The root-knot nematode effector Mi1D08B targets a NINJA-family co-repressor to suppress jasmonate production and promote infection in soybean

Abstract

Plant-parasitic nematodes deploy secreted effector proteins that reprogram host cellular processes to establish parasitism. Here, we characterized Mi1D08B, a putative dorsal-gland effector from the root-knot nematode Meloidogyne incognita and defined its role in subverting soybean jasmonate-mediated immunity. Mi1D08B is conserved across several Meloidogyne species and localizes to the plant nucleus and cytoplasm. Overexpression of Mi1D08B significantly increased galling and egg production, demonstrating a strong virulence role. A gall-specific yeast two-hybrid screen identified the NINJA-family co-repressor mc410 as a host target of Mi1D08B. Consistent with the functional relevance of this interaction, mc410 promoter activity was detected in galls and giant cells throughout nematode infection. Genetic manipulation of mc410 phenocopied Mi1D08B activity as mc410 overexpression enhanced susceptibility, whereas mc410 silencing reduced nematode infection. Hormone profiling revealed that Mi1D08B overexpression elevated 12-oxo-phytodienoic acid (OPDA) but reduced jasmonic acid (JA) and JA-Ile, consistent with a bottleneck at the peroxisomal OPDA-to-JA conversion. Furthermore, several metabolites associated with this conversion were reduced, indicating that Mi1D08B perturbs metabolic flux through the peroxisomal phase of jasmonate biosynthesis. Gene expression analyses supported this biochemical signature, with upregulation of plastidial OPDA-biosynthetic genes and downregulation of peroxisomal OPDA-reductases, JA-conjugating enzymes, and JA-responsive markers. Together, our data support a model in which Mi1D08B effector interacts with a NINJA co-repressor to suppress JA biosynthesis and signaling, thereby coupling nuclear transcriptional repression to altered metabolism. This mechanism deepens our understanding of nematode manipulation of host hormone networks and highlights the Mi1D08B–mc410 interface and OPDA conversion as promising targets for engineering nematode resistance.