Light-mediated anthocyanin biosynthesis in rose petals involves a balanced regulatory module comprising transcription factors RhHY5, RhMYB114a, and RhMYB3b

Abstract

Roses are significant botanical species with both ornamental and economic value, displaying diverse floral traits, particularly an extensive array of petal colors. The red pigmentation of rose petals is predominantly attributed to anthocyanin accumulation. However, the underlying regulatory mechanism of anthocyanin biosynthesis in roses remains elusive. This study presents a novel light-responsive regulatory module governing anthocyanin biosynthesis in rose petals, which involves the transcription factors RhHY5, RhMYB114a, and RhMYB3b. Under light conditions, RhHY5 represses RhMYB3b expression, and induces RhMYB114a expression that positively regulates anthocyanin biosynthesis in rose petals through the direct activation of anthocyanin structural genes via the MYB114a-bHLH3-WD40 complex. Notably, this function likely involves an interaction and synergy between RhHY5 and the MYB114a-bHLH3-WD40 complex. Additionally, RhMYB3b is activated by RhMYB114a to prevent excessive accumulation of anthocyanin. Conversely, in low light conditions, the degradation of RhHY5 leads to down-regulation of RhMYB114a and up-regulation of RhMYB3b, which in turn inhibits the expression of both RhMYB114a and anthocyanin structural genes. Additionally, RhMYB3b competes with RhMYB114a for binding to RhbHLH3 and the promoters of anthocyanin-related structural genes. Overall, our study uncovers a complex light-mediated regulatory network that governs anthocyanin biosynthesis in the rose, thereby advancing our understanding of the underlying molecular mechanisms of anthocyanin biosynthesis in rose flowers.

Haplotype-resolved genome assembly of the diploid Rosa chinensis provides insight into the mechanisms underlying key ornamental traits

“…Previous studies have reported that S6 subgroup of MYB involved in anthocyanin accumulation, contained 5 genes ( RcMYB113a , RcMYB113b , RcMYB113c , RcMYB114a and RcMYB114b ) (Li et al, 2021 ). Three of them ( MYB113a, RcMYB11 3c called RcMYB114 in previous reports, and RcMYB114a ), have been reported (Lin-Wang et al, 2010 ; Li et al 2022 , Yan et al 2023 ). In our study, another new gene RcMYB114b was identified .…”

“…The expression of RcMYB114a was up-regulated at the flower in early opening stage and highest at the fully open flower stage, whereas the expression of RcMYB114b was highest at the flower in early opening stage and down-regulated at the fully open flower stage. Different from above, RcMYB11 3c was largely unexpressed (Yan et al 2023 ). In addition, different expression patterns of homologous genes were also found in strawberry, which may affect fruit color (Lin-Wang et al, 2010 ).…”

“…These reported showed that although these five genes belong to the same subfamily, they not only regulate different metabolite accumulation, but also have different expression sites/periods. For example, RcMYB114a (Yan et al 2023 ) and RcMYB114b promoted cyanidin-3-glucoside accumulation. While RcMYB113c promoted cyanidin-3-O-sophoroside accumulation (Li et al 2022 ).…”

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

“…Similarly, LhMYB18 interacted with LhbHLH2 to activate the promoter of DFR, which was responsible for large spot formation in an Asiatic hybrid lily cultivar [19], while HaMYB1 modulated UFGT to promote anthocyanin accumulation in Helianthus annuus [48]. Recently, RcMYB1 [49], RhMYB114a [50], RhMYB3b [50], and Rosa1 [51] were shown to play roles in anthocyanin synthesis in roses. In this study, three MYBs and one MYB-related TF were highly associated with anthocyanins in R. persica.…”

“…Similarly, two R2R3-MYBs (DPL and PHZ) regulate the pigmentation pattern of flowers, and transcripts for PHZ are induced by high light in petunias [54]. In turn, light-responsive RhHY5 positively activates the expression of RhMYB114a and represses the expression of RhMYB3b to regulate anthocyanin biosynthesis in rose petals [50]. The overexpression of a C2H2-type zinc finger protein gene MdZAT5 in apple calli and Arabidopsis enhances anthocyanin accumulation [55].…”