Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene family
© The Author(s). 2017
Received: 3 April 2017
Accepted: 24 July 2017
Published: 9 August 2017
Among the 13 families of early-diverging eudicots, only Circaeasteraceae (Ranunculales), which consists of the two monotypic genera Circaeaster and Kingdonia, lacks a published complete plastome sequence. In addition, the phylogenetic position of Circaeasteraceae as sister to Lardizabalaceae has only been weakly or moderately supported in previous studies using smaller data sets. Moreover, previous plastome studies have documented a number of novel structural rearrangements among early-divergent eudicots. Hence it is important to sequence plastomes from Circaeasteraceae to better understand plastome evolution in early-diverging eudicots and to further investigate the phylogenetic position of Circaeasteraceae.
Using an Illumina HiSeq 2000, complete plastomes were sequenced from both living members of Circaeasteraceae: Circaeaster agrestis and Kingdonia uniflora . Plastome structure and gene content were compared between these two plastomes, and with those of other early-diverging eudicot plastomes. Phylogenetic analysis of a 79-gene, 99-taxon data set including exemplars of all families of early-diverging eudicots was conducted to resolve the phylogenetic position of Circaeasteraceae.
Both plastomes possess the typical quadripartite structure of land plant plastomes. However, a large ~49 kb inversion and a small ~3.5 kb inversion were found in the large single-copy regions of both plastomes, while Circaeaster possesses a number of other rearrangements, particularly in the Inverted Repeat. In addition, infA was found to be a pseudogene and accD was found to be absent within Circaeaster, whereas all ndh genes, except for ndhE and ndhJ, were found to be either pseudogenized (ΨndhA, ΨndhB, ΨndhD, ΨndhH and ΨndhK) or absent (ndhC, ndhF, ndhI and ndhG) in Kingdonia. Circaeasteraceae was strongly supported as sister to Lardizabalaceae in phylogenetic analyses.
The first plastome sequencing of Circaeasteraceae resulted in the discovery of several unusual rearrangements and the loss of ndh genes, and confirms the sister relationship between Circaeasteraceae and Lardizabalaceae. This research provides new insight to characterize plastome structural evolution in early-diverging eudicots and to better understand relationships within Ranunculales.
The early-diverging eudicot family Circaeasteraceae (Ranunculales) sensu APG IV  contains only the two monotypic genera Circaeaster Maxim. and Kingdonia Balf.f. & W.W. Smith, which were historically treated as separate families (Circaeasteraceae and Kingdoniaceae) (e.g. [2–6]). Kingdonia has also been placed in Ranunculaceae in the past (e.g. [7–10]). Circaeaster agrestis Maxim. can be found in China and the Himalayas, whereas Kingdonia uniflora Balf.f. & W.W. Smith is endemic to China. Fossil fruits somewhat similar to those of Circaeaster have been reported from the mid-Albian of Virginia, USA [11, 12], while no fossil record is known for Kingdonia. Both species are herbs growing at high elevations, and possess the same distinctive dichotomous venation, which is very rare among angiosperms.
The Ranunculales sensu APG IV  form a well-supported clade comprised of seven families: Berberidaceae, Circaeasteraceae, Eupteleaceae, Lardizabalaceae, Menispermaceae, Papaveraceae and Ranunculaceae. To date, complete plastomes have been sequenced for representatives from all of these families except Circaeasteraceae [13–24]. These and plastomes from other eudicot families have helped to successfully resolve phylogenetic relationships among early-diverging eudicots, including among most families of Ranunculales (e.g.[17–19, 23, 24]). This is highly promising given that the relationships among many of these families had been poorly to moderately resolved in previous studies utilizing only a few genes (e.g. [25–38]). In previous phylogenetic studies of Ranunculales based on only a few genes, Circaeasteraceae has been resolved as sister to Lardizabalaceae, but only with weak or moderate support [25, 26, 29, 32, 36, 38, 39].
