A phyllody-inducing effector SJP3 compromises disease resistance by hijacking ZjWRKY40-mediated ZjTIFY3B / 5A pathway in jujube

Phytoplasma-trigged morphological alterations in plants not only favor their survival and fitness but also facilitate attractiveness to leafhopper vectors. The effector SJP3 from jujube witches’ broom (JWB) phytoplasmas was previously identified as the key virulence factor that induced leaf-like flowers. However, whether the effector SJP3 interfered with plant defense responses during JWB phytoplasma infection remained unknown. In this study, we demonstrated that the effector SJP3 compromised jasmonic acid (JA)-mediated resistance in jujube. Both the N- and C-terminus of SJP3 directly interacted with the entire WRKY and zinc-finger domains of ZjWRKY40. Deletion mutant of SJP3 N- or C-terminus lost its ability to stabilize ZjWRKY40 protein. Heterologous expressions of SJP3 and ZjWRKY40 in Arabidopsis showed increased susceptibility to a bacterial pathogen (Pseudomonas syringae pv. tomato DC3000). Transcriptomic and qRT-PCR analysis revealed that SJP3 repressed JA signaling pathway, especially upregulating the expression of two JA signaling suppressors ZjTIFY3B and ZjTIFY5A in transgenic jujube leaves. Furthermore, SJP3 enhanced the abilities of ZjWRKY40 as well as its two homologues to promote ZjTIFY3B and ZjTIFY5A expression. Exogenous application of methyl jasmonate significantly decreased JWB phytoplasma titre and SJP3 expression. Collectively, these findings revealed that the effector SJP3 supressed defense responses during JWB phytoplasma infection by hijacking ZjWRKY40-mediated ZjTIFY3B/5A pathway in the diseased jujube plants. Our results also provided valuable gene resources that could be used for JWB disease resistance breeding by CRISPR-Cas technologies.