The plastome reveals new insights into the evolutionary and domestication history of peonies in East Asia

Abstract

Backgroud Paeonia holds considerable value in medicinal, ornamental horticultural, and edible oil industries, but the incomplete state of phylogenetic research in this genus poses a challenge to the effective conservation and development of wild germplasm, and also impedes the practical utilization of existing cultivars. Due to its uniparental inheritance and lack of recombination, the plastome (i.e., plastid genome), which is a valuable molecular marker for phylogenetic analyses, is characterized by an appropriate rate of nucleotide evolution. Methods In this study, 10 newly assembled data and available reported data were combined to perform a comparative genomics and phylogenetics analysis of 63 plastomes of 16 Paeonia species, primarily from East Asia, which is the origin and diversity center of Paeonia. Results Ranging between 152,153 and 154,405 bp, most plastomes displayed a conserved structure and relatively low nucleotide diversity, except for six plastomes, which showed obvious IR construction or expansion. A total of 111 genes were annotated in the Paeonia plastomes. Four genes (rpl22, rps3, rps19 and ycf1) showed different copy numbers among accessions while five genes (rpl36, petN, psbI, rpl33 and psbJ) showed strong codon usage biases (ENC < 35). Additional selection analysis revealed that no genes were under positive selection during the domestication of tree peony cultivars whereas four core photosynthesis-related genes (petA, psaA, psaB and rbcL) were under positive selection in herbaceous peony cultivars. This discovery might contribute to the wide adaption of these cultivars. Two types of molecular markers (SSR and SNP) were generated from the 63 plastomes. Even though SSR was more diverse than SNP, it had a weaker ability to delimit Paeonia species than SNP. The reconstruction of a phylogenetic backbone of Paeonia in East Asia revealed significant genetic divergence within the P. ostii groups. Evidence also indicated that the majority of P. suffruticosa cultivars had a maternal origin, from P. ostii. The results of this research also suggest that P. delavayi var. lutea, which likely resulted from hybridization with P. ludlowii, should be classified as a lineage within the broader P. delavayi group. Conclusions Overall, this study’s research findings suggest that the Paeonia plastome is highly informative for phylogenetic and comparative genomic analyses, and could be useful in future research related to taxonomy, evolution, and domestication.

The complete chloroplast genome of the first registered Paeonia Itoh hybrid cv. Hexie in China

“…The following sequences were used: P. suffruticosa JQ952559 (Chen et al. 2023 ), P. ostii MK701990 (Guo et al. 2020 ), P. decomposita NC_039425 (Chen et al.…”

“… 2018 ), P. anomala MT210549 (Chen et al. 2023 ), P. lactiflora MZ636553 (unpublished), P. mairei MZ617462 (unpublished), P. veitchii NC_032401 (Samigullin et al. 2018 ), P. intermedia MT210547 (Chen et al.…”

“… 2018 ), P. intermedia MT210547 (Chen et al. 2023 ), P. ovovata NC_026076 (Samigullin et al. 2018 ), P. obovate subsp.…”

Complete Plastid Genome Sequences of Three Tropical African Beilschmiediineae Trees (Lauraceae: Crytocaryeae)

“…Comparative plastome analyses have revealed structural variations, gene content differences, and evolutionary rate variations that provide insights into the phylogenetic relationships and evolutionary history of these plant groups, as evidenced by studies on Betulaceae [53], Paeonia (Paeoniaceae) [54], and Trollius (Ranunculaceae) [55]. In this study, by comparing cp genome analyses, we hope to shed light on the evolutionary relationships between species and gain insight into the mechanisms of adaptation and differentiation in their respective habitats (Madagascar and sub-Saharan Africa).…”

The pan-plastome of Hemerocallis citrina reveals new insights into the genetic diversity and cultivation history of an economically important food plant

“…Wang et al assembled 316 plastomes of Nelumbo nucifera , constructed a panplastome genome atlas, mapped phylogeographic patterns, and resolved seven well-supported genetic clusters to describe the genetic diversity in this species [ 12 ]. Qihang Chen et al studied the plastomes of East Asian peonies and used these data to resolve their evolutionary and domestication history [ 13 ]. Magdy et al constructed the panplastome of Capsicum spp.…”