Abstract
Herbivorous insect pests are responsible for 18-20% of crop yield losses worldwide. Spodoptera frugiperda (Lepidoptera: Noctuidae), the fall armyworm (FAW), a polyphagous insect native to the Americas, has recently spread worldwide, posing a threat to global food security. It is mainly detected on Poaceae, such as maize (Zea mays) and sporadically on rice (Oryza sativa). Recognition of insect attack by the plant is mediated by Damage-Associated Molecular Patterns (DAMPs) produced at the time of wounding and Herbivore-Associated Molecular Patterns (HAMPs) present in oral secretions (OS), leading to the induction of a defense response. Recent studies have shown that some insects can circumvent these defenses via their oral microbiota by suppressing the pathway/accumulation of jasmonate (JA), a key phytohormone in the herbivory response. Our aim is to determine whether the FAW oral microbiota interferes with defenses and modulates the JA pathway in rice, to identify the microbial and molecular players in this tripartite interaction and to measure the benefit to the insect in suppressing this pathway. To this end, we simulated a caterpillar attack on rice leaves via mechanical wounding followed by OS deposition, and analyzed the modulation of rice defense responses by global transcriptomic analysis (RNA-seq). We identified a set of genes whose expression is specifically induced by wounding, OS and/or co-modulated by both. To study the impact of microbiota, we fed larvae an antibiotic-treated artificial diet and harvested dysbiotic OS that we deposited on rice leaves. We thus identified a list of 33 genes specifically inhibited by the OS microbiota, including genes involved in JA biosynthesis. An HPLC approach showed us a strong biochemical impact with the suppression of JA accumulation by the microbiota. Contact between insects and JA-deficient WT and mutant rice showed a reduced effect of JA on insect weight gain. A transcriptomic analysis comparing WT and JA-deficient rice shows the influence of JA in the plant's response to FAW herbivory. The JA pathway is responsible for the induction of numerous defense genes, notably those encoding ROS and TPS, but not for direct defense responses. Characterization of the OS microbiota revealed Enterococcus mundtii as the main OS symbiont. We still need to understand how this bacterium is able to specifically inhibit JA biosynthesis in FAW host plants.