Resistance-breaking population of Meloidogyne incognita utilizes plant peroxidase to scavenge reactive oxygen species, thereby promoting parasitism on tomato carrying Mi-1 gene.

Resistance conferred by the Mi-1 gene from Solanum peruvianum is effective and widely used for controlling root-knot nematodes (RKNs, Meloidogyne spp.). However, breakdown of resistance by RKNs seriously threatens the durable application of the resistance resource. Here, a resistance-breaking population of M. incognita was selected from an avirulent population by continuously inoculating on Mi-1-carrying tomato. Histological observations showed the resistance-breaking population would not induce hypersensitive response (HR) when infecting Mi-1-carrying tomato, while avirulent population did. A total of 308 differentially expressed genes (DEGs) were identified from Mi-1-carrying tomato upon infection with resistance-breaking versus avirulent populations by RNA-seq. The expression patterns of 23 selected DEGs were validated by quantitative real-time PCR (qRT-PCR). Subsequently, seven out of nine highly up-regulated DEGs were successfully knocked down in Mi-1-carrying tomato by tobacco rattle virus (TRV) mediated RNAi. The TRV line targeting a peroxidase gene showed a much higher magnitude of reactive oxygen species (ROS) and distinct reduction of pathogenicity upon infection of the resistance-breaking population compared with that of TRV::gfp line. Our results suggested that plant peroxidase might be exploited by resistance-breaking population of M. incognita to scavenge ROS, so as to overcome Mi-1-mediated resistance.