Ferritin From Striped Stem Borer (Chilo suppressalis) Oral Secretion Acts as an Effector Helping to Maintain Iron Homoeostasis and Impair Defenses in Rice

The striped stem borer (Chilo suppressalis, SSB) is a highly destructive insect pest in rice (Oryza sativa). SSB oral secretions (OSs) can induce plant defense responses in rice. However, the specific effectors in SSB OSs that mediate these interactions with rice remain poorly understood. In this study, hallmarks of ferroptosis-like plant defense response, such as the reprogramming of ferroptosis-related genes, reduced glutathione levels, accumulation of ferric ion, and enhanced lipid peroxidation by reactive oxygen species (ROS), were detected in rice subjected to SSB infestation and SSB OSs treatment. Furthermore, we identified and characterized a protein from SSB OSs, the ferritin CsFer1, which plays a critical role in the regulation of plant iron homoeostasis. CsFer1 was shown to possess Fe2+ binding capacity and ferroxidase activity. Through recombinant CsFer1 protein treatment, overexpression of CsFer1 in rice and SSB larvae with silencing CsFer1 feeding in rice, we found that CsFer1 helped maintain iron homoeostasis under SSB infestation, suppressing H2O2 and JA accumulation, ultimately compromising rice resistance to herbivorous pests. Moreover, such a phenomenon about the regulation of iron homoeostasis and suppression of insect resistance was observed in the CsFer1 overexpressed tobacco. Collectively, these findings suggest that CsFer1 functions as an effector involved in the regulation of iron homoeostasis- and lipid peroxidation-related plant defense during plant-insect interaction.