An avirulence-associated small secreted effector from Meloidogyne incognita enhances tomato resistance via lipoxygenase targeting

Root-knot nematodes (RKNs) pose a major threat to global crop production, yet the molecular mechanisms underlying plant resistance to RKN infection remain incompletely understood. Here, we identify a small-secreted effector from Meloidogyne incognita, Mi-MSP5, as an avirulence determinant that enhances tomato resistance through targeted modulation of host lipoxygenase activity. Transgenic tomato hairy roots overexpressing Mi-MSP5 exhibited approximately 50% reduction in susceptibility, indicating a strong defense-promoting role. Yeast two-hybrid screens of nematode-induced tomato gall prey library identified the lipoxygenase homology protein LOXH1 as a specific Mi-MSP5 interactor. LOXH1 and Mi-MSP5 colocalized and interacted at the plasma membrane in planta, and LOXH1 expression was transiently upregulated during early stages of nematode infection. Functional assays revealed that LOXH1 overexpression phenocopied Mi-MSP5-mediated resistance, whereas partial silencing of LOXH1 increased susceptibility. Biochemical analyses demonstrated that both Mi-MSP5 and LOXH1 overexpression led to approximately a twofold increase in lipoxygenase enzymatic activity in roots. Moreover, this activation correlated with enhanced expression of jasmonic acid (JA)-responsive defense genes. Collectively, our findings uncover a novel effector-triggered immunity mechanism in which a nematode effector co-opts a non-catalytic host lipoxygenase domain protein to boost lipoxygenase activity and activate JA-mediated defenses, providing a promising strategy for engineering durable nematode resistance in plants.