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This research was supported by the Natural Science Foundation of China (No. 31471898) and the Key Technology Research of Oil Peony Industry in Shaanxi Province (2014HXFWYL016) and Special project to Build World‐class Disciplines Of Beijing Forestry University (2019XKJS0324). Determining the factors promoting speciation is a major task in ecological and evolutionary research and can be aided by phylogeographic analysis. The Qinling–Daba Mountains (QDM) located in central China form an important geographic barrier between southern subtropical and northern temperate regions, and exhibit complex topography, climatic, and ecological diversity. Surprisingly, few phylogeographic analyses and studies of plant speciation in this region have been conducted. To address this issue, we investigated the genetic divergence and evolutionary histories of three closely related tree peony species (Paeonia qiui, P. jishanensis, and P. rockii) endemic to the QDM. Forty populations of the three tree peony species were genotyped using 22 nuclear simple sequence repeat markers (nSSRs) and three chloroplast DNA sequences to assess genetic structure and phylogenetic relationships, supplemented by morphological characterization and ecological niche modeling (ENM). Morphological and molecular genetic analyses showed the three species to be clearly differentiated from each other. In addition, coalescent analyses using DIYABC conducted on nSSR variation indicated that the species diverged from each other in the late Pleistocene, while ecological niche modeling (ENM) suggested they occupied a larger area during the Last Glacial Maximum (LGM) than at present. The combined genetic evidence from nuclear and chloroplast DNA and the results of ENM indicate that each species persisted through the late Pleistocene in multiple refugia in the Qinling, Daba, and Taihang Mountains with divergence favored by restricted gene flow caused by geographic isolation, ecological divergence, and limited pollen and seed dispersal. Our study contributes to a growing understanding of the origin and population structure of tree peonies and provides insights into the high level of plant endemism present in the Qinling–Daba Mountains of Central China. Publisher PDF

Tree peony (Paeonia Sect. Moutan) is an economically important ornamental plant, but little is known about the genetic architecture of important ornamental traits. To effectively improve ornamental value, we require a better understanding of genetic architecture in the complex traits of the tree peony. Association mapping is a powerful tool for detection of variation associated with traits. Thus, we examined the genetic diversity and the population structure of 462 unrelated cultivated P. rockii individuals, then performed association mapping to identify simple sequence repeat (SSR) markers associated with 12 floral traits. We observed a moderate level of genetic diversity (PIC = 0.459) and low linkage disequilibrium (LD) between markers, demonstrating that the potential value of an LD approach in elucidating the molecular basis of the quantitative variation in this species. An analysis of population structure revealed three subgroups in the association population. Subsequent single-marker association analysis identified 46 significant associations, involving the 11 traits with 37 SSRs. These loci explained a small proportion of the phenotypic variance, ranging from 2.68 to 23.97% (mean 5.50%). We also validated 15 of the 46 associations in a linkage mapping population of 159 individuals. Finally, five associations were further confirmed in the linkage mapping population, involving the four traits with four SSRs. These results can serve as a foundation for further analyses of the genetic architecture of floral traits, and the SSRs associated in this work have potential applications in marker-assisted breeding in tree peony.

Paeonia jishanensis, one of the most important ancestral species of cultivated tree peonies, is an endangered ornamental and medicinal plant endemic to China. A total of 236 individuals of P. jishanensis from 10 extant populations were analysed using 21 EST-SSR markers to assess their genetic diversity and population structure. Moderate genetic diversity levels (HE = 0.340) and high genetic differentiation among populations (FST = 0.335) were revealed. Combining the results of STRUCTURE, PCoA and neighbour-joining analyses, the 10 populations were divided into four genetic groups that were significantly related to their geographical origins, which was further supported by hierarchical AMOVA showing the highest variation of 17.9% among groups. The Mantel test showed a significant positive correlation between genetic distance and geographic distance among populations (r = 0.873, P

Tree peony (Paeonia sect. Moutan) is a famous ornamental crop worldwide that is difficult to propagate. The present study provides efficient protocols for the micropropagation of three economically important tree peony cultivars (Paeonia suffruticosa ‘Jin Pao Hong’, P. suffruticosa ‘Wu Long Peng Sheng’, and P. × lemoinei ‘High Noon’). For optimal shoot multiplication, different concentrations of GA3 were added into woody plant medium (WPM) (double strength Ca2+) containing 1.0 mg l−1 BAP; 0.5 mg l−1 GA3 yielded the highest multiplication rate with more than 4 shoots per explant for the three cultivars. For better rooting, different polyamines (putrescine, spermine, or spermidine) were added individually to half-strength MS medium containing 1.0 mg l−1 IBA. 5.0, 1.0, and 1.0 mg l−1 putrescine produced the optimal rooting for ‘Jin Pao Hong’ (100%), ‘Wu Long Peng Sheng’ (100%), and ‘High Noon’ (80%), respectively; each rooted shoot had 4–6 roots measuring 4–6 cm in length. Poor survival rates during acclimatization were obtained for ‘Jin Pao Hong’ (52.6%), ‘Wu Long Peng Sheng’ (40.1%), and ‘High Noon’ (64.0%) when the plantlets were grown in uninoculated vermiculite/peat/perlite sterilized substrate; in contrast, ‘High Noon’ plantlets inoculated with Glomus mosseae showed a high survival rate (83.4%) and vigorous growth. The protocols reported in this study can be used for rapid and large-scale propagation of the three tree peony cultivars. Furthermore, this study raises interesting possibilities for stimulating the in vitro rooting of tree peony cultivars through polyamine application and for improving the ex vitro establishment of tree peony plantlets through arbuscular mycorrhizal fungi inoculation.

