Differential activation of defense responses in cucumbers by adapted versus non-adapted lineages of the cotton-melon aphid

Background: The cotton-melon aphid, Aphis gossypii Glover, is a polyphagous pest damaging plants across over 100 families. It has multiple host-specialized lineages, including one colonizing Malvaceae (MA) and one colonizing Cucurbitaceae (CU). The mechanisms underlying these host relationships remain unknown. Here, we compared defensive compounds, gene expressions and aphid susceptibility of cucumbers (Cucumis sativus L.) that were infested with both lineages for up to 14 days.

Results: Total jasmonic acid (JA) remained constant in CU-infested cucumbers while increased to a maximum of 19.11 folds at 1 dpi (days post infestation) in MA-infested cucumbers. Total salicylic acid (SA) increased to a maximum of 4.42 folds at 7 dpi in MA-infested cucumbers while increased to a maximum of 2.83 folds at 14 dpi in CU-infested cucumbers. Reactive oxygen species were constantly higher in MA-infested cucumbers than CU-infested cucumbers at each time point. Genes involved in defense signaling, for example, MAPKs, PR-1s, and WRKY, and genes involved in JA and SA biosynthesis, were largely up-regulated in MA-infested cucumbers compared with CU-infested ones. Both lineages exhibited more stylet probing, less phloem ingestion, higher mortality, and less reproduction on MA-infested cucumbers compared with CU-infested ones.

Conclusion: MA lineage aphids elicited stronger defenses in cucumbers than the CU lineage aphids. A lack of salivary effectors specific to cucumbers most likely prevents MA lineage aphids from using cucumbers. Identifying lineage-specific elicitors or effectors is therefore expected to unveil the molecular mechanisms of host specificity of this aphid. © 2025 Society of Chemical Industry.