Tissue-specific regulation of volatile emissions moves predators from flowers to attacked leaves

Abstract

Plant-predator mutualisms have been widely described in nature.1,2 How plants fine-tune their mutualistic interactions with the predators they recruit remains poorly understood. In the wild potato (Solanum kurtzianum), predatory mites, Neoseiulus californicus, are recruited to flowers of undamaged plants but rapidly move downward when the herbivorous mites, Tetranychus urticae, damage leaves. This "up-down" movement within the plant corresponds to the shift of N.californicus from palynivory to carnivory, as they change from feeding on pollen to herbivores when moving between different plant organs. This up-down movement of N.californicus is mediated by the organ-specific emissions of volatile organic compounds (VOCs) in flowers and herbivory-elicited leaves. Experiments with exogenous applications, biosynthetic inhibitors, and transient RNAi revealed that salicylic acid and jasmonic acid signaling in flowers and leaves mediates both the changes in VOC emissions and the up-down movement of N.californicus. This alternating communication between flowers and leaves mediated by organ-specific VOC emissions was also found in a cultivated variety of potato, suggesting the agronomic potential of using flowers as reservoirs of natural enemies in the control of potato pests.