Salivary proteins of a gall-inducing aphid and their impact on early gene responses of susceptible and resistant host-plant genotypes

Plant manipulation by herbivores requires fine-tuned reprogramming of host metabolism, mediated by effector molecules delivered by the parasite into its host. While plant galls may represent the epitome of plant manipulation, secretomes of gall-inducers and their impact on host-plants have been rarely studied. We characterized, with transcriptomic and enzymatic approaches, salivary glands and saliva of a gall-inducing aphid, Phloeomyzus passerinii. Early responses to aphid saliva of plant genes belonging to different metabolic and signaling pathways were assessed in vivo, with poplar protoplasts, and in planta, in a heterologous Arabidopsis system. Several effectors potentially interfering with plant signaling have been identified, including binding proteins, oxidoreductases, and phosphatidylinositol phosphate kinases. Compatible interactions between protoplasts of a susceptible poplar genotype and the saliva of P. passerinii led to an overall downregulation of defense-related genes while an upregulation was observed during both incompatible interactions, with a resistant poplar genotype, and non-host interactions, with the saliva of Myzus persicae, an aphid which does not feed on poplars. Compatible interactions affected both auxin transport and homeostasis potentially leading to an intracellular accumulation of auxin, which was further supported by in planta assays. Our results support the hypothesis that effectors interfere with downstream signaling and phytohormone pathways.