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

Abstract

Abstract 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 were poor on cucumbers, but significantly improved on cucumbers that were previously infested by Cucurbit lineage for 14 d. Following feeding experience on pre-infested cucumbers Malvaceae lineage acquired ability to use healthy cucumbers. The pre-infestation largely decreased insect-negative metabolites such as cucurbitacins and phenols and increased insect-negative metabolites such as soluble sugars. The pre-infestation decreased salicylic acid by 25.9% while increased jasmonic acid by 13.37-fold in cucumbers, which corresponded to expression of marker genes in phytohormone signaling pathways. Exogenous salicylic acid significantly decreased 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 process of acclimation to cucumbers may activate some effector genes targeting cucumber in Malvaceae lineage. 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.