Domestication reshaped induced defense signaling in the apple-aphid interaction

Abstract

Domestication can shift the balance between constitutive and inducible plant defense, but how this shift is reflected in defense-signaling gene expression remains poorly understood in perennial crops. We investigated how domestication altered induced transcriptional defense responses in apple to its major pest, the rosy apple aphid (Dysaphis plantaginea). We paired wild (Malus orientalis, and two geographically differentiated M. sylvestris populations from France and Romania) and cultivated (cider and dessert M. domestica) apple genotypes with two Dysaphis plantaginea genotypes collected from the same French and Romanian regions as the wild M. sylvestris populations sampled, a reciprocal design that is logistically demanding in a long-lived perennial host and its clonally propagated aphid pest, combining controlled infestation experiments with phenotypic measurements, paired host-aphid RNA-seq, co-expression network analysis, and genome-wide selection scans. Aphid fitness and host resistance varied strongly across host populations: domesticated apples supported higher aphid performance, whereas Romanian M. sylvestris showed the highest resistance, revealing marked host–aphid genotype-specific asymmetric compatibility. Cultivated apples mounted extensive inducible transcriptional reprogramming of hormone-signaling and secondary-metabolism pathways, whereas wild populations showed weaker transcriptional perturbation despite greater resistance, consistent with a shift toward more constitutive defense in the wild. Cross-species co-expression analyses identified coordinated host-aphid modules linking host defense-signaling genes, including a WRKY70 homolog and a CNL-class resistance gene, to aphid transcripts with effector-like annotations. Together, these results indicate that domestication shifted the balance between constitutive and inducible defense signaling in apple, offering a mechanistic entry point into how induced immunity to phloem-feeding insects is reshaped in a long-lived, clonally propagated perennial crop.