College of Horticulture and Landscape Architecture, Yangzhou University, Yangzhou 225009, Jiangsu, China.
Joint International Research Laboratory of Agriculture and Agri-Product Safety, The Ministry of Education of China, Yangzhou University, Yangzhou 225009, Jiangsu, China.
Plant Physiol. 2024 Nov 4;196(3):1869-1886. doi: 10.1093/plphys/kiae420.
Blotches in floral organs attract pollinators and promote pollination success. Tree peony (Paeonia suffruticosa Andr.) is an internationally renowned cut flower with extremely high ornamental and economic value. Blotch formation on P. suffruticosa petals is predominantly attributed to anthocyanin accumulation. However, the endogenous regulation of blotch formation in P. suffruticosa remains elusive. Here, we identified the regulatory modules governing anthocyanin-mediated blotch formation in P. suffruticosa petals, which involves the transcription factors PsMYB308, PsMYBPA2, and PsMYB21. PsMYBPA2 activated PsF3H expression to provide sufficient precursor substrate for anthocyanin biosynthesis. PsMYB21 activated both PsF3H and PsFLS expressions and promoted flavonol biosynthesis. The significantly high expression of PsMYB21 in nonblotch regions inhibited blotch formation by competing for anthocyanin biosynthesis substrates, while conversely, its low expression in the blotch region promoted blotch formation. PsMYB308 inhibited PsDFR and PsMYBPA2 expressions to directly prevent anthocyanin-mediated blotch formation. Notably, a smaller blotch area, decreased anthocyanin content, and inhibition of anthocyanin structural gene expression were observed in PsMYBPA2-silenced petals, while the opposite phenotypes were observed in PsMYB308-silenced and PsMYB21-silenced petals. Additionally, PsMYBPA2 and PsMYB308 interacted with PsbHLH1-3, and their regulatory intensity on target genes was synergistically regulated by the PsMYBPA2-PsbHLH1-3 and PsMYB308-PsbHLH1-3 complexes. PsMYB308 also competitively bound to PsbHLH1-3 with PsMYBPA2 to fine-tune the regulatory network to prevent overaccumulation of anthocyanin in blotch regions. Overall, our study uncovers a complex R2R3-MYB transcriptional regulatory network that governs anthocyanin-mediated blotch formation in P. suffruticosa petals, providing insights into the molecular mechanisms underlying blotch formation in P. suffruticosa.
花器官上的斑点吸引传粉者并促进传粉成功。牡丹（Paeonia suffruticosa Andr.）是一种国际知名的切花，具有极高的观赏和经济价值。牡丹花瓣上的斑点形成主要归因于花色素苷的积累。然而，牡丹斑点形成的内在调节机制仍不清楚。在这里，我们鉴定了调控牡丹花瓣中花色素苷介导的斑点形成的调控模块，该模块涉及转录因子 PsMYB308、PsMYBPA2 和 PsMYB21。PsMYBPA2 激活 PsF3H 的表达，为花色素苷生物合成提供足够的前体底物。PsMYB21 同时激活 PsF3H 和 PsFLS 的表达，促进类黄酮生物合成。PsMYB21 在非斑点区域的高表达通过竞争花色素苷生物合成底物来抑制斑点形成，而在斑点区域的低表达则促进斑点形成。PsMYB308 抑制 PsDFR 和 PsMYBPA2 的表达，直接防止花色素苷介导的斑点形成。值得注意的是，在 PsMYBPA2 沉默的花瓣中观察到斑点面积较小、花色素苷含量降低以及花色素苷结构基因表达受到抑制，而在 PsMYB308 沉默和 PsMYB21 沉默的花瓣中观察到相反的表型。此外，PsMYBPA2 和 PsMYB308 与 PsbHLH1-3 相互作用，它们对靶基因的调节强度受到 PsMYBPA2-PsbHLH1-3 和 PsMYB308-PsbHLH1-3 复合物的协同调节。PsMYB308 还与 PsMYBPA2 竞争结合 PsbHLH1-3，以微调调控网络，防止花色素苷在斑点区域过度积累。总的来说，我们的研究揭示了一个复杂的 R2R3-MYB 转录调控网络，该网络调控牡丹花瓣中花色素苷介导的斑点形成，为牡丹斑点形成的分子机制提供了新的见解。
