The mid-to-late-stage fungal effector EqBPIE1 mediates chloroplast-to-nucleus immune signaling and broad-spectrum resistance

Powdery mildew caused by Erysiphe quercicola is a serious threat to natural rubber (Hevea brasiliensis) production, but the molecular basis of host immunity against this pathogen remains poorly understood. Here, we identify EqBPIE1 (E. quercicola Broad-spectrum Plant Immunity Elicitor 1), a fungal effector expressed during the mid-to-late colonization stage, that localizes to the cytosol, chloroplasts, and nucleus of host cells. EqBPIE1 enhances chloroplast-derived reactive oxygen species production, promotes perinuclear chloroplast clustering and stromule (stroma-filled tubule) formation, and thereby facilitates the relay of immune signals to the nucleus. In the nucleus, EqBPIE1 interacts with the NLR protein HbRG1 (H. brasiliensis Resistance Gene 1) to trigger hypersensitive cell death. Silencing EqBPIE1 increased susceptibility of H. brasiliensis to E. quercicola, whereas heterologous expression and foliar application conferred broad-spectrum resistance against fungal, bacterial, and oomycete pathogens in multiple plant species. Our findings establish an effector-mediated chloroplast-to-nucleus immune signaling pathway and highlight EqBPIE1 as a promising molecular tool for engineering durable, broad-spectrum disease resistance across crops.