Graft transmissible resistance to Alternaria alternata is mediated by rootstock to scion JA transport activating raffinose synthesis

Black spot disease, caused by the fungus Alternaria alternata, is a global plant pathogen that lacks sustainable control measures and poses a serious threat to multiple economically important crops. One approach to enhancing disease resistance in susceptible plants is grafting them onto disease-resistant rootstocks, yet the mechanisms by which roots enhance disease resistance in shoots remains largely unknown. Here, using chrysanthemum-Artemisia vulgaris grafts, we identified that a raffinose synthase-encoding gene, CmRS6, is essential in the susceptible chrysanthemum scion for graft-transmitted resistance from the disease-resistant A. vulgaris rootstock. Exogenous raffinose treatments enhanced A. alternata resistance in chrysanthemum, tomato, cabbage, and apple, highlighting its broad defensive role. The CmERF1B transcription factor activated CmRS6 expression and raffinose accumulation, whereas CmJAZ1-like repressed CmERF1B via direct interaction. While we found evidence for rootstock-to-scion transport of raffinose, long-distance JA transport from A. vulgaris rootstocks to chrysanthemum scions was the primary mechanism for graft-transmitted resistance, and A. alternata infection further promoted JA transport. Collectively, our study demonstrates that rootstock-to-scion JA transport mediates graft-transmitted A. alternata resistance by up-regulating scion raffinose biosynthesis, thereby offering new strategies for the sustainable control of A. alternata in crops.