The spatio‐temporal biosynthesis of floral flavonols is controlled by differential phylogenetic MYB regulators in Freesia hybrida

Abstract

Floral flavonols play specific pivotal roles in pollinator attraction, pollen germination and fertility, in addition to other functions in vegetative organs. For many plants, the process of flavonol biosynthesis in late flower development stages and in mature flower tissues is poorly understood, in contrast to early flower development stages. It is thought that this process may be regulated independently of subgroup 7 R2R3 MYB (SG7 MYB) transcription factors. In this study, two FLS genes were shown to be expressed synchronously with the flower development-specific and tissue-specific biosynthesis of flavonols in Freesia hybrida. FhFLS1 contributed to flavonol biosynthesis in early flower buds, toruses and calyxes, and was regulated by four well-known SG7 MYB proteins, designated as FhMYBFs, with at least partial regulatory redundancy. FhFLS2 accounted for flavonols in late developed flowers and in the petals, stamens and pistils, and was targeted directly by non SG7 MYB protein FhMYB21L2. In parallel, AtMYB21 and AtMYB24 also activated AtFLS1, a gene highly expressed in Arabidopsis anthers and pollen, indicating the conserved regulatory roles of MYB21 against FLS genes in these two evolutionarily divergent angiosperm plants. Our results reveal a novel regulatory and synthetic mechanism underlying flavonol biosynthesis in floral organs and tissues which may be exploited to investigate supplementary roles of flavonols in flowers.

Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions

“…Spotted or striped pigmentation patterns in petals of monkeyflower ( Mimulus ) are derived from the interaction of a local autocatalytic feedback loop and a long‐range inhibitory feedback loop, which give rise to dispersed anthocyanin spots (Ding et al, 2020). Flavonols such as kaempferol derivatives and quercetin derivatives and anthocyanins such as malvidin 3‐glucoside confer the red color of petals of Freesia hybrida (Shan et al, 2020; Li et al, 2020f). Anthocyanins are also required for the pigmentation of purple leaves and the spikelet hull in rice (Chin et al, 2016; Sun et al, 2018a) and purple tea ( Camellia sinensis ; Kumari et al, 2019).…”

Plant Volatile Organic Compounds Evolution: Transcriptional Regulation, Epigenetics and Polyploidy

“…In contrast to ODO1, EBOII and EBOI, the MYB4 TF is a specific repressor of the cinnamate-4-hydroxylase from the phenylpropanoid pathway, consequently controlling the flux towards phenylpropanoid volatile compounds in petunias [ 89 ]. Recently, R2R3-MYB TFs were found to regulate flavonol biosynthesis through targeting flavonol synthase (FLS) genes in Freesia × hybrida [ 90 ]. FLS genes are responsible for the spatio-temporal biosynthesis of floral flavonols and are regulated by the well-known SG7 MYB protein family [ 85 , 91 ], but MYB21 was also found to regulate FLS [ 90 ].…”

“…Recently, R2R3-MYB TFs were found to regulate flavonol biosynthesis through targeting flavonol synthase (FLS) genes in Freesia × hybrida [ 90 ]. FLS genes are responsible for the spatio-temporal biosynthesis of floral flavonols and are regulated by the well-known SG7 MYB protein family [ 85 , 91 ], but MYB21 was also found to regulate FLS [ 90 ]. The MYB21 TF has been considered a terpenoid biosynthesis regulator, so there might exist a connection between terpenoids and flavonoid biosynthesis, but it is still unclear.…”

Involvement of the R2R3-MYB transcription factor MYB21 and its homologs in regulating flavonol accumulation in Arabidopsis stamen

“…Most recently, it has been reported that MYB99 modulates phenylpropanoid biosynthesis in a regulatory triad with MYB21 and MYB24 ( Battat et al , 2019 ). Furthermore, Shan et al (2020) reported that FhMYB21L1 and FhMYB21L2 activated FhFLS1 expression by directly binding to its promoter regions in Freesia hybrida . Given that AtMYB21 and AtMYB24 are the homologs of FhMYB21L1 and FhMYB21L2 in Arabidopsis, both have been predicted to regulate AtFLS1 expression ( Shan et al , 2020 ).…”

“…Furthermore, Shan et al (2020) reported that FhMYB21L1 and FhMYB21L2 activated FhFLS1 expression by directly binding to its promoter regions in Freesia hybrida . Given that AtMYB21 and AtMYB24 are the homologs of FhMYB21L1 and FhMYB21L2 in Arabidopsis, both have been predicted to regulate AtFLS1 expression ( Shan et al , 2020 ). However, the molecular mechanism and biological function of MYB21/24/57 in the regulation of flavonol biosynthesis require further investigation in vitro and in vivo .…”