Abstract
The origin of cultivated tree peonies, known as the ‘king of flowers' in China for more than 1000 years, has attracted considerable interest, but remained unsolved. Here, we conducted phylogenetic analyses of explicitly sampled traditional cultivars of tree peonies and all wild species from the shrubby section Moutan of the genus Paeonia based on sequences of 14 fast-evolved chloroplast regions and 25 presumably single-copy nuclear markers identified from RNA-seq data. The phylogeny of the wild species inferred from the nuclear markers was fully resolved and largely congruent with morphology and classification. The incongruence between the nuclear and chloroplast trees suggested that there had been gene flow between the wild species. The comparison of nuclear and chloroplast phylogenies including cultivars showed that the cultivated tree peonies originated from homoploid hybridization among five wild species. Since the origin, thousands of cultivated varieties have spread worldwide, whereas four parental species are currently endangered or on the verge of extinction. The documentation of extensive homoploid hybridization involved in tree peony domestication provides new insights into the mechanisms underlying the origins of garden ornamentals and the way of preserving natural genetic resources through domestication.
Highlights
Agricultural and industrial developments have considerably reduced biodiversity, which in turn has threatened our sustainability [1,2]
Variable intron markers from 25 genes that could be sequenced with the least sequence polymorphism within an individual were identified as nuclear markers
For marker 4, the cultivars were found to share sequences with P. rockii and P. ostii. These results suggest that the tree peony cultivars originated from hybridization between multiple wild species, including P. cathayana, P. rockii, P. qiui, P. ostii and P. jishanensis
Summary
Agricultural and industrial developments have considerably reduced biodiversity, which in turn has threatened our sustainability [1,2]. This study represents a comprehensive effort to investigate the origin of cultivated tree peonies with the complete sampling of all wild species and extensive sampling of traditional cultivars, together with multiple phylogenetic markers from both nuclear and chloroplast genomes. The total of 441 accessions from all 37 known populations of the nine wild tree peony species were previously collected in Anhui, Gansu, Henan, Hubei, Shaanxi, Shanxi, Sichuan, Xizang and Yunnan Provinces of China, and the genetic variations within and among these populations were evaluated [17,18]. For the study of the origins of the cultivars, the four chloroplast regions that were most variable among the wild species were sequenced and used as phylogenetic markers for analysing cultivars and wild species. Convergence of MCMC chain was explored by running at least two independent analyses and checked by TRACER v. 1.4
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