Integrated transcriptomic and metabolomic analyses of the molecular mechanisms of flower color variation in three Camellia species

Flower color is an important ornamental trait that influences plant growth and pollination. However, the molecular mechanisms of flower color variation in Camellia, a widely used ornamental woody flower for landscaping, remain unexplored. Here, we used an integrated transcriptomic and metabolomic approach to investigate the molecular regulatory mechanisms underlying petal coloration diversity in three Camellia species: Camellia amplexicaulis Cohen Stuart (red flower, RD), C. petelotii (Merr.) Sealy (yellow flower, YE), and C. oleifera Abel (white flower, WH). We found that in RD flowers, the anthocyanin content, which is closely associated with red flowers, was the highest. In YE flowers, compounds believed to play important roles in flower coloration, such as apigenin, vitexin and their derivatives, as well as quercetin and its derivatives, were significantly greater than those in flowers of other colors. Kaempferol and its derivative contents, which are considered white petal pigments, were greater in WH flowers. Additionally, we identified 139 structural genes involved in flavonoid biosynthesis and screened 29 key structural genes, including PAL, 4CL, CHI, CHS, ANS, ANR, LAR, CYP75B1, FLS, C12RT1, FG3, and CYP93B2_16. The expression patterns of these genes in flowers of different colors were closely related to the patterns of flavonoid metabolite accumulation, indicating that these genes play a key role in flower color development. Transcription factors (TFs) also play important roles in regulating flower color formation. We identified 3,181 TFs, including members of the MYB, bHLH, bZIP, and WRKY TF families, which play crucial roles in the flavonoid and anthocyanin biosynthetic pathways. According to the results of the correlation analysis, 66 TFs were highly correlated with the total flavonoid and anthocyanin contents, and these TFs directly or indirectly regulate flower color development. Moreover, we identified numerous potential metabolites, along with many candidate structural genes and TFs, that may cause flower color variations. Therefore, our findings provide new insights into the molecular regulatory network of Camellia flower color diversity and offer significant genetic insight and a theoretical foundation for the cultivation of Camellia varieties with desirable color characteristics. With further functional validation and breeding applications, these results may increase the ornamental value of Camellia species and contribute to the genetic improvement of the Camellia flower.