The root-knot nematode effector MiPDI1 targets a stress-associated protein (SAP) to establish disease in Solanaceae andArabidopsis

Large amounts of effectors are secreted by the oesophageal glands of plant-parasitic nematodes, but their molecular mode of action remains largely unknown. We characterized aMeloidogyne incognitaprotein disulphide isomerase (PDI)-like effector protein (MiPDI1) that facilitates nematode parasitism. In situhybridization showed thatMiPDI1was expressed specifically in the subventral glands ofM. incognita. It was significantly upregulated during parasitic stages. Immunolocalization demonstrated MiPDI1 secretionin plantaduring nematode migration and within the feeding cells. Host-induced silencing of theMiPDI1gene affected the ability of the nematode to infect the host, whereasMiPDI1expression inArabidopsisincreased susceptibility toM. incognita, providing evidence for a key role of MiPDI1 inM. incognitaparasitism. Yeast two-hybrid, bimolecular fluorescence complementation and coimmunoprecipitation assays showed that MiPDI1 interacted with a tomato stress-associated protein (SlSAP12) orthologous to the redox-regulated AtSAP12, which plays an important role in plant responses to abiotic and biotic stresses.SAP12silencing or knocking out inNicotiana benthamianaand Arabidopsis increased susceptibility toM. incognita. Our results suggest that MiPDI1 acts as a pathogenicity factor promoting disease by fine-tuning SAP-mediated responses at the interface of redox signalling, defence and stress acclimation in Solanaceae andArabidopsis.