Over the past decade, knowledge of the organization and evolution of angiosperm plastomes has rapidly expanded [40, 41]. Plastomes of most flowering plants possess a typical quadripartite structure with two Inverted Repeat regions (IRA and IRB) separating the Small and Large Single-Copy regions (SSC and LSC) . Nevertheless, deviations from this canonical structure have been found with increasing frequency as the pace of plastome sequencing has exploded in recent years. For example, the length of the IR region has been found to vary significantly in some plant groups (e.g. [43–45]), and Sun et al.  documented six major “IR types” among 18 early-diverging eudicot plastomes, representing 12 of the 13 early-diverging eudicot families. Reconstruction of the ancestral IR gene content suggests that 18 genes were likely present in the IR region of the ancestor of eudicots , although representatives from Circaeasteraceae were absent from this study. Likewise, large inversions have been detected throughout the plastome in an increasing number of taxa (e.g. [46–50]). However, no obvious large inversions or rearrangements have been detected from early-diverging eudicot plastomes. Finally, gene loss (including pseudogenization) has also been found to be widespread among angiosperm plastomes, especially in species whose plastomes are highly rearranged .
To characterize plastome structural evolution in early-diverging eudicots and to better understand relationships within Ranunculales, we sequenced the complete plastomes of both extant species of Circaeasteraceae and included these two plastomes in a larger phylogenetic analysis including representatives of all major lineages of angiosperms. Consistent with previous work, we find that these complete plastome sequences improve support for phylogenetic relationships among Ranunculales, including the position of Circaeasteraceae. Moreover, we report several significant plastome structural changes, including a large inversion and several gene loss events.
Comparison of the plastid genomes of Circaeaster agrestis and Kingdonia uniflora
Total plastome length (bp)
IR length (bp)
SSC length (bp)
LSC length (bp)
ndhC, ndhF, ndhI, ndhG
ΨndhA, ΨndhB, ΨndhD, ΨndhH, ΨndhK
Overall G/C content (%)
Average depth of coverage
Number of plastid reads
Read length (bp)
Genes with one intron
trnK-UUU, trnG-UCC, trnL-UAA, trnV-UAC, trnI-GAU, trnA-UGC, petB, petD, atpF, ndhA, ndhB, rpl16, rpoC1, rps16
trnK-UUU, trnG-UCC, trnL-UAA, trnV-UAC, trnI-GAU, trnA-UGC, petB, petD, atpF, rpl16, rpoC1, rps16
Genes with two introns
rps12, clpP, ycf3
rps12, clpP, ycf3
GenBank accession number
Structure and gene content of the Circaeaster and Kingdonia plastomes
Overall, Circaeaster and Kingdonia were found to possess the typical gene and intron complement of angiosperms, with a few notable exceptions (Table 1). Both plastomes contain 30 tRNA genes and four rRNA genes, as is typical in angiosperms. The plastome of Circaeaster agrestis has 77 protein-coding genes and one pseudogene (ΨinfA, which is truncated to a length of 36 bp); accD is absent. The plastome of Kingdonia uniflora only has 70 protein-coding genes due to the loss or pseudogenization of nearly all ndh genes: four genes (ndhC, ndhF, ndhI and ndhG) were absent and five (ΨndhA, ΨndhB, ΨndhD, ΨndhH and ΨndhK) were identified as pseudogenes. More specifically, the second exon is absent from ΨndhA and ΨndhB, ΨndhD is severely truncated to 18 bp (vs. 1503 bp in Circaeaster), ΨndhH is truncated to 618 bp (vs. 1182 bp in Circaeaster) in length, and ΨndhK is only 237 bp (vs. 669 bp in Circaeaster) in length. The Ks values of these pseudogenes were calculated between Circaeaster and Kingdonia (Additional file 3). A total of 32 and 14 repeats ≥30 bp in length were found in the plastome of Circaeaster and Kingdonia, respectively (Additional files 4 and 5). For comparison, the number of repeats ≥30 bp in seven other Ranunculales species are as follows: (1) 17 in Akebia trifoliata (Thunb.) Koidz.; (2) 24 in Epimedium sagittatum (Sieb. & Zucc.) Maxim.; (3) 17 in Euptelea pleiosperma Hook.f. & Thomson; (4) 29 in Mahonia bealei (Fortune) Pynaert; (5) nine in Nandina domestica Thunb.; (6) nine in Papaver somniferum L.; and (7) eight in Stephania japonica (Thunb.) Miers (Additional file 6).
