Raspberry viruses manipulate plant–aphid interactions

Plants come under attack by a variety of organisms, including insects and pathogenic microorganisms such as viruses. Plant viruses can interact indirectly with their vectors by inducing changes to plant chemistry which may alter its attractiveness as a host for herbivore vectors. Using red raspberry as a study system, this study aimed to investigate the host plant mediated interactions occurring between the large raspberry aphid, Amphorophora idaei, and two of the viruses that it transmits, Black raspberry necrosis virus (BRNV) and Raspberry leaf mottle virus (RLMV). In whole plant bioassays, BRNV and RLMV-infected plants were shown to be initially more attractive to A. idaei and aphids remained on the initially selected host plant for a period of approximately 30 minutes. In addition, A. idaei took three days longer to reach reproductive maturity compared with those feeding on non-infected plants, suggesting a virally-induced manipulation of aphid behaviour whereby a deceptive attraction of the vector to a host plant found to be nutritionally poor, presumably acts to promote virus transmission. Investigations of the underlying plant chemistry revealed that raspberry viruses may be capable of facilitating aphid feeding by reducing leaf phenolic concentration when aphids are feeding and that infection with BRNV and RLMV resulted in significantly elevated levels of carbon and free amino acids in the leaves. While increased concentrations of amino acids might be expected to promote aphid performance, the amino acid composition was dominated by glutamate (77% of total content of infected plants), a previously suggested indicator of reduced host-plant suitability for aphids. Volatile entrainments from virus-infected plants showed elevated levels of the green leaf volatile (Z)-3-hexenyl acetate. Bioassays subsequently revealed that this compound acted as an aphid attractant at a concentration of 50 ng ml-1 but that aphid behaviour was unaffected by lower concentrations. The combined utilisation of PCR diagnostics developed from newly sequenced viral genomes and the implementation of a non-invasive, targeted method of sampling plant headspace volatiles enabled this study to provide novel insights into the nature of host plant mediated interactions between aphids and the viral pathogens that they transmit.