Molecular mechanisms of tobacco in response to whitefly feeding at different developmental stages and evolutionary study of key AP2 transcription factors

Whitefly adults and nymphs impose distinct stresses on plants. Using a tobacco-whitefly model, this study reveals that plants achieve precise, stage-specific defense through modular transcriptional reprogramming. Adult feeding primarily rewires primary metabolism, whereas nymph feeding broadly activates hormone signaling, MAPK cascades, and secondary metabolism. Co-expression network analysis shows that upregulation of the cyan-greenyellow module mediates direct defense, while suppression of the darkturquoise-midnightblue module reflects a growth-defense trade-off. The AP2/EREBP transcription factor family is identified as a central regulator, together with BBR-BPC, MIKC_MADS, and TALE families, forming a multi-layered regulatory network. qRT-PCR validation confirmed significant induction of nine defense-related genes. This work provides new insights into plant-insect interactions and offers candidate targets for breeding insect-resistant crops. • Tobacco employs modular transcriptional reprogramming to mount stage-specific defenses against whitefly adults and nymphs. • Nymph feeding activates broad defense pathways including hormones, MAPK signaling, and secondary metabolism. • Co-expression network analysis reveals that the cyan–greenyellow module mediates direct defense, and suppression of the darkturquoise–midnightblue module reflects a growth–defense trade-off. • The AP2/EREBP transcription factor family is identified as a central regulator, with evolutionary signatures of functional innovation. • Together with BBR-BPC, MIKC_MADS, and TALE families, AP2/EREBP forms a multi-layered transcriptional network fine-tuning stage-specific resistance.