Plastome structure and gene content
The unusual structural rearrangements and gene losses (especially the loss of the ndh genes) detected in the two Circaeasteraceae plastomes represent the first reported among early-diverging eudicot plastomes, and hence shed important insight into the evolution of early eudicot plastomes. The fact that two of the observed inversions (the ~49 kb and ~3.5 kb inversions) are shared by Circaeaster and Kingdonia suggests that they predate the evolutionary split between these two genera. Although uncommon, relatively large inversions have been detected in a number of other angiosperm lineages and often serve as useful phylogenetic markers [50, 52–54]. Some of the best examples of relatively large inversions that are synapomorphies for clades of flowering plants include the 22.8 kb inversion shared by all Asteraceae except Barnadesioideae [53, 55], the 78 kb inversion shared by all Fabaceae subtribe Phaseolinae , and the 36 kb inversion present in all core genistoid legumes [50, 57]. Highly rearranged plastome structures also characterize a number of other angiosperm lineages, such as Campanulaceae, Geraniaceae, and the IR-lacking clade of Fabaceae, and these are associated with greatly elevated rates of molecular evolution and large numbers of short repeats . In some cases the endpoints of large plastome inversions have been found to be associated with short inverted repeats (sIRs), although we did not detect sIRs in association with the inversion endpoints in Circaeaster or Kingdonia.
The IR regions of Circaeaster and Kingdonia are also structurally unique among angiosperms, with several rearrangements. The most unusual of these involves the transposition of the ndhB, rps7 and 3′ end of the rps12 gene to a point near the junction of the IRB and the SSC region (Fig. 1). These three genes form a transcriptional operon  and this operon is not disrupted in Circaeaster, nor does its transposition interrupt adjacent operons. The IR/SSC endpoints themselves are also rearranged in Circaeaster, with rpl32 and trnL-UAG within the IR and non-adjacent to ndhF, unlike almost all other angiosperms . The IR boundaries of Kingdonia are also unusual for their expansion to include several genes that are normally in the SSC (e.g. ycf1, rps15), resulting in a much smaller and rearranged SSC (which is also influenced by the loss of ndh genes; see below). The exact sequence of rearrangements that could account for the unusual IR arrangements of Circaeasteraceae is clearly complicated and hence difficult to reconstruct. IR expansion and contraction is well-known in a number of other angiosperm lineages (e.g. ), including within early-diverging eudicots, which have been found to possess a number of expansions and contractions . Given the expansions and rearrangements observed in Circaeaster and Kingdonia, neither fit into any of the six IR types for early-diverging eudicots delineated in Sun et al. , and thus we designate two new early-diverging eudicot IR types for Circaeaster (type G) and Kingdonia (type H) (Fig. 1).
Usually, gene content is highly conserved among photosynthetic angiosperm plastomes [50, 60], but in Circaeasteraceae, a number of genes have been lost or pseudogenized, each of which has been found to be lost repeatedly across angiosperms. For example, the loss of accD in Circaeaster is mirrored in a number of other lineages where accD is pseudogenized or absent, e.g., grasses , Lobeliaceae , Campanulaceae [52, 63, 64], Acorus , Oleaceae , Pelargonium , and Lolium perenne . Likewise, infA is also known to be a pseudogene in numerous other angiosperms, including two Ranunculales (Ranunculus macranthus and Epimedium sagittatum) , tobacco , and numerous rosids . Whether accD or infA have been transferred to the nucleus in Circaeaster is unknown.
