Integrated Metabolomic and Transcriptomic Profiling Unveils Anthocyanin Regulation in Chemically Induced Flower Color Variation of Impatiens hybrida ‘Solarscape’

Background The Impatiens plants are one of the world's top three flower bed floriferous plants with important ornamental and horticultural values, vivid floral colors are more likely to attract pollinators, and one of the important ornamental traits of flowers. This study was conducted to determine whether the flower color of Impatiens can be altered after induction, with the aim of clarifying the molecular basis underlying its variation and to offer a vital reference for developing novel Impatiens varieties. Compared with diploids, the flower color of colchicine-induced Impatiens showed obvious changes, the flowers changed from pinkish purple to orange. Results Integrated metabolomics and transcriptomics were comprehensively utilized to reveal the metabolic pathways of anthocyanin biosynthesis in non-mutant purple flowers and mutant orange. The floral hue discrepancies between Ih-WT and Ih-MU in Impatiens hybrida ‘Solarscape’ exhibit marked variations in luminance (L*), the red-green axis (a*), the yellow-blue axis (b*), and color intensity (Chroma c*). Specifically, the L* value of Ih-WT is significantly higher than that of Ih-MU, and the a*, b*, and Chroma c* values of Ih-WT are significantly greater than those of Ih-MU. Metabolomics identified 93 differential metabolites, most of which were Cyanidin and Pelargonidin-like metabolites, and the accumulation of Cyanidin and Pelargonidin was the principal factor underlying the petal color transition to orange in I. hybrida 'Solarscape'. The accumulation of Cyanidin and Pelargonidin was the main reason for the orange coloration of I. hybrida 'Solarscape' petals. Comparative analysis of the differential metabolites in the two flower samples indicated that the two anthocyanins, Pelargonidin-3-O-sophoroside and Cyanidin-3-O-sophoroside, were the pigments most likely to regulate petal coloration. Analysis of the transcriptome identified 1888 differentially expressed genes (DEGs), including key genes for anthocyanin synthesis (IhC4H, IhUFGT, IhDFR, and IhANS) and regulators (IhMYB308, IhNAC56, and IhMYC2) with high levels of expression of Ih-MU in orange flowers, indicating that they play a role in the regulation of anthocyanin biosynthesis. These genes may be pivotal for the biosynthesis of orange anthocyanins. Co-expression analysis of differentially expressed genes and the relative levels of differentially expressed anthocyanins revealed that each anthocyanin is strongly associated with multiple genes, indicating that the anthocyanin accumulation process is governed by multiple genes. The expression levels of these genes exhibited a statistically significant positive correlation with the relative concentrations of Pelargonidin-3-O-sophoroside, Cyanidin-3-O-(6-O-p-coumaroyl)-glucoside, and Cyanidin-3-O-sophoroside. Conclusions This study showed substantial alterations in color and anthocyanin synthesis in chemically mutagenized I. hybrida 'Solarscape' flowers, and these findings could provide some insight into the relationship between Impatiens and other flowers could offer a theoretical foundation for the breeding improvement of Impatiens and other flowers. Keywords: Impatiens hybrida 'Solarscape'; floral color variation; metabolomics; transcriptomics; anthocyanin biosynthesis