Virus-induced changes in host plant phenotype cue behavioral changes in Aphis glycines that enhance acquisition and transmission of soybean mosaic virus

Vector-borne viruses can modify the phenotype of their host plants to manipulate the behavior of their vectors and maximize their dissemination. The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is a primary vector of soybean mosaic virus (SMV), a non-persistent potyvirus that is a serious disease of soybean. We investigated mechanisms by which SMV changes A. glycines feeding and dispersal behavior via virus-induced modifications of plant phenotype. These changes affect gustatory, visual and olfactory cues that alter the behavior of both viruliferous and virus-free aphids to enhance virus acquisition and transmission. SMV-infected soybean seedlings exhibited up-regulation of the amino acids threonine and tyrosine which rendered viruliferous aphids more restless and prone to dispersal. Whereas dispersing viruliferous A. glycines preferred to settle and feed on virus-free soybean seedlings, virus-free aphids preferred SMV-infected seedlings. Volatile cues emanating from SMV-infected seedlings, primarily up-regulated methyl salicylate and down-regulated (Z)-3-hexen-1-ol, were implicated in repulsion of viruliferous aphids, whereas the mottled yellow coloration of SMV-infected seedlings was a visual attractant for aphids regardless of virus status. Our results reveal how a non-persistent virus uses multimodal 'push and pull' mechanisms to manipulate vector behavior for its own benefit, and suggests new avenues for exploring the mechanisms of altered behavior in viruliferous aphids.