Transcription factor SlJIG orchestrates multi-layer defense in tomato against the invasive pest Phthorimaea absoluta

In plants, many (bHLH) transcription factors play key roles in processes governing resistance to biotic and abiotic stresses. Whether and how bHLH transcription factors participate in tomato defense against the invasive pest Phthorimaea absoluta remains unclear. We here reveal that the bHLH transcription factor gene SlJIG responds positively to P. absoluta infestation, to methyl jasmonate-treatment and to wounding. Gene editing SlJIG in tomato plants increased susceptibility to P. absoluta larvae and attractiveness to oviposition by P. absoluta females but decreased attractiveness to Nesidiocoris poppiusi, a natural predator of P. absoluta. SlJIG was found to enhance resistance through the transcriptional activation of key enzymes in the α-tomatine (HMGR1 and FPPS1) and flavonoid (CHI1 and FLS) biosynthesis pathway. Gene editing SlJIG decreased biosynthesis of α-tomatine and kaempferol, which are two key defensive metabolites against P. absoluta larvae. It also repressed the transcription of terpene synthesis TPS12, resulting in lower emission of α-humulene, which is correlated with the preference changes of P. absoluta and N. poppiusi. These findings underscore the pivotal role of SlJIG as a regulator of tomato defense against P. absoluta and highlight its potential as a target for molecular breeding to enhance tomato resistance.