Cytospora canker, caused by Cytospora mali, is the most destructive disease in production of apples (Malus domestica). Adding potassium (K) to apple trees can effectively control this disease. However, the underlying mechanisms of apple resistance to C. mali under high-K (HK) status remain unknown. Here, we found that HK (9.30 g/kg) apple tissues exhibited high disease resistance. The resistance was impeded when blocking K channels, leading to susceptibility even under HK conditions. We detected a suite of resistance events in HK apple tissues, including upregulation of resistance genes, callose deposition, and formation of ligno-suberized tissues. Further multiomics revealed that the phenylpropanoid pathway was reprogrammed by increasing K content from low-K (LK, 4.30 g/kg) status, leading to increases of 18 antifungal chemicals. Among them, the physiological concentration of coumarin (1,2-benzopyrone) became sufficient to inhibit C. mali growth in HK tissues, and exogenous application could improve the C. mali resistance of LK apple branches. Transgenic apple calli overexpressing beta-glucosidase 40 (MdBGLU40), which encodes the enzyme for coumarin synthesis, contained higher levels of coumarin and exhibited high resistance to C. mali even under LK conditions. Conversely, the suppression of MdBGLU40 through RNAi reduced coumarin content and resistance in HK apple calli, supporting the importance of coumarin accumulation in vivo for apple resistance. Moreover, we found that the upregulation of transcription factor MdMYB1r1 directly activated MdBGLU40 and the binding affinity of MdMYB1r1 to the MdBGLU40 promoter increased in HK apple tissue, leading to high levels of coumarin and resistance in HK apple. Overall, we found that the accumulation of defensive metabolites strengthened resistance in apple when raising K from insufficient to optimal status, and these results highlight the optimization of K content in fertilization practices as a disease management strategy.

Colletotrichum fungi cause destructive diseases among a wide range of hosts worldwide. We found that effector CfEC92 from C. fructicola specifically binds ATP through an unidentified ATP-binding domain, leading to changes in the protein secondary structure. The residues Cys ²⁶ , Asn ³⁸ , and Cys ³⁹ were critical for ATP binding with CfEC92, and mutations at these sites impaired the ability to suppress host immunity. CfEC92 interacted with MdNDPK2, a negative immune regulator in apple. The CfEC92-ATP complex altered the conformation of MdNDPK2, enhancing its affinity for ATP, and further increasing its autophosphorylation and kinase activity. The activated MdNDPK2 phosphorylated MdMPK3 to suppress host immunity. Homology and functional tests showed that the Cx ₁₁ NC motif was highly conserved among Colletotrichum species, suggesting that CNC effectors represent a class of broad-spectrum virulence factors. Our findings revealed a mechanism by which Colletotrichum effectors cooperate with helper ATP to promote target protein phosphorylation and suppress host immunity.