A host-specialized aphid lineage helps another conspecific lineage utilize a new host by disrupting the plant defenses

Polyphagous aphids often have host-specialized lineages, and the mechanisms remain to be elucidated. The aphid Aphis gossypii has several host-specialized lineages including one specialized on Cucurbitaceae and one on Malvaceae. We found that the performance of Malvaceae lineage was poor on cucumbers, but significantly improved on cucumbers that were previously infested by Cucurbit lineage for 14 d. Following two-generation feeding experience on pre-infested cucumbers, Malvaceae lineage acquired the ability to use uninfested cucumbers. The pre-infestation largely decreased insect-negative metabolites such as cucurbitacins and phenols and increased insect-positive metabolites such as soluble sugars. The pre-infestation decreased the salicylic acid by 25.9% but increased the jasmonic acid by 1337% in cucumbers, which corresponded to expression of marker genes in phytohormone signaling pathways. Exogenous salicylic acid significantly decreased the performance improvement of Malvaceae lineage on pre-infested cucumbers, but exogenous jasmonic acid did not. Those results indicate that infestation by Cucurbit lineage altered the metabolism of cucumbers and interrupted the defense-associated phytohormones, from which we conclude that the disability in overcoming cucumber's defenses caused the incompatibility of Malvaceae lineage to cucumbers. The acclimation to cucumbers of Malvaceae lineage aphids may result from activation of some effector genes targeting cucumbers. Our findings provide new insights into the mechanisms of aphid host-specialization and new clues for preventing A. gossypii switching from Malvaceae hosts to cucurbits.

Automated summary

In this study, the performance of different host lineages of the aphid Aphis gossypii on cucumbers was investigated. The researchers found that the Malvaceae lineage showed poor performance on cucumbers, but its performance significantly improved after feeding on cucumbers previously infested by the Cucurbit lineage. The infestation altered the metabolism of cucumbers and disrupted the defense-associated phytohormones, leading to the incompatibility of the Malvaceae lineage with cucumbers.