The transmission dynamics of insect-vectored diseases are determined by complex interactions among pathogens, hosts, and vectors. A growing number of studies have documented effects of vector-borne pathogens on phenotypic traits of their primary hosts (e.g. chemical cues) that influence the frequency and nature of interactions with vectors, with implications for pathogen transmission. But while many key interactions among hosts and vectors are mediated by chemical cues and signals, there has been little work to date on the chemical ecology of insect-vectored diseases. In this study, we examined the chemical mediation of interactions among a widespread plant pathogen, the non-persistently transmitted Cucumber mosaic virus (CMV), a common host plant, squash (Cucurbita pepo), and two aphid vectors (Myzus persicae and Aphis gossypii). Chemical analyses were performed to document virus-induced changes in plant volatile emissions (odors), nutritional status (levels of key amino acids) and defense signaling (hormones). Further analyses explored the impacts of these changes on aphid vector behavior (long- and short-range attraction/repulsion) and performance (population growth).
Results/Conclusions
Our results indicate that CMV infection reduces host plant quality for aphids and that aphids rapidly disperse from infected plants. Yet, individuals of both aphid species were nevertheless attracted to the elevated volatile emissions of infected plants. These results suggest that CMV induces a plant phenotype conducive to its non-persistent mode of transmission and different from that previously reported for other plant viruses that require more sustained aphid feeding for effective transmission. Chemical analysis of infected and healthy plants documented several key differences in plant hormones and amino acid levels contributing to this phenotype. Infected plants exhibited reduced levels of amino acids in the phloem, including several essential amino acids and others necessary for the synthesis of essential amino acids by mutualistic bacterial symbionts. Additionally, we detected elevated levels of polyunsaturated C-18 fatty acids, which serve as precursors for a number of defense compounds and defense-related signaling pathways, including those regulating volatile emissions. Taken together, our findings suggest that CMV induces changes in host plant traits that are conducive to vector transmission and, more generally, that the transmission mode may play an important role in shaping pathogen-induced changes in host phenotypes.
