Abstract
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.