Biochemical and physiological mechanisms underlying effects of Cucumber mosaic virus on host-plant traits that mediate transmission by aphid vectors

The transmission of insect-vectored diseases entails complex interactions among pathogens, hosts and vectors. Chemistry plays a key role in these interactions; yet, little work has addressed the chemical ecology of insect-vectored diseases, especially in plant pathosystems. Recently, we documented effects of Cucumber mosaic virus (CMV) on the phenotype of its host (Cucurbita pepo) that influence plant-aphid interactions and appear conducive to the non-persistent transmission of this virus. CMV reduces host-plant quality for aphids, causing rapid vector dispersal. Nevertheless, aphids are attracted to the elevated volatile emissions of CMV-infected plants. Here, we show that CMV infection (1) disrupts levels of carbohydrates and amino acids in leaf tissue (where aphids initially probe plants and acquire virions) and in the phloem (where long-term feeding occurs) in ways that reduce plant quality for aphids; (2) causes constitutive up-regulation of salicylic acid; (3) alters herbivore-induced jasmonic acid biosynthesis as well as the sensitivity of downstream defences to jasmonic acid; and (4) elevates ethylene emissions and free fatty acid precursors of volatiles. These findings are consistent with previously documented patterns of aphid performance and behaviour and provide a foundation for further exploration of the genetic mechanisms responsible for these effects and the evolutionary processes that shape them. This study explores the biochemical mechanisms underlying the influence of a widespread plant pathogen, the non-persistently transmitted Cucumber mosaic virus (CMV), on aspects of host-plant phenotype that influence interactions with aphid vectors. This virus has previously been shown to enhance the attractiveness of plants for aphids (via volatile cues), while simultaneously reducing host plant palatability and quality (stimulating dispersal and virus transmission). Our current results demonstrate that CMV infection reduces host plant quality by altering ratios of carbohydrates to free amino acids in both non-vascular cells (those first sampled by aphids and from which virions are acquired) and in phloem sap, and that infection results in an increase in organic volatile precursors and herbivore defense signaling molecules both constitutively and in response to aphid damage. These changes are consistent with observed effects on host-plant phenotype and patterns of vector behavior, as well as with existing knowledge about the use of host plant resources by CMV during replication and systemic spread. Our results thus provide new insight into the transmission ecology of a multi-host plant pathogen of significant economic and ecological importance.