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Paeonia ostii, a member of tree peony, is an emerging oil crop with important medical and oil uses and widely cultivated in China. Dissolving the genetic diversity and domestication history of this species is important for further genetic improvements and deployments. We firstly selected 29 simple sequence repeats (SSRs) via transcriptome mining, segregation analyses and polymorphism characterizations; then, 901 individuals from the range-wide samples were genotyped using well-characterized SSR markers. We observed moderate genetic diversity among individuals, and Shaanxi Province was identified as the center of genetic diversity for our cultivated plants. Five well-separated gene pools were detected by STRUCTURE analyses, and the results suggested that multiple independent domestication origins occurred in Shaanxi Province and Tongling City (Anhui Province). Taken together, the genetic evidence and the historical records suggest multiple long-distance introductions after the plant was domesticated in Shandong, Henan and Hunan provinces. The present study provides the first genetic evaluation of the domestication history of P. ostii, and our results provide an important reference for further genetic improvements and deployments of this important crop.

An understanding of plant domestication history provides insights into general mechanisms of plant adaptation and diversification and can guide breeding programmes that aim to improve cultivated species. Cultivated tree peonies (genus Paeonia L.) are among the most popular ornamental plants in the world; yet, the history of their domestication is still unresolved. Here, we explored whether the domestication in China of historically cultivated peonies, that is, the common and flare cultivated tree peonies, was a single event or whether independent domestications occurred. We used 14 nuclear microsatellite markers and a comprehensive set of 553 tree peonies collected across China, including common tree peonies, flare tree peonies and the wild species or subspecies that are potential contributors to the cultivated tree peonies, that is, Paeonia rockii ssp. rockii, P. rockii ssp. atava, P. jishanensis and P. decomposita. Assignment methods, a principal component analysis and approximate Bayesian computations provided clear evidence for independent domestications of these common tree and flare tree peonies from two distinct and allopatric wild species, P. jishanensis and P. rockii ssp. atava, respectively. This study provides the first example of independent domestications of cultivated trees from distinct species and locations. This work also yields crucial insight into the history of domestication of one of the most popular woody ornamental plants. The cultivated peonies represent an interesting case of parallel and convergent evolution. The information obtained in this study will be valuable both for improving current tree peony breeding strategies and for understanding the mechanisms of domestication, diversification and adaptation in plants.

Herbaceous peony (Paeonia lactiflora) is a globally important ornamental plant. Spontaneous floral mutations occur frequently during cultivation, and are selected as a way to release new cultivars, but the underlying evolutionary developmental genetics remain largely elusive. Here, we investigated a collection of spontaneous corolla mutational plants (SCMPs) whose other floral organs were virtually unaffected. Unlike the corolla in normal plants (NPs) that withered soon after fertilization, the transformed corolla (petals) in SCMPs was greenish and persistent similar to the calyx (sepals). Epidermal cellular morphology of the SCMP corolla was also similar to that of calyx cells, further suggesting a sepaloid corolla in SCMPs. Ten floral MADS-box genes from these Paeonia plants were comparatively characterized with respect to sequence and expression. Codogenic sequence variation of these MADS-box genes was not linked to corolla changes in SCMPs. However, we found that both APETALA3 (AP3) and PISTILLATA (PI) lineages of B-class MADS-box genes were duplicated, and subsequent selective expression alterations of these genes were closely associated with the origin of SCMPs. AP3-PI obligate heterodimerization, essential for organ identity of corolla and stamens, was robustly detected. However, selective down-regulation of these duplicated genes might result in a reduction of this obligate heterodimer concentration in a corolla-specific manner, leading to the sepaloid corolla in SCMPs, thus representing a new sepaloid corolla model taking advantage of gene duplication. Our work suggests that modifying floral MADS-box genes could facilitate the breeding of novel cultivars with distinct floral morphology in ornamental plants, and also provides new insights into the functional evolution of the MADS-box genes in plants.