Tree peony (Paeonia ostii) is an economically important ornamental plant native to China. It is also notable for its seed oil, which is abundant in unsaturated fatty acids such as α-linolenic acid (ALA). Here, we report chromosome-level genome assembly (12.28 Gb) ofP. ostii. In contrast to monocots with giant genomes, tree peony does not appear to have undergone lineage-specific whole-genome duplication. Instead, explosive LTR expansion in the intergenic regions within a short period (~ two million years) may have contributed to the formation of its giga-genome. In addition, expansion of five types of histone encoding genes may have helped maintain the giga-chromosomes. Further, we conduct genome-wide association studies (GWAS) on 448 accessions and show expansion and high expression of several genes in the key nodes of fatty acid biosynthetic pathway, includingSAD,FAD2andFAD3, may function in high level of ALAs synthesis in tree peony seeds. Moreover, by comparing with cultivated tree peony (P. suffruticosa), we show that ectopic expression of class A geneAP1and reduced expression of class C geneAGmay contribute to the formation of petaloid stamens. Genomic resources reported in this study will be valuable for studying chromosome/genome evolution and tree peony breeding.

Most common plant oils have little α-linolenic acid (C18:3^Δ9,12,15, ALA) and an unhealthy ω6/ω3 ratio. Here, fatty acids (FAs) in the seeds of 11 species of Paeonia L., including 10 tree peony and one herbaceous species, were explored using gas chromatograph–mass spectrometer. Results indicated that all Paeonia had a ω6/ω3 ratio less than 1.0, and high amounts of ALA (26.7–50%), oleic acid (C18:1^Δ9, OA) (20.8–46%) and linoleic acid (C18:2^Δ9,12, LA) (10–38%). ALA was a dominant component in oils of seven subsection Vaginatae species, whereas OA was predominant in two subsection Delavayanae species. LA was a subdominant oil component in P. ostii and P. obovata. Moreover, the FA composition and distribution of embryo (22 FAs), endosperm (14 FAs) and seed coat (6 FAs) in P. ostii, P. rockii and P. ludlowii were first reported. Peony species, particularly P. decomposita and P. rockii, can be excellent plant resources for edible oil because they provide abundant ALA to balance the ω6/ω3 ratio. The differences in the ALA, LA and OA content proportion also make the peony species a good system for detailed investigation of FA biosynthesis pathway and ALA accumulation.

Paeoniaceae is an abundant germplasm resource with significant medicinal values in China, the principal medicinal components of which include paeoniflorin and paeonol. These compounds are typically obtained from air-dried root samples, which the use of freeze-drying as an alternative method has not been tested. Additionally, the presence of these two compounds in various wild Paeoniaceae species has not been previously explored, nor have the differences between various plant organs been fully evaluated. Here, freeze-drying and air-drying methods were compared to assess the changes in paeoniflorin and paeonol in root samples using ultra-performance liquid chromatography-mass spectrometer. The contents of these compounds in the roots, leaves, stems, and petals were then tested in freeze-dried materials. We also quantitatively detected the paeoniflorin and paeonol contents in the roots of 14 species collected from 20 natural habitats. Results indicated that the paeoniflorin content decreased under air-drying in comparison to freeze-drying, while the opposite trend was observed for paeonol. Our findings also demonstrated that the root xylem of species in Section Moutan, particularly Paeonia ostii, contains considerable paeonol and paeoniflorin and should thus be fully utilized as a medicinal resource. Furthermore, paeonol was mainly detected in the roots, while paeoniflorin was widely distributed in different organs; the highest content was in the leaf at the budding stage, suggesting that the leaves should be developed as a new paeoniflorin resource. Paeoniflorin contents were also found to be higher at earlier development stages. Based on the standards of the Chinese Pharmacopoeia, five species of Section Moutan and six species of Section Paeonia could be used as potential traditional Chinese medicinal resources. These findings of this study enhance our understanding of these two medicinal compounds and provide a foundation for the further development and utilization of Paeoniaceae as medicinal plant resources.

Paeoniflorin, a monoterpene glucoside, is increasingly used in the clinical treatment of many diseases because it has a variety of pharmacological activities. Besides, paeoniflorin has been considered the characteristic chemical constituent of Paeoniaceae plants since it was first reported in 1963. Therefore, how to better develop and utilize paeoniflorin in Paeoniaceae has always been a research hotspot. We reviewed the current knowledge on paeoniflorin in Paeoniaceae, with particular emphasis on its distribution and influencing factors. Moreover, the limited understanding of the biosynthesis pathway has restricted the production of paeoniflorin by synthetic biology. This review provides insights into the post-modification pathway of paeoniflorin biosynthesis and proposes directions for further analysis in the future.

Paeonia ostii, a widely cultivated tree peony species in China, is a resourceful plant with medicinal, ornamental and oil value. However, fleshy roots lead to a low tolerance to waterlogging in P. ostii. In this study, P. ostii roots were sequenced using a hybrid approach combining single-molecule real-time and next-generation sequencing platforms to understand the molecular mechanism underlying the response to this sequentially waterlogging stress, the normal growth, waterlogging treatment (WT), and waterlogging recovery treatment (WRT). Our results indicated that the strategy of P. ostii, in response to WT, was a hypoxic resting syndrome, wherein the glycolysis and fermentation processes were accelerated to maintain energy levels and the tricarboxylic acid cycle was inhibited. P. ostii enhanced waterlogging tolerance by reducing the uptake of nitrate and water from the soil. Moreover, transcription factors, such as AP2/EREBP, WRKY, MYB, and NAC, played essential roles in response to WT and WRT. They were all induced in response to the WT condition, while the decreasing expression levels were observed under the WRT condition. Our results contribute to understanding the defense mechanisms against waterlogging stress in P. ostii.