The loss or pseudogenization of nearly all ndh genes from Kingdonia has also been observed in a number of other land plants. The ndh genes encode subunits of the plastid NDH (NADH dehydrogenase-like) complex, which permits cyclic electron flow associated with Photosystem I and hence facilitates chlororespiration [71, 72]. Although the NDH complex is widely retained across land plants, it has been found to be dispensable under optimal growth conditions and the plastid ndh genes have been lost in a number of autotrophic and heterotrophic lineages [72, 73]. For example, the plastid ndh loci have been lost or pseudogenized en masse from parasitic plants such as Orobanchaceae and Cuscuta (Convolvulaceae) [74–76], from mycoheterotrophs including several orchids  and Petrosavia (Petrosaviaceae) , and from autotrophs including Gnetales, conifers, Najas (Hydrocharitaceae), Carnegiea (Cactaceae), and Erodium (Geraniaceae) [79–84]. It is not clear whether the ndh genes in Kingdonia have been transferred to the nucleus or whether their loss represents the complete loss of the NDH complex, but in any case Kingdonia is the only known early-diverging eudicot that has experienced ndh pseudogenization and loss.
Moreover, the loss of the ndh genes in Kingdonia accounts for the smaller overall size of the Kingdonia plastome and may have also played an indirect role in the expansion of the IR of Kingdonia. The complete loss of ndhF, which normally occupies a position immediately adjacent to the IRB/SSC boundary, may have led to instability of the IR/SSC boundaries, leading to rearrangements of the SSC and IR. This hypothesis is supported by other recent studies in orchids  and Najas flexilis  where ndhF loss is associated with shifts in the IR/SSC boundary.
Phylogeny of Ranunculales
The circumscription of Ranunculales was long controversial (e.g. [3, 4, 9, 10, 85, 86]), but molecular phylogenetics has clarified the delimitation of Ranunculales to Berberidaceae, Circaeasteraceae, Eupteleaceae, Lardizabalaceae, Menispermaceae, Papaveraceae, and Ranunculaceae [1, 5, 6, 26, 29, 31, 32, 36, 38]. While the expansion of Circaeasteraceae to include Kingdonia is accepted by a majority of taxonomists , the rank and position of Kingdonia have long been in dispute . The complete plastome sequence data strongly support the sister relationship between Kingdonia and Circaeaster, in concordance with previous molecular results [25, 26, 31, 32, 36, 38, 87]. The two inversions and the rare, open dichotomous leaf venation shared by these taxa are good synapomorphies that additionally support the placement of Circaeaster and Kingdonia in one family.
The plastomes of Circaeaster agrestis and Kingdonia uniflora provide the first reference genome sequences for Circaeasteraceae, which will enrich the sequence resources of plastomes in early-diverging eudicots. The unusual rearrangements including large inversions and unusual IR structure detected in the Circaeasteraceae plastomes will help us better characterize plastome structural evolution in early-diverging eudicots. Phylogenetic analyses of the 79-gene, 99-taxon data set confirmed the position of Circaeasteraceae in Ranunculales, with maximum support as sister to Lardizabalaceae. The two Circaeasteraceae plastomes will also be of benefit for further phylogenomic analyses within early-diverging eudicots.
Taxon sampling, chloroplast DNA isolation, high-throughput sequencing
Fresh leaves of Circaeaster agrestis were collected from Shennongjia, Hubei Province, China, in 2015, and from Kingdonia uniflora in Meixian, Shanxi Province, China, in 2016. Voucher specimens (Circaeaster agrestis: Y.X. Sun 1510; Kingdonia uniflora: Y.X. Sun 1606) were deposited at the Herbarium of Wuhan Botanical Garden, Chinese Academy of Sciences (HIB). For both species, high-quality chloroplast DNA was obtained following the plastid DNA extraction method of Shi et al. . The sequencing libraries were constructed and quantified following the methods introduced by Sun et al. . For both plastomes, a 500-bp DNA TruSeq Illumina (Illumina Inc., San Diego, CA, USA) sequencing library was constructed using 2.5–5.0 ng sonicated chloroplast DNA as input. Libraries were quantified using an Agilent 2100 Bioanalyzer (Agilent Technologies, Santa Clara, CA, USA) and by real-time quantitative PCR. Libraries were then multiplexed, and 2 × 125 bp sequencing was performed on an Illumina HiSeq 2000 platform at the Beijing Genomics Institute.
