Rice Defense Responses Orchestrated by Oral Bacteria of the Rice Striped Stem Borer, Chilo suppressalis

Plant defenses in response to chewing insects are generally regulated by jasmonic acid (JA) signaling pathway, whereas salicylic acid (SA) signaling is mainly involved in plant defense against biotrophic pathogens and piercing-sucking insects. Previous studies showed that both JA- and SA-related defenses in rice plants were triggered by the infestation of the rice striped stem borer (SSB, Chilo suppressalis), a destructive pest causing severe damage to rice production. Herbivore-associated microbes play an important role in modulating plant–insect interaction, and thus we speculate that the SSB symbiotic microbes acting as a hidden player may cause this anomalous result. The antibiotics (AB) treatment significantly depressed the performance of field-collected SSB larvae on rice plants, and reduced the quantities of bacteria around the wounds of rice stems compared to non-AB treatment. In response to mechanical wounding and oral secretions (OS) collected from non-AB treated larvae, rice plants exhibited lower levels of JA-regulated defenses, but higher levels of SA-regulated defenses compared to the treatment of OS from AB-treated larvae determined by using a combination of biochemical and molecular methods. Among seven culturable bacteria isolated from the OS of SSB larvae, Enterobacter and Acinetobacter contributed to the suppression of JA signaling-related defenses in rice plants, and axenic larvae reinoculated with these two strains displayed better performance on rice plants. Our findings demonstrate that SSB larvae exploit oral secreted bacteria to interfere with plant anti-herbivore defense and avoid fully activating the JA-regulated antiherbivore defenses of rice plants.