Paeonia rockii is a wild tree peony species with large and dark purple variegations at the base of its petals. It is the genetic resource for various variegation patterns in tree peony cultivars, which is in contrast to the pure white petals of Paeonia ostii. However, the molecular mechanism underlying the formation of variegation in this plant is still unknown. Here, we conducted Illumina transcriptome sequencing for P. rockii, P. ostii (with pure white petals) and their F1 individuals (with purple-red variegation). A total of 181,866 unigenes were generated, including a variety of unigenes involved in anthocyanin biosynthesis and sequestration and the regulation of anthocyanin biosynthesis. The dark purple or purple-red variegation patterns mainly occurred due to the proportions of cyanidin (Cy)- and peonidin (Pn)-based anthocyanins. The variegations of P. rockii exhibited a “Cy > Pn” phenotype, whereas the F1 progeny showed a “Pn > Cy” phenotype. The CHS, DFR, ANS, and GST genes might play key roles in variegation pigmentation in P. rockii according to gene expression and interaction network analysis. Two R2R3-MYB transcription factors (c131300.graph_c0 and c133735.graph_c0) regulated variegation formation by controlling CHS, ANS and GST genes. Our results indicated that the various variegation patterns were caused by transcriptional regulation of anthocyanin biosynthesis genes, and the transcription profiles of the R2R3-MYBs provided clues to elucidate the mechanisms underlying this trait. The petal transcriptome data produced in this study will provide a valuable resource for future association investigations of the genetic regulation of various variegation patterns in tree peonies.

As a crucial medicinal group in Paeoniaceae, Paeonia plants are rich in bioactive monoterpenoids and phenolic compounds (e.g., paeoniflorin, paeonol, and flavonoids) in their roots, flowers, and other parts. They serve as core medicinal resources in traditional Chinese medicine (TCM) for nourishing blood, activating blood circulation, alleviating inflammation, and relieving pain. In recent years, in-depth studies have clearly elucidated the molecular mechanisms of these bioactive components. With breakthroughs in whole-genome sequencing, transcriptomics, and metabolomics technologies, over 100 secondary metabolites in Paeonia plants has been accurately identified, and multiple pharmacological mechanisms have been analyzed. This review systematically summarizes the current status of Paeonia plants in terms of plant resources, the exploration of bioactive components, analysis of the pharmacological mechanisms, and development/utilization. Combined with the cutting-edge progress in multi-omics technologies and synthetic biology, this review indicates the key directions of Paeonia in innovative drug research and development, aiming to provide a theoretical reference and technical support for the in-depth development of this group of medicinal plants.