The HY5 transcription factor DcbZIP48 confers thermotolerance in carnation

Heat stress (HS) adversely affects heat-sensitive ornamentals, including carnation (Dianthus caryophyllus L.), by impairing developmental stability and yield quality, which ultimately diminishes their commercial viability. The basic leucine zipper (bZIP) transcription factors are known mediators of stress adaptation, yet their functional roles in carnation thermotolerance remain largely unexplored. Here, we performed a genome-wide survey and identified 63 DcbZIP genes, which were systematically classified into 12 distinct subfamilies. Evolutionary analysis revealed lineage-specific expansion patterns, with the S subfamily emerging as the largest group (10 members). Gene structure analysis demonstrated conserved exon-intron organization within phylogenetic clades, with motif composition showing high consistency among subfamily members. Promoter analysis revealed abundant stress-responsive elements, suggesting potential roles in abiotic stress adaptation. Expression profiling demonstrated that DcbZIP48, a homolog of the H-group protein HY5, exhibited marked upregulation in a time-dependent manner under HS. Functional investigations revealed that overexpression of DcbZIP48 substantially enhanced thermotolerance in transiently transformed carnation, as reflected by improved growth performance, reinforced reactive oxygen species (ROS) scavenging capacity, elevated antioxidant enzyme activities, preserved chloroplast function, and altered the expression of heat-responsive genes. In contrast, silencing DcbZIP48 via virus-induced gene silencing (VIGS) exacerbated heat sensitivity. Collectively, these results uncover DcbZIP48 as a HY5-like transcription factor that positively regulates thermotolerance and provide foundational insights into the DcbZIP family in carnation, thereby supporting future genetic improvements for heat resilience in carnation.