>I. cairica</i>.