Unraveling arbuscular mycorrhizal fungi-induced resistance of purple branch rose (Rosa rugosa ‘Zizhi’) to Lymantria dispar based on metabolomics

Currently, people primarily rely on chemical pesticides to prevent and control insect pests, which not only introduce problems with environmental pollution but also produce chemical residues that will make it difficult to guarantee the safety of edible plants. Arbuscular mycorrhizal fungi (AMF) are soil microorganisms that form a symbiotic relationship with plants, which improves plant resistance. This natural phenomenon provides new ideas for eco-friendly biological control. The present study assessed the effects of AMF (Funneliformis mosseae, Rhizophagus intraradices and their combination) inoculation on rose growth and its resistance to gypsy moth larvae (Lymantria dispar) by investigating the growth performance and metabolomics of rose plants and the growth and physiological parameters of gypsy moth larvae. AMF inoculation improved the growth of both the aboveground and belowground parts of the rose plants. The developmental duration of gypsy moth larvae feeding on mycorrhizal rose leaves was prolonged by 4.8–5.8 days. Moreover, feeding on mycorrhizal rose leaves significantly reduced the body weight of the gypsy moth larvae by 9–24%, body length by 4–6%, and the width of head sheath by 11–15%. The superoxide dismutase (SOD) and carboxylesterase (CarE) enzymes in the larvae that fed on the leaves of mycorrhizal rose were significantly higher than those in the control, while the acid phosphatase (ACP) was inhibited (P < 0.05). Peroxidase (POD) and alkaline phosphatase (AKP) in larvae that fed on mycorrhizal rose leaves were significantly higher than those in the control at 5 days. Glutathione S transferases (GSTs) were significantly higher than the control at 3 and 5 days. Metabolomics analyses showed that inoculation with AMF promoted the accumulation of jasmonic acid (JA) and abscisic acid (ABA) in rose leaves. The treatment groups were 1.6- and 3.4-fold higher than those of the control, respectively. The AMF significantly regulated 1,589 metabolites in rose leaves. The AMF promoted the accumulation of flavonoids and inhibited the accumulation of glycosides in rose leaves. A total of 19 metabolites that significantly correlated with the growth and development of gypsy moths were screened out. Among ABA, glycerophosphocholine, 1-(sn-glycero-3-phospho)-1D-myo-inositol, (-)-catechin, N-acetyl-D-glucosamine 6-phosphate, 3-(4-hydroxyphenyl)-1-propanol and 3-trans-caffeoyltormentic acid were significantly different from those of the control. These compounds may play a role in the resistance of rose to gypsy moth induced by AMF. In conclusion, AMF inoculation improved the resistance of R. rugosa to L. dispar through modifications on the metabolism and physiology. These findings highlight the interaction of “mycorrhizal-plant-insect”. It provides a reference for the application of AMF to control plant pest.