Plastome assembly, annotation, and structural analyses
Following Sun et al. , duplicate reads, adapter-contaminated reads, and reads with more than five Ns were filtered out. Remaining, high-quality reads were assembled into contigs with a minimum length of 1000 bp using CLC Genomics Workbench with default parameters, except for a word size value of 60.
Plastomes were annotated using DOGMA  and through comparison with the sequences of published early-diverging eudicot plastomes. Physical maps were drawn using GenomeVx , followed by subsequent manual editing with Adobe Illustrator CS5. Boundaries for tRNAs were identified with tRNAscan-SE 1.21  and confirmed by comparison with available early-diverging eudicot plastome sequences. The finished genomes were deposited in GenBank (Table 1).
To investigate plastome structural evolution, whole plastome alignment between Circaeasteraceae and representatives of other early-diverging eudicot families was performed with ProgressiveMauve v 2.4.0 , including only one copy of the IR (IRB), and locally collinear blocks (LCBs) were identified. Because the 18 reported early-diverging eudicot plastomes in Sun et al.  share the same gene order, and because Circaeasteraceae was resolved as sister to Akebia in present research, the Akebia plastome was used as the reference sequence for ProgressiveMauve comparisons. mVISTA  was employed to generate sequence identity plots. The number and location of repeat elements in the plastomes of Circaeaster and Kingdonia as well as seven other Ranunculales species (Akebia trifoliata, Epimedium sagittatum, Euptelea pleiosperma, Berberis bealei, Nandina domestica, Papaver somniferum and Stephania japonica) were determined by REPuter , with a minimum size of 30 bp and a Hamming distance of 1. Before performing the analysis, one copy of the IR was removed.
All protein-coding regions were extracted from the plastomes of Circaeaster and Kingdonia. These sequences were then added manually to the 97-taxon alignment of Sun et al. , resulting in a data set with complete coverage of early-diverging eudicot families sensu APG IV . GenBank information for all plastomes used for present phylogenetic analyses can be found in Additional file 8. Regions of ambiguous alignment and sites with more than 80% missing data were excluded from the alignment.
Maximum likelihood (ML) analyses were conducted using RAxML version 7.4.2 , under the general time-reversible (GTR) substitution model and the Γ model of rate heterogeneity. We conducted both unpartitioned and partitioned analyses. PartitionFinder version 1.1.1  was used to select the best-fit partitioning scheme, considering all 237 possible gene-by-codon position partitions (79 genes × 3 codon positions). For both ML analyses, a single set of branch lengths for all partitions was used. Ten independent ML searches were conducted and bootstrap support was estimated with 1000 bootstrap replicates.
The authors would like to thank Gen-lu Bai for helping with collecting plant materials.
This work was supported by the National Natural Science Foundation of China (31600176, 31370242 and 31370223), and NSTIPC (2013FY111200) and SPRPCAS (XDA13020500).
Availability of data and materials
All sequences used in this study are available from the National Center for Biotechnology Information (NCBI) (see Additional file 8). Additionally, two plastomes sequenced in this study have been deposited in the NCBI genome database (Accession numbers: see Methods).
YS, HW and JL conceived and designed the study. YS performed de novo assembly, genome annotation, phylogenetic and other analyses. YS and MM drafted the manuscript. YS, NL and AK performed the experiments. AM, LY and SJ collected the leaf materials. All authors read and approved the final manuscript.
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