Multi-omics and physiological analysis reveal crosstalk between aphid resistance and nitrogen fertilization in wheat

The availability of nitrogen (N) can dramatically influence crops resistance to herbivorous insects. However, the interaction between N fertilization and crop resistance to insects is not well understood. In this study, the effects of N fertilization on the grain aphid (Sitobion miscanthi) were investigated using three wheat (Triticum aestivum) cultivars with different aphid resistances. We measured aphid life cycle parameters, fecundity, survival rate, weight and feeding behavior, in conjunction with wheat metabolomics, transcriptomics and alien introgression analysis. Our results demonstrated that higher N application benefits aphid feeding across all three wheat cultivars. We also reveal that the highly resistant cultivar (ZM9) can only exert its resistance-advantage under low N fertilization, losing its advantage compared to moderately resistant cultivar YN19 and susceptible cultivar YN23 under higher N fertilization. The effects of N fertilization on wheat-aphid interactions were due to changes in the regulation of carbon and nitrogen metabolism. Integration of multi-omics highlighted specific aphid-induced differentially expressed genes (DEGs, e.g., TUB6, Tubulin 6; ENODL20, Early nodulin-like protein 20; ACT7 Actin 7; Prx47, Peroxidase 47) and significantly different metabolites (SDMs, e.g., crotonoside, guanine, 2"²-O-methyladenosine, ferulic acid) in ZM9. Additionally, we report the unique SDMs-DEGs interactions, associated with introgression during wheat domestication, may help infer aphid resistance. In summary, this study provides new insights into the relationships between N fertilization practices, defense responses and integrated pest management for sustainable wheat production.