Tomato resistance to Phelipanche aegyptiaca by activation of reactive oxygen scavenging and phenylpropanoid metabolism

Phelipanche aegyptiaca is a destructive parasitic weed that poses significant challenges to tomato cultivation. Breeding for resistance is an effective weed management strategy for mitigating yield losses caused by P . aegyptiaca, and identifying resistance-related genes while clarifying the underlying mechanism is critical for breeding success. In this study, comparative transcriptomic and proteomic analyses were conducted on the resistant variety ‘H1015’ and susceptible variety ‘H2401’ following P . aegyptiaca infection. Genes and proteins associated with phenylpropanoid and reactive oxygen metabolism were significantly enriched in ‘H1015’ compared to ‘H2401’, indicating phenylpropanoid and reactive oxygen metabolism might positively dominate the resistance of P . aegyptiaca . These findings were further confirmed by metabolomic profiling and enzyme activities assay, the derivatives of phenylpropanoid metabolism-related secondary metabolites were significantly accumulated in ‘H1015’, and the enzymes of POD, CAT, and SOD were continuously increased in the later stage. The functions of related genes were characterized by gain- and loss-of-function assays, which found that 4CL, the key enzyme of the phenylpropanoid pathway, functions as a positive regulator and plays a pivotal role in enhancing tomato resistance to P . aegyptiaca . The 4CL overexpressing transgenic tomato and Arabidopsis exhibited an improved ability against P . aegyptiaca parasitism, while silencing of 4CL showed an opposite trend in the level of resistance. The effect of metabolites belonging to phenylpropanoid and reactive oxygen metabolism on P. aegyptiaca germination and radicle development was investigated in vitro. It was found that the growth of P . aegyptiaca was strongly inhibited by rosemarinic acid, apigenin 7-glucoside, and salicylic acid. Collectively, it was speculated that the phenylpropanoid and reactive oxygen metabolism conferred tomato resistance to P. aegyptiaca . Overall, these results reveal the resistance mechanisms of tomatoes against P. aegyptiaca and provide a promising candidate gene for tomato resistance breeding.