A bacterial effector SJP3 induces leaf-like sepal formation by hijacking SHORT VEGETATIVE PHASE in plants

Jujube (Ziziphus jujuba), the most economically important member of the Rhamnaceae family, is sensitive to phytoplasma-induced witches' broom disease. The SAP54/phyllogen-like effector SJP3 in jujube witches' broom (JWB) phytoplasmas interacts with and stabilizes the MADS-box protein SHORT VEGETATIVE PHASE 3 (ZjSVP3), resulting in pistil reversion. Here, we further demonstrated that SJP3 induced leaf-like sepal formation by activating the ZjSVP1-ZjSVP3 complex at multiple levels. Among the cascading events, SJP3-mediated ZjAP1 and ZjSEP3 degradation promoted ZjSVP1 expression. The miRNA396c-ZjSVP1 pathway was a conserved mechanism through which SJP3 repressed miRNA396c and upregulated ZjSVP1 expression. While ZjSVP3 escaped from the regulation of ZjAP1, ZjSEP3 and miRNA396c, interestingly, SJP3 exploited the escape and induced ZjSVP3 accumulation, resulting in continuous activation of the expression of ZjSVP1 and itself. ZjSVP3 interacted with ZjSVP1 to form a heterodimer. SJP3 directly targeted the ZjSVP1-ZjSVP3 complex to induce the misexpression of SVP-binding motif-containing genes (such as ZjGATL1 and ZjLAC17) that contributed to the conversion of floral organs into leaf-like structures, in turn extending the tissue-to-tissue spread and colonization of JWB phytoplasmas. Overall, these results provide insight into the mechanism underlying the hijacking of the floral repressors ZjSVP1 and ZjSVP3 by the effector SJP3 to induce leaf-like sepal formation in perennial woody plant species.