The soybean aphid (Aphis glycines) is an important insect pest of soybean (Glycine max). Previously, jasmonic acid (JA) was shown to elicit effective plant defense responses against soybean aphids. However, aphids were able to attenuate wound- or JA-induced responses in infested leaves in the compatible interaction and the mechanism of suppression remained uncharacterized. We hypothesized that aphids induce a decoy pathway to suppress plant defense responses and showed that aphids exploit the abscisic acid (ABA) pathway to suppress JA-mediated signaling. Both endogenous and exogenous ABA suppressed the wound-induced JA response. Furthermore, aphid populations were significantly reduced in the absence of a functional ABA biosynthetic (aba2 RNAi) or signaling (scof-1 RNAi) pathway and attenuation of JA responses by aphids was abolished in these mutants.

Suppression of defenses by aphids could result in susceptibility toward other pests infesting the plant. Previously, soybean aphid feeding was shown to facilitate the performance of other soybean aphid biotypes or soybean cyst nematodes (Heterodera glycines) on uninfected systemic leaves or roots of soybean, respectively. Therefore, it is critical to understand the impact of soybean aphids on a whole-plant level, including the plant-mediated response triggered on uninfested plant tissues. We quantified aphid-induced transcriptome changes in locally infested leaves and systemic roots during an early (12 hours) and late (7 days) aphid infestation. Our results suggest that leaves and roots have distinct responses to foliar soybean aphid feeding and the plant response is highly variable across time. Aphids caused delayed onset of defenses and a growth-defense tradeoff in locally infested leaves. Most interestingly, foliar feeding by soybean aphids triggered the transient repression of widespread defense responses in roots.

This report provides the first genetic evidence of aphid counter-defense mechanisms in soybean and begins to unravel the systemic plant response to soybean aphids. Aphids use host ABA signaling to suppress plant defense responses in locally infested tissues but this does not seem to be the case in the transient suppression of root defense transcripts. Thus, suppression of defenses in uninfected tissues caused by soybean aphids likely occurs via different mechanisms.