Manipulation of aphid behavior by a persistent plant virus.

Plants are frequently infected with cytoplasmic RNA viruses that persist for many generations through nearly 100% vertical transmission without producing any symptoms. Movement between plant cells and horizontal transmission has not been observed in these viruses; instead they are distributed to all host cells through host cell division. Jalapeño peppers ( Capsicum annuum ) are all infected with Pepper cryptic virus 1 (PCV 1, family Partitiviridae ). We compared the effect of odor cues from PCV 1 infected (J+) and virus free (J-) Jalapeño pepper on the aphid Myzus periscae , a common vector of acute plant viruses. Pairwise preference experiments showed a stark contrast to insect-plant interactions in acute virus infections: virus infected plants deterred aphids. The acute plant virus Cucumber mosaic virus (CMV) manipulates its host's volatile emission to attract aphid vectors and facilitate its transmission. We inoculated J+ and J- with CMV. Volatiles of J+ and J- CMV infected plants were more attractive to aphids than J+ and J- mock inoculated plants. However, in pairwise preference between J+ CMV- and J- CMV-infected plants, aphids preferred the J- CMV volatile blend. Aphid reproduction on J+ and J- plants was measured as an indicator for the effect of PCV 1 on host quality for aphids. Aphid reproduction on J+ plants was more than two fold lower than on J- plants. IMPORTANCE This study demonstrates that a plant persistent virus can manipulate aphid behavior. This manipulation is in stark contrast with previously described effects of acute viruses on their host to facilitate their transmission. This study demonstrates a positive relationship between Pepper cryptic virus 1 and Jalapeño pepper plants by protecting the plants from the vector of acute viruses, and reducing aphid herbivory. This work reveals an important implication of persistent plant viruses for pest and pathogen management in agriculture.