Virus effects on plant chemistry and vector behavior vary with host environment and virus genotype

Background/Question/Methods

Vector-borne parasites may alter host traits in ways that influence the frequency and nature of interactions between hosts and vectors, with implications for transmission. However, only a handful of studies have explored pathogen effects on chemically-mediated interactions between plants and vector insects. Our previous work with the FNY strain of Cucumber mosaic virus (CMV) has shown that this virus alters squash host volatile emissions, nutritional quality, and defense responses in ways that favor the attraction of vectors to infected plants, followed by rapid dispersal after simultaneous acquisition of taste cues and virions. However, CMV exhibits considerable genotypic diversity and most genotypes are capable of infecting hosts across multiple families. To explore broader patterns of host manipulation by CMV, we acquired additional CMV genotypes from different geographic areas and host species. We performed biochemical analyses to measure host volatile emissions and levels of key nutrients for each genotype infecting the native host (from which it was isolated) and a novel host from a different plant family. Using this same native/novel host design, we also evaluated vector performance on and emigration behavior from sick and healthy hosts, and investigated the adaptive significance of virus-induced changes in plant chemistry for each pathogen-host-vector combination.

Results/Conclusions

Our results suggest that CMV induces changes in native hosts that are conducive to vector attraction and subsequent rapid dispersal after acquisition of taste cues – a condition that is optimal for transmission of non-persistently transmitted viruses like CMV. When an isolate is infecting a native host, volatile emissions are qualitatively similar in identity and relative compound ratios to those of healthy plants, but elevated in amount, creating a stronger signal for foraging aphid vectors. However, when an isolate is placed in a novel host, emissions are qualitatively different from those of healthy plants and compound ratios are altered. In native hosts, CMV reduces host plant quality for aphid vectors, leading to higher rates of dispersal of winged aphids from infected plants after acquisition of taste cues (and virions). However, in novel hosts, CMV increases host plant quality for aphids, resulting in retention of vectors on virus-infected plants after acquisition of taste cues/virions. Our results indicate that CMV variants have different effects on host plant chemistry and transmission-relevant vector behaviors depending on the particular CMV-host combination. These results are discussed in the context of effects on CMV fitness in different plant communities.