Comparative transcriptomic and metabonomic analysis revealed the relationships between biosynthesis of volatiles and flavonoid metabolites in Rosa rugosa

Abstract

Rosa rugosa is not only cultivated as a landscaping plant, but also used in cosmetics, the medical and food industries. However, little information is currently available on the gene regulatory networks involved in its scent and color biosynthesis and metabolism. In this study, R. rugosa Thunb. f. rosea Rehd with red petals (RR) and its white petal variant (WR), were used to study the molecular mechanisms in flower color and scent. Sixtyfive differential flavonoid metabolites and 15 volatiles were found to have significant differences between RR and WR. Correspondingly, the key regulators (MYB-bHLH-WD40) of anthocyanin synthesis pathway and their structural genes involved in flavonoid biosynthesis, benzenoid/ phenylpropanoid biosynthesis, terpenoid biosynthesis pathways were also found to be differentially expressed by comparative transcriptome. Further, qPCR permitted the identification of some transcripts encoding proteins that were putatively associated with scent and color biosynthesis in roses. Particularly, the results showed that the ACT gene (encoding CoA geraniol/citronellol acetyltransferase, GeneID: 112190420), which expressed lower in WR, was involved in three pathways: flavonoid biosynthesis, phenylpropanoid biosynthesis and terpenoid biosynthesis, however, GT5 (anthocyanin glycosylation gene, GeneID:112186660), expressed higher in WR, was involved in both flavonoid and phenylpropanoid biosynthesis pathways. These results suggested that ACT and GT5 might play important roles in regulating the relationship of color pigmentation and volatile emission. Citation: Feng D, Zhang H, Qiu X, Jian H, Wang Q, et al. 2021. Comparative transcriptomic and metabonomic analysis revealed the relationships between biosynthesis of volatiles and flavonoid metabolites in Rosa rugosa. Ornamental Plant Research 1: 5 https://doi.org/10.48130/OPR-2021-0005 INTRODUCTION Rosa rugosa, an important ornamental plant in Rosaceae, is widely used in landscaping, cosmetics, food and the medical industry, due to its unique fragrance, color and tolerance to environmental stresses[1,2]. Flower color is an important trait for plants to attract pollinators, which benefit for completing sexual-hybridization. In nature, the petals of most varieties of R. rugosa are pink and purple, only a few are white or other color[3]. The major primary compounds that influence flower colors are flavonoids, which could lead to anthocyanin accumulation and in turn contributing to flower color[4,5]. The flavonoid biosynthetic pathway finally leads to three types of anthocyanin metabolites: cyanidin, pelargonidin, and delphinidin, and these became stabilised via methylation, hydroxylation, acylation and glycosylation[6,7]. Many regulatory genes and structural genes (especially genes encoding key synthases) that participate in anthocyanin biosynthetic pathways have been identified in plants[8−12]. In rose, an anthocyanin synthase gene, F3’5’H, was expressed in a transgenic plants resulting in blue flowers[13]. RrFLS, RrDFR and RrF3’H were reported to be the key genes controlling petal color in three novel-colored R. rugosa cultivars[14]. Overexpression of RrMYB5 and RrMYB10 might promote the production of proanthocyanidins in R. rugosa and tobacco[15]. Furthermore, it was proposed that disequilibrium expression of flavonol synthase (FLS, the key synthase in producing flavonols) and Dihydroflavonol-4-Reductase (DFR, the key enzyme in accumulating anthocyanins) genes share the same substrates and leads to different colors[16]. For the modification genes, RrGT2 and RrGT1 play important roles in anthocyanin accumulation[2,3]. Flower scent is another important trait in ornamental plants, which is not only critical for pleasant fragrance, but also can defend against fungi and bacteria due to the volatile compounds involved in scent production[17,18]. According to the biosynthetic origin, the volatile metabolites were classified into three classes: terpenoids, benzenoids/phenylpropanoids and fatty acid derivatives[19]. Some structural genes, especially genes encoding key enzymes involved in the volatile compound biosynthetic pathways, have also been reported[20−26]. For regulatory genes, RhMYB1 has been shown to be a regulatory gene involved in the biosynthesis of ARTICLE