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

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.