Pan-genome landscape of the JAZ family in pepper (Capsicum annuum L.): core-variable architecture and hormone crosstalk in leaves

The JASMONATE ZIM-DOMAIN (JAZ) proteins are master repressors of jasmonate (JA) signaling and central hubs for phytohormone crosstalk. While JAZ family evolution has been studied in model plants, their pan-genome dynamics and transcriptional specialization in pepper ( Capsicum annuum L.), a globally important Solanaceous crop, remain unexplored. In this study, we conducted a comprehensive pan-genome analysis of the JAZ family across 20 diverse pepper accessions. We identified 12 CaJAZ members exhibiting a dichotomous evolutionary pattern: core genes ( CaJAZ2 / 3 / 4 / 5 / 7 ) under strong purifying selection versus dispensable genes ( CaJAZ6 / 9 ) showing lineage-specific structural variations. Notably, CaJAZ9 underwent extensive tandem duplication (up to 5 copies in specific landraces), while CaJAZ6 exhibited adaptive loss in cultivated varieties, suggesting diversifying selection. Promoter analysis revealed prevalent light-responsive elements (Box 4/G-box) and hormone-specific motifs (ABRE, CGTCA). Crucially, structural parsing of the Jas motif unmasked a highly stratified receptor-interacting matrix. We discovered that the structural truncation of the universally conserved Pro-Tyr (P-Y) anchor in CaJAZ6 perfectly uncouples it from MeJA-induced degradation, rendering it “transcriptionally deaf” and acting as a recalcitrant molecular brake. Transcriptionally, the family displayed distinct temporal modules: rapid transient activation by MeJA (peak at 1 h), sustained biphasic responses to ABA (secondary peak at 12 h), and delayed induction by SA (12–24 h). A functional “division of labor” was observed, with CaJAZ3 / 4 / 9 acting as JA-specific sentinels and CaJAZ1 / 2 / 5 serving as multi-hormone integrators. This study provides the first pan-genome atlas of the pepper JAZ family, revealing that structural variation (PAV/CNV/motif anomalies) and promoter architecture underlie adaptive diversification. The identification of core versus variable haplotypes offers precise genetic targets for breeding climate-resilient pepper varieties with optimized growth-defense trade-offs.