Saliva-Mediated Contrasting Effects of Two Citrus Aphid Species on Asian Citrus Psyllid Feeding Behavior and Plant Jasmonic Acid Pathway

SIMPLE SUMMARY: The Asian citrus psyllid, Diaphorina citri Kuwayama, is one of the most important citrus pests because it transmits the bacterium that causes citrus Huanglongbing during feeding. The saliva of herbivorous insects can modulate plant defenses and, in turn, impact insect fitness, which is mostly studied in insects feeding on herbaceous plants. The role of saliva in the relationship between the Asian citrus psyllid and its woody host plant citrus, on the other hand, is unknown. Because two citrus aphid species, Aphis spiraecola Patch and Aphis (Toxoptera) citricidus (Kirkaldy), have a contrasting impact on the performance of subsequently infested D. citri, we explored the role of their saliva on D. citri feeding behavior and host plant defenses. We found that the infiltrating saliva of A. spiraecola into the host citrus leaves of the psyllid disrupted the subsequent feeding behavior of D. citri and also activated the expression of genes involved in plant salicylic acid (SA) and jasmonic acid (JA) defense pathways. By contrast, saliva infiltrations of A. citricidus (Kirkaldy) promoted D. citri feeding, activated the expression of one gene involved in the SA pathway, and repressed several genes involved in the JA pathway. We demonstrate that the saliva of aphids can affect D. citri performance, possibly by modulating plant defenses. This is the first study to show that insect saliva can influence D. citri feeding behavior by changing plant defenses. ABSTRACT: While herbivorous insect saliva plays a crucial role in the interaction between plants and insects, its role in the inter-specific interactions between herbivorous insects has received little attention. Pre-infestation of citrus plants with Aphis spiraecola Patch and Aphis (Toxoptera) citricidus (Kirkaldy) exhibited positive and negative effects on the performance (feeding and reproduction) of Diaphorina citri Kuwayama. We explored the role of saliva in this plant-mediated interaction by infiltrating fresh and boiled aphid saliva into plants and detecting D. citri feeding behavior and citrus plant defense response. Leaf infiltration of A. spiraecola saliva disrupted the subsequent feeding of D. citri, indicated by prolonged extracellular stylet pathway duration and decreased phloem sap ingestion duration. By contrast, infiltration of A. citricidus saliva decreased the duration of the extracellular stylet pathway and phloem sap ingestion of D. citri. Furthermore, gene expression analysis showed that several salicylic acid (SA)- and jasmonic acid (JA)-pathway-related genes were activated by A. spiraecola saliva infiltration. However, two SA-pathway-related genes were activated and three JA-pathway-related genes were suppressed following A. citricidus saliva infiltration. Treatment with boiled saliva did not similarly impact D. citri feeding behavior or plant defense response. This study suggests that salivary components (those that can be inactivated by heating) from two citrus aphid species differently affect plant defenses and that they were responsible for the contrasting plant-mediated effects of two citrus aphids on the feeding behavior of D. citri. This study indicates a novel three-way citrus aphid–plant–citrus psyllid interaction.