Vermicompost Amendments Disrupt Feeding Behavior of Diaphorina citri Kuwayama and Boost Activities of Salicylic Acid and Jasmonic Acid Pathway-Related Enzymes in Citrus

SIMPLE SUMMARY: Diaphorina citri Kuwayama is a phloem-feeding insect that uses piercing–sucking mouthparts to ingest phloem sap from plants. It is the most common citrus pest because it spreads the bacteria that causes huanglongbing during the probing and feeding process. Nowadays, eco-friendly methods such as soil amendment with vermicompost are gaining popularity in the integrated management of D. citri. Here, we investigated why vermicompost amendments cause negative effects to D. citri. We observed that vermicompost disrupted D. citri feeding behavior, particularly for the variables related to phloem sap ingestion, with a significant reduction in the duration of phloem sap ingestion as well as a longer time spent to reach and gain access to phloem sap. Additionally, we demonstrated that vermicompost amendments increased plant defense-associated enzyme activities. We speculate that vermicompost amendments enhance plant resistance against D. citri, which disrupts the insect feeding and eventually impairs the performance of D. citri. Furthermore, we showed how vermicompost amendments affect the feeding behavior of piercing–sucking insects for the first time, and the feeding behavior (decreased efficiency of phloem sap ingestion) suggests vermicompost may suppress the transmission of huanglongbing bacteria by D. citri, yet it still needs to be further studied. ABSTRACT: Plants grown with vermicompost amendments are known to be harmful to sap-sucking insects, but the underlying mechanism remains to be determined. Here we investigated the feeding behavior of Diaphorina citri Kuwayama on Citrus limon (L.) Burm. F using the electrical penetration graph technique. Plants were grown in soil with different vermicompost rates (0%, 20%, 40%, and 60% w/w). Additionally, plants were tested for the activity of salicylic acid (SA) and jasmonic acid (JA) pathway-related enzymes. When compared to the control, vermicompost treatments (40% and 60%) decreased duration of phloem sap feeding and increased duration of the pathway phase of D. citri, and the 60% vermicompost made it more difficult for D. citri to reach and gain access to phloem sap. Enzymatic assays indicated that the 40% amendment rate increased phenylalanine ammonia lyase (involved in the SA pathway) and polyphenol oxidase (involved in the JA pathway), while the 60% amendment rate increased -1,3-glucanases (involved in the SA pathway) and lipoxygenase (involved in the JA pathway). The 20% amendment rate had no effect on feeding or enzyme activities. This study revealed that vermicompost amendments can reduce the efficiency of D. citri feeding, which may result from increased plant resistance via the SA and JA pathway.