PhUGT78A22, a novel glycosyltransferase in Paeonia ‘He Xie’, can catalyze the transfer of glucose to glucosylated anthocyanins during petal blotch formation

Abstract

Background Flower color patterns play an important role in the evolution and subsequent diversification of flowers by attracting animal pollinators. This interaction can drive the diversity observed in angiosperms today in many plant families such as Liliaceae, Paeoniaceae, and Orchidaceae, and increased their ornamental values. However, the molecular mechanism underlying the differential distribution of anthocyanins within petals remains unclear in Paeonia. Results In this study, we used an intersectional hybrid between the section Moutan and Paeonia, hereafter named Paeonia ‘He Xie’, which has purple flowers with dark purple blotches. After Ultra-high performance liquid chromatography-diode array detector (UPLC-DAD) analysis of blotched and non-blotched parts of petals, we found the anthocyanin content in the blotched part was always higher than that in the non-blotched part. Four kinds of anthocyanins, namely cyanidin-3-O-glucoside (Cy3G), cyanidin-3,5-O-glucoside (Cy3G5G), peonidin-3-O-glucoside (Pn3G), and peonidin-3,5-O-glucoside (Pn3G5G) were detected in the blotched parts, while only Cy3G5G and Pn3G5G were detected in the non-blotched parts. This suggests that glucosyltransferases may play a vital role in the four kinds of glucosylated anthocyanins in the blotched parts. Moreover, 2433 differentially expressed genes (DEGs) were obtained from transcriptome analysis of blotched and non-blotched parts, and a key UDP-glycosyltransferase named PhUGT78A22 was identified, which could use Cy3G and Pn3G as substrates to produce Cy3G5G and Pn3G5G, respectively, in vitro. Furthermore, silencing of PhUGT78A22 reduced the content of anthocyanidin 3,5-O-diglucoside in P. ‘He Xie’. Conclusions A UDP-glycosyltransferase, PhUGT78A22, was identified in P. ‘He Xie’, and the molecular mechanism underlying differential distribution of anthocyanins within petals was elucidated. This study provides new insights on the biosynthesis of different kinds of anthocyanins within colorful petals, and helps to explain petal blotch formation, which will facilitate the cultivar breeding with respect to increasing ornamental value. Additionally, it provides a reference for understanding the molecular mechanisms responsible for precise regulation of anthocyanin biosynthesis and distribution patterns.

Integrative Metabolomic and Transcriptomic Analyses Reveal the Mechanism of Petal Blotch Formation in Rosa persica

“…In this study, DFR (Rbe013916), ANS (Rbe016466), and UFGT (Rbe026328) were specifically highly expressed in the blotch parts of R. persica petals. Their expression patterns were consistent with the expression of PsDFR, PsANS, and PhUGT78A22 in peonies [42][43][44]. Moreover, the abundance of anthocyanins showed a similar trend, which could be attributed to the high expression of these aforementioned genes in the blotch parts of petals.…”

“…Additionally, four structural genes, ScCHS2, ScF3H1, ScDFR3, and ScANS, were inhibited in the colorless regions of the bicolor cultivars of S. cruentus [30]. Similarly, the differentially expressed anthocyanin structural genes of PsCHS, PsF3 ′ H, PsDFR, and PsANS were expressed at a significantly higher level in the spot than the non-spot areas of the petals of P. suffruticosa [42]; PhUGT78A22 can catalyze the conversion of cyanidin-3-O-glucoside and peonidin-3-O-glucoside to cyanidin-3,5-O-glucoside and peonidin-3,5-O-glucoside during blotch formation [43]. In this study, DFR (Rbe013916), ANS (Rbe016466), and UFGT (Rbe026328) were specifically highly expressed in the blotch parts of R. persica petals.…”

Transcriptome and metabolome combine to analyze the mechanism of leaf coloration formation in Aeonium arboretum ‘Pink Sybil’

“…It converts unstable anthocyanins into stable anthocyanins via glycosylation. In Paeonia, variations in Ph UGT78A22 expression resulted in distinct glycosylation of pigments in the spotted and unspotted regions of the petals, resulting in floral color variations (Li et al 2022). Furthermore, high expression of UFGT increased the red pigmentation of the fruit skin.…”

Establishment of a Homologous Silencing System with Intact-Plant Infiltration and Minimized Operation for Studying Gene Function in Herbaceous Peonies

“…Tree peonies are a group of woody species in the family Paeoniaceae, and they and herbaceous peonies are generally collectively referred to as "peonies". The silencing of flavonoid glycosyltransferase genes (UFGTs) and rooting-related oxygenase (ARRO-1) by VIGS in a tree peony, i.e., P. suffruticosa (a species of tree peonies), showed that the two genes play key roles in flower color formation and root development [21,22]. The TRYPTOPHAN DECARBOXYLASE gene (TDC) and WRKY41a are highly expressed in stems of P. lactiflora, and their silencing by VIGS decreases the secondary wall thickness and distinctly weakens the stem strength.…”

“…From the abovementioned examples, it can be seen that only a few studies have reported the gene functions identified by VIGS and the infected organs are totally different, indicating that this technique remains immature in research on peonies. To explore gene functions in peonies using VIGS, an intact plant remains the optimal material for infection, phenotype observation, and gene function validation, although in vitro organs such as petals and flower buds could also be used as infection materials for gene silencing and to verify their functions to a certain degree [21,28]. For example, the dormancy of in vitro inner flower buds without outer scales in MS medium cultivation is not exactly equivalent to the dormancy of mixed buds generated on underground rhizomes of an intact plant in field or pot cultivation.…”