Dan‐Qing Zhang’s research while affiliated with Shaanxi Normal University and other places

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Publications (6)


The only purple-flower species in Actaea L. is pollinated by a hornet
  • Article

July 2024

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12 Reads

Journal of Plant Ecology

Lin-Feng Qiu

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Jiu-Dong Zhang

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Ying Li

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[...]

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Examining the pollination biology of plant species is not only crucial for enhancing our understanding of their reproductive biology, but also essential for elucidating their adaptation and evolutionary history. Here, we investigated the breeding system and pollination biology of two closely related species in Actaea. The flower of A. purpurea is unique in the genus with purple and chartaceous (paper-like) sepals, fewer stamens with yellow anthers and purple filaments. Through three seasons of field observation and exclusion experiments, we determined that A. purpurea was primarily pollinated by a hornet species, Vespa bicolor, which also served as the most efficient pollinator. In contrast, A. japonica was primarily pollinated by large flies. A. purpurea exhibited a significantly higher cumulative nectar volume than A. japonica, which could be a crucial factor attracting V. bicolor. A control experiment further demonstrated that removing the nectar leaf (petal) significantly decreased the visiting frequency of V. bicolor. Breeding system studies revealed that both species were self-compatible, yet they primarily underwent outcrossing in natural habitats. Our study presents a compelling case of possible pollinator shift in A. purpurea accompanied by morphological divergence. A more in-depth investigation of this system would offer crucial insights into the extent to which pollinators are involved in the plant speciation process and whether they contribute to reproductive isolation between closely related species.


Circos map showing the landscape of the two Rhodiola genomes. (a) R. chrysanthemifolia; (b) R. kirilowii. From outside to inside, a. Chromosome length; b. GC content; c. Gene density; d. TE density; e. DNA transposon density; f. LTR/Copia density; g. LTR/Gypsy density; h. LINE density; i. SINE density. The most central curve connections indicate intraspecific collinearity.
Phylogenetic analysis of Rhodiola chrysanthemifolia, R. kirilowii and other representative angiosperm species. (a) Time tree and gene family evolution of the 17 angiosperm species. Expanded, contracted, and rapidly evolved gene families are shown in red, green, and violet, respectively. 1:1:1: Universal single‐copy gene, at most multiple copies and deletions in one species; N:N:N: Universal multi‐copy gene; P, the Paleocene, E, the Eocene, O, the Oligocene, M, the Miocene, Pli, the Pliocene, Q, the Quaternary; MRCA, most recent common ancestor; MYA, million years ago; (b) Venn graph showing number of genes shared by R. chrysanthemifolia, R. kirilowii, K. fedtschenkoi, V. vinifera, and A. thaliana, as well as species‐specific gene families relative to all 17 angiosperms; (c) KEGG enrichment bubble plot of significantly expanded gene families in R. chrysanthemifolia, R. kirilowii, and Rhodiola, respectively; (d) Distribution of LTR insertion time of the two Rhodiola species. LTR, long terminal repeat; MYA, million years ago.
Whole‐genome duplication analyses of the Rhodiola chrysanthemifolia and R. kirilowii genomes. (a) Macrosynteny between R. chrysanthemifolia, R. kirilowii, K. fedtschenkoi and V. vinifera. Gray lines indicate genome syntenic block connection, and R. chrysanthemifolia: R. kirilowii: K. fedtschenkoi: V. vinifera genes with a value of 2:2:2:1 were highlighted in color; (b) The syntenic depth of each grape gene corresponding to the genomes of R. chrysanthemifolia, R. kirilowii and K. fedtschenkoi. Syntenic depth refers to the number of times a syntenic block of a genomic region is syntenic with another genome; (c) Distribution of intraspecific Ks in R. chrysanthemifolia, R. kirilowii, K. fedtschenkoi and V. vinifera; (d) Distribution of interspecific Ks among R. chrysanthemifolia, R. kirilowii, K. fedtschenkoi and V. vinifera.
Chromosomal fusion/fission between Rhodiola chrysanthemifolia and R. kirilowii. (a) Macrosynteny between syntenic groups of R. chrysanthemifolia and R. kirilowii. Gray lines indicate genome syntenic block connection, and R. chrysanthemifolia and R. kirilowii genes with a value of 1:1 were highlighted in color; (b) Interspecific syntenic dot plot of R. chrysanthemifolia and R. kirilowii; (c) Syntenic bar plot of R. kirilowii chromosome with R. chrysanthemifolia as the reference genome; (d) EEJ pattern (terminal connection); (e) RTA pattern (chromosomal arm translocation); (f) NCF pattern (nested chromosome fusion); (g) Bar plot showing mean values of relative nucleotide diversity of R. chrysanthemifolia Chr1, Chr4, Chr6, and R. kirilowii Chr5, Chr9, Chr10 chromosomes.
Genes involved in the biosynthetic pathway of salidroside. (a) HPLC results of the crown and roots of Rhodiola chrysanthemifolia and R. kirilowii; UV = 277 nm, and the gray shade is the occurrence time of the salidroside peak; (b) Candidate genes and their relative expression level for the salidroside biosynthetic pathway of R. chrysanthemifolia and R. kirilowii; (c) The salidroside biosynthetic pathway candidate genes with upregulated expression only in rhizome and root of R. kirilowii. R, root; Ri, rhizome; S, stem; L, leaf; Fl, flower; Fr, fruit; (d) Correlation heat map of WGCNA module with traits; (e) Protein‐protein interaction network of the WGCNA darkolivegreen module.
Two chromosome‐level genome assemblies of Rhodiola shed new light on genome evolution in rapid radiation and evolution of the biosynthetic pathway of salidroside
  • Article
  • Publisher preview available

