The NF-Y gene family in Rosa: evolutionary divergence across three species and potential roles in heat tolerance and secondary metabolism

Abstract

Plant pigmentation and secondary metabolism are intrinsically linked to pollinator attraction, environmental adaptation, and ornamental quality, yet the transcriptional regulators that coordinate multiple metabolic branches remain poorly understood. Nuclear Factor Y (NF-Y) transcription factors are well-established mediators of developmental and stress signaling, but their involvement in orchestrating plant metabolic networks has not been explored in the genus Rosa . Here, we performed genome-wide identification and multi-omics characterization of 30, 30, and 29 NF-Y genes from R. chinensis , R. rugosa , and R. wichuraiana , respectively. We then conducted evolutionary analyses, orthology-based protein interaction modeling, promoter cis-element analysis, transcriptome profiling under heat stress, and integrated Weighted Gene Co-expression Network Analysis (WGCNA) with untargeted metabolomics. Evolutionary analyses revealed that segmental duplications drove family expansion under strong purifying selection, with the NF-YB and NF-YC subfamilies exhibiting distinct structural diversification. Orthology-based protein interaction modeling predicted the NF-YC subgroup I as a likely scaffold for heterotrimer assembly, while promoter cis-element analysis showed enrichment in hormone-responsive motifs (ABRE and MeJA), linking these genes to both environmental cues and metabolic signaling. Transcriptome profiling under heat stress demonstrated species-specific NF-Y expression dynamics, with the NF-YA subfamily contributing the most responsive members. Crucially, by integrating WGCNA with untargeted metabolomics, we associated multiple RcNF-Y genes with cultivar-dependent accumulation of flavonoids, terpenoids, and alkaloids—spanning the major classes of pigmentation-related and defense-related secondary metabolites. Among these, RcNF-YA4, RcNF-YA5 , and RcNF-YB12 were associated with flavonoid accumulation, whereas RcNF-YC2 was associated with terpenoid and alkaloid accumulation. This suggests that RcNF-YC2 may function as a potential hub bridging stress signaling with broad-spectrum metabolic regulation. Notably, the NF-Y members responding to heat stress and those linked to metabolic output showed limited overlap, implying functional specialization within the family. Collectively, our findings suggest a potential role of the rose NF-Y family in integrating thermal stress signals with diverse secondary metabolic pathways. This study prioritizes RcNF-YC2 as a candidate target for genetic or biotechnological improvement of fragrance and stress resilience in ornamental crops.