Early modulation of the jasmonate pathway in rice (Oryza sativa) by the oral microbiota of Spodoptera frugiperda larvae

International audience

English. Plant-insect interactions cause significant yield losses ranging from 18 to 20% in crops. Spodoptera frugiperda (Lepidoptera: Noctuidae), a polyphagous insect native to the Americas, has recently spread throughout the world, posing a threat to global food security. It is mainly detected on Poaceae such as maize (Zea mays) and sporadically on rice (Oryza sativa) which seems to be a deleterious plant for this species. The recognition of the insect by the plant will be done via the Damage Associated Molecular Patterns (DAMPs) produced at the time of the wound and the Herbivore Associated Molecular Patterns (HAMPs) present in the oral secretions (OS), which will lead to the induction of defense response. Recent studies have shown that some insects can circumvent these defenses via the oral microbiota by suppressing the jasmonate (JA) pathway central to the herbivory response. Our objective is to determine whether the oral microbiota of S. frugiperda modulates the JA pathway in rice and to identify the microbial and molecular players in this tripartite interaction and to investigate the advantage of 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 the response to DAMPs, HAMPs and co-modulated by DAMPs and HAMPs. We then characterized the OS microbiota via a metabarcoding approach and identified Enterococcus mundtii as the dominant bacterium. To study the impact of the microbiota on the JA pathway, we fed the larvae an antibiotic-treated artificial diet and harvested dysbiotic OS that we deposited on rice leaves. We thus obtain a low transcriptomic impact of the dysbiotic microbiota with a modulation of 33 genes. However, an HPLC approach showed us a strong biochemical impact with a suppression of the JA pathway by the microbiota. A contact between insects and WT and mutant JA-deficient rice showed a reduced effect of JA on the insects' weight gain. The next step will be to determine the bacterium responsible for this suppression with E. mundtii as the first candidate.