Group VII basic helix-loop-helix (bHLH) transcription factors, particularly the PHYTOCHROME INTERACTING FACTORS (PIFs), act as signaling hubs in plants, integrate diverse internal and external cues to orchestrate transcriptional networks that drive pleiotropic morphogenesis. Despite their significance, the evolutionary origins underpinning their functional diversity remain largely elusive. Here, we systematically elucidated the evolutionary trajectories of group VII bHLH homologs. We identified the emergence of PIF4/5 orthologs as a distinct angiosperm-specific innovation, characterized by unique motif acquisition and intensified purifying selection. Synteny analysis revealed that whole-genome duplication (WGD) events were instrumental in establishing the divergent PIF3 and PIF2/6 lineages. Additionally, codon usage analysis uncovered species-specific biases, with basal angiosperms, lycophytes, mosses, algae, and monocots exhibiting elevated GC content and related indices, suggesting adaptive optimization for translational efficiency. Bridging evolution with function, weighted gene co-expression network analysis (WGCNA) in Arabidopsis thaliana identified a turquoise module strongly correlated with elevated temperature, pinpointing AtPIF4 as a central hub gene. Functional validation suggested that AtPIF4 is a nuclear-localized protein and that an intact, conserved bHLH domain is required for AtPIF4-dependent hypocotyl elongation under warm ambient temperatures. Collectively, this study provides insights into AtPIF4-mediated thermomorphogenesis and establishes an evolutionary framework for understanding the diversification of group VII bHLH homologs across plant lineages.