October 2023

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91 Reads

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9 Citations

Rhodiola L. is a genus that has undergone rapid radiation in the mid‐Miocene and may represent a typic case of adaptive radiation. Many species of Rhodiola have also been widely used as an important adaptogen in traditional medicines for centuries. However, a lack of high‐quality chromosome‐level genomes hinders in‐depth study of its evolution and biosynthetic pathway of secondary metabolites. Here, we assembled two chromosome‐level genomes for two Rhodiola species with different chromosome number and sexual system. The assembled genome size of R. chrysanthemifolia (2n = 14; hermaphrodite) and R. kirilowii (2n = 22; dioecious) were of 402.67 and 653.62 Mb, respectively, with approximately 57.60% and 69.22% of transposable elements (TEs). The size difference between the two genomes was mostly due to proliferation of long terminal repeat‐retrotransposons (LTR‐RTs) in the R. kirilowii genome. Comparative genomic analysis revealed possible gene families responsible for high‐altitude adaptation of Rhodiola, including a homolog of plant cysteine oxidase 2 gene of Arabidopsis thaliana (AtPCO2), which is part of the core molecular reaction to hypoxia and contributes to the stability of Group VII ethylene response factors (ERF‐VII). We found extensive chromosome fusion/fission events and structural variations between the two genomes, which might have facilitated the initial rapid radiation of Rhodiola. We also identified candidate genes in the biosynthetic pathway of salidroside. Overall, our results provide important insights into genome evolution in plant rapid radiations, and possible roles of chromosome fusion/fission and structure variation played in rapid speciation.

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Plastomic data shed new light on the phylogeny, biogeography, and character evolution of the family Crassulaceae

July 2023

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92 Reads

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12 Citations

Journal of Systematics and Evolution

Crassulaceae is a mid‐sized family of angiosperms, most species of which are herbaceous succulents, usually with 5‐merous flowers and one or two whorls of stamens. Although previous phylogenetic studies revealed seven major “clades” in Crassulaceae and greatly improved our understanding of the evolutionary history of the family, relationships among major clades are still contentious. In addition, the biogeographic origin and evolution of important morphological characters delimiting infrafamilial taxa have not been subject to formal biogeographic and character evolution analyses based on a well‐supported phylogeny backbone. In this study, we used plastomic data of 52 species, representing all major clades revealed in previous studies to reconstruct a robust phylogeny of Crassulaceae, based on which we unraveled the spatiotemporal framework of diversification of the family. We found that the family may originate in southern Africa and then dispersed to the Mediterranean, from there to eastern Asia, Macaronesia, and North America. The crown age of Crassulaceae was dated at ca . 63.93 million years ago, shortly after the Cretaceous–Paleogene (K‐Pg) boundary. We also traced the evolution of six important morphological characters previously used to delimit infrafamilial taxa and demonstrated widespread parallel and convergent evolution of both vegetative (life form and phyllotaxis) and floral characters (number of stamen whorls, petals free or fused, and flower merism). Our results provide a robust backbone phylogeny as a foundation for further investigations, and also some important new insights into biogeography and evolution of the family Crassulaceae.


