Specialist aphids feeding causes local activation of salicylic and jasmonic acid signaling in Arabidopsis veins

Aphids, the phloem sap feeders, probe into leaf tissues and activate a complex network of plant defence responses. Phytohormonal signaling plays a major role in this network; however, the dynamics of the signals spreading is yet to be clarified. Despite the growing knowledge about transcriptomic changes upon infestation, results often differ due to sampling, varying strongly between the tissues collected at the single feeding site, individual leaves, pooled infested leaves, or whole plant rosettes. This study focuses on activation of salicylic and jasmonic acid signals in Arabidopsis leaves during infestation by cabbage aphid (Brevicoryne brassicae) in high spatio-temporal resolution. We used genetically encoded fluorescent biosensors, histochemistry and qRT-PCR to precisely map activation of distinct branches of phytohormonal signaling. We found a rapid induction of salicylic and jasmonic acid signaling markers in cells surrounding stylet puncture, co-localizing with callose deposition. For both PR1 and JAZ10 we detected activation at 24 hpi, increasing and spreading along the veins until 72 hpi and, to a lesser extent, within the epidermal pavement cells. The SA signaling wave appeared in parallel with JA-associated, and continued to increase in time. Our results first show a local activation of SA- and JA-related responses after stylet penetration of Arabidopsis leaves and bring a detailed insight into the spatio-temporal complexity of plant defence activation during specialist aphid attack.