Multi-omics analysis of Raptor1A knockout reveals resistance to Tuta absoluta in tomato without growth penalties

The Target of Rapamycin (TOR) signaling pathway plays a pivotal role in balancing plant growth and defense. However, the specific contribution of TOR complex components to insect resistance remains poorly understood. In this study, we identified and characterized SlRaptor1A, a scaffold protein of TOR complex 1 (TORC1), in tomato (Solanum lycopersicum), and revealed its function as a negative regulator of defense against the destructive pest Tuta absoluta. CRISPR-Cas9-mediated knockout of SlRaptor1A does not affect tomato growth and yield but confers enhanced resistance to T. absoluta. Integrated transcriptomic and metabolomic analyses showed that SlRaptor1A suppressed jasmonic acid (JA) and salicylic acid (SA) signaling pathways, reduced alkaloid accumulation, and downregulated phenylpropanoid biosynthesis during T. absoluta infestation. Slraptor1a mutants exhibited elevated levels of JA/SA and their derivatives, accompanied by upregulation of defense-related genes and accumulation of secondary metabolites potentially associated with insect resistance. Co-expression network analysis further confirmed the coordination of gene expression and metabolite production in response to infestation. These findings demonstrate that SlRaptor1A suppresses tomato defense through hormonal and metabolic regulation and provide a promising genetic target for breeding pest-resistant tomato cultivars without growth and yield penalties.