Genomic data provide a robust phylogeny backbone for Rhodiola L. (Crassulaceae) and reveal extensive reticulate evolution during its rapid radiation

June 2023

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87 Reads

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7 Citations

Molecular Phylogenetics and Evolution

The Tibetan Plateau and adjacent mountain regions (TP; including the Tibetan Plateau, Himalaya, Hengduan Mountains and Mountains of Central Asia) harbor great biodiversity, some lineages on which may have undergone rapid radiations. However, only a few studies have investigated the evolutionary pattern of such diversification in depth using genomic data. In this study, we reconstructed a robust phylogeny backbone of Rhodiola, a lineage that may have undergone rapid radiation in the TP, using Genotyping-by-sequencing data, and conducted a series of gene flow and diversification analyses. The concatenation and coalescent-based methods yield similar tree topologies, and five well-supported clades were revealed. Potential gene flow and introgression events were detected, both between species from different major clades and closely related species, suggesting pervasive hybridization and introgression. An initial rapid and later slowdown of the diversification rate was revealed, indicating niche filling. Molecular dating and correlation analyses showed that the uplift of TP and global cooling in the mid-Miocene might have played an important role in promoting the rapid radiation of Rhodiola. Our work demonstrates that gene flow and introgression might be an important contributor to rapid radiation possibly by quickly reassembling old genetic variation into new combinations.


Nonadaptive molecular evolution of plastome during the speciation of Actaea purpurea and its relatives

September 2022

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85 Reads

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4 Citations

We have seen an explosive increase of plant plastid genome (plastome) sequences in the last decade, and the view that sequence variation in plastomes is maintained by the mutation‐drift balance has been challenged by new evidence. Although comparative genomic and population‐level studies provided us with evidence for positive evolution of plastid genes at both the macro‐ and micro‐evolution levels, less studies have systematically investigated how plastomes have evolved during the speciation process. We here sequenced 13 plastomes of Actaea purpurea (P.K. Hsiao) J. Compton, and its closest relatives, and conducted a systematic survey of positive selection in their plastid genes using the McDonald‐Kreitman test and codon‐based methods using maximum likelihood to estimate the ratio of nonsynonymous to synonymous substitutions (ω) across a phylogeny. We found that during the speciation of A. purpurea and its relatives, all plastid genes evolved neutrally or were under purifying selection. Genome size, gene order, and number were highly conserved. Comparing to A. purpurea, plastomes of Actaea japonica and Actaea biternata had low genetic diversity, consistent with previous studies. Our work not only sheds important light on the evolutionary history of A. purpurea and its kin, but also on the evolution of plastomes during plant speciation. Thirteen plastomes of 1representative populations of Actaea purpurea and its relatives were conserved with respect to size, structure, gene content, and order, with few variations. Positive selection analysis suggests that all plastid genes evolve neutrally or are subjected to purifying selection. Actaea japonica's low genetic diversity probably results from a recent expansion, not a recent selective sweep on plastid genes.


Divergence in the Aquilegia ecalcarata complex is correlated with geography and climate oscillations: Evidence from plastid genome data

September 2021

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208 Reads

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20 Citations

Quaternary climate oscillations and geographical heterogeneity play important roles in determining species and genetic diversity distribution patterns, but how these factors affect the migration and differentiation of East Asian plants species at the population level remains poorly understood. The Aquilegia ecalcarata complex, a group that originated in the Late Tertiary and is widely distributed throughout East Asia, displays high genetic variation that is suitable for studying elaborate phylogeographic patterns and demographic history related to the impact of Quaternary climate and geography. We used plastid genome data from 322 individuals in 60 populations of the A. ecalcarata complex to thoroughly explore the impact of Quaternary climate oscillations and geography on the phylogeographic patterns and demographic history of the A. ecalcarata complex through a series of phylogenetic, divergence time estimation, and demographic history analyses. The dry, cold climate and frequent climate oscillations that occurred during the early Pleistocene and the Mid‐Pleistocene transition led to the differentiation of the A. ecalcarata complex, which was isolated in various areas. Geographically, the A. ecalcarata complex can be divided into Eastern and Western Clades and five subclades, which conform to the divergence of the East Asian flora. Our results clearly show the impact of Quaternary climate and geography on evolutionary history at the population level. These findings promote the understanding of the relationship between plant genetic differentiation and climate and geographical factors of East Asia at the population level.

Citations (5)


... Clean data for each individual was mapped to our previously assembled chromosome-level reference genome of R. chrysanthemifolia (402.67 Mb; Zhang et al., 2024), respectively, using the Burrows-Wheeler Alignment-Maximal Exact Match module with default parameters in bwa-mem2 v2.21 (Vasimuddin et al., 2019). The mapping results were converted to BAM files using SAMtools v1.8.4 (Danecek et al., 2021). ...

Reference:

Population genomic analysis unravels the evolutionary processes leading to budding speciation
Two chromosome‐level genome assemblies of Rhodiola shed new light on genome evolution in rapid radiation and evolution of the biosynthetic pathway of salidroside

... (Thiede and Eggli 2007). Sinocrassula is monophyletic and sister to Kungia K.T.Fu, then these two genera are together sister to the clade comprised of Meterostachys Nakai, Orostachys Fisch., and Hylotelephium H.Ohba in Sempervivoideae (Gontcharova et al. 2006;Messerschmid et al. 2020;Liu et al. 2023). Sinocrassula is a small genus consisting of ca. 13 species, mainly distributed in South and East Asia, with few species extending to Southeast Asia (Fu and Ohba 2001;Wang et al. 2012Wang et al. , 2022Averyanov et al. 2014). ...

Plastomic data shed new light on the phylogeny, biogeography, and character evolution of the family Crassulaceae
  • Citing Article
  • July 2023

Journal of Systematics and Evolution

... Trifida Journal of Integrative Plant Biology individuals from 23 populations of R. chrysanthemifolia, 25 individuals from two populations of R. liciae, and 30 individuals from two populations of R. sinuata for wholegenome resequencing (WGR; Figure 1A; Table S1). Furthermore, we selected four individuals from other clades as outgroups based on Ren et al. (2023). Fresh leaves were dried in silica gel in the field and stored in −20°C for DNA extraction. ...

Genomic data provide a robust phylogeny backbone for Rhodiola L. (Crassulaceae) and reveal extensive reticulate evolution during its rapid radiation
  • Citing Article
  • June 2023

Molecular Phylogenetics and Evolution

... and Cimicifuga heracleifolia Kom., are referred as the official sources of Cimicifugae Rhizoma [3]. Except the above cultivars, Actaea purpurea [11], Actaea japonica, Cimicifuga simplex [12] black cohosh [13] and Actaea asiatica Hara [14] are often used as counterfeits or fake products regionally due to its similarity in the plant appearance and efficacy. Although the application of these products may be beneficial for obtaining materials locally and addressing resource shortages. ...

Nonadaptive molecular evolution of plastome during the speciation of Actaea purpurea and its relatives

... In this study, we found that the chloroplast genome of E. nitida contains 209 SSR sites, mainly single nucleotide repeats, with no C-type long repeats, and mainly polyA and polyT, which provides a basis for genetic analysis (Kuang et al. 2011). Chloroplast genome sequences can be used to infer phylogenetic relationships and determine species affinities (Xue et al. 2021). The present study supports that E. nitida is a member of Eurya Thunberg and obtains a high support rate; it also further finds its closest related species, E. hebeclados, and its sister branches. ...

Divergence in the Aquilegia ecalcarata complex is correlated with geography and climate oscillations: Evidence from plastid genome data