Open Access

Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene family

  • Yanxia Sun1,
  • Michael J. Moore2,
  • Nan Lin1, 3,
  • Kole F. Adelalu1, 3,
  • Aiping Meng1,
  • Shuguang Jian4,
  • Linsen Yang5,
  • Jianqiang Li1Email author and
  • Hengchang Wang1Email author
BMC Genomics201718:592

https://doi.org/10.1186/s12864-017-3956-3

Received: 3 April 2017

Accepted: 24 July 2017

Published: 9 August 2017

Abstract

Background

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.

Results

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.

Conclusion

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.

Keywords

Early-diverging eudicots Circaeasteraceae Plastome Rearrangements Gene loss Phylogenetic analyses

Background

The early-diverging eudicot family Circaeasteraceae (Ranunculales) sensu APG IV [1] 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. [26]). Kingdonia has also been placed in Ranunculaceae in the past (e.g. [710]). 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 [1] 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 [1324]. 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.[1719, 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. [2538]). 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) [42]. 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. [4345]), and Sun et al. [23] 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 [23], 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. [4650]). 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 [51].

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.

Results

Plastome assemblies

Illumina paired-end sequencing produced 474,002 and 1,092,236 raw reads for Circaeaster and Kingdonia, respectively. The mean coverage of the plastome was 392.3× for Circaeaster, and 926.4× for Kingdonia. For both Circaeaster and Kingdonia, assembly yielded a single scaffold comprising the entire plastome sequence. Junction regions between the IR and Single-Copy regions were confirmed by PCR and Sanger sequencing (C8-C11 and K5-K8 in Additional file 1). Assembly statistics are presented in Table 1.
Table 1

Comparison of the plastid genomes of Circaeaster agrestis and Kingdonia uniflora

 

Circaeaster agrestis

Kingdonia uniflora

Total plastome length (bp)

151,033

147,378

IR length (bp)

28,023

30,916

SSC length (bp)

16,857

4857

LSC length (bp)

78,130

80,689

Absent genes

accD

ndhC, ndhF, ndhI, ndhG

Pseudogenes

ΨinfA

ΨndhA, ΨndhB, ΨndhD, ΨndhH, ΨndhK

Overall G/C content (%)

38.2

37.8

Average depth of coverage

392.3×

926.4×

Number of plastid reads

474,002

1,092,236

Read length (bp)

125

125

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

KY908400

KY908401

Structure and gene content of the Circaeaster and Kingdonia plastomes

The plastome size of Circaeaster agrestis is 151,033 bp and that of Kingdonia uniflora is 147,378 bp (Fig. 1). Both plastomes possess the typical quadripartite structure of angiosperms, although both also contain several remarkable structural rearrangements. Most notably, a large ~49 kb inversion in the LSC region, including all genes from trnQ-UUG to rbcL/accD (accD is absent from Circaeaster) is present in both plastomes (Figs. 1, 2). In addition, both plastomes also share a much smaller inversion (~3.5 kb) involving all four genes from atpB to trnV-UAC (Figs. 1, 2). Circaeaster also possesses a number of other unique structural changes, including a ~ 3.5 kb inversion involving all four genes from psaI to petA (Figs. 1, 2) and a highly unusual IR structure. Specifically, the following changes have occurred within the IR of Circaeaster: (1) ndhB, rps7, and the 3′ end of rps12 have shifted to a position between trnN-GUU and ycf1 (compared to their typical positions between trnL-CAA and trnV-GAC in nearly all other angiosperms); (2) rpl32 and trnL-UAG are within the IR (rather than in the SSC region as in nearly all other angiosperms), and (3) ycf1 is almost entirely outside the IR (rather than having ~1000 bp of ycf1 within the IR, as is more typical of angiosperms). Within Kingdonia, the IR/SSC boundary has shifted to include all of ycf1, rps15, ΨndhH, and ΨndhA. In both plastomes, there are unusual arrangements of rpl32 and trnL-UAG, which in almost all other angiosperms are found adjacent to each other on the same strand within the SSC. The endpoints of these inversions were confirmed in both plastomes via PCR and Sanger sequencing using custom-designed primers (Additional files 1 and 2).
Fig. 1

Plastome maps of Circaeaster agrestis and Kingdonia uniflora. IR, inverted repeat; LSC, large single-copy region; SSC, small single-copy region; Inv1, large inversion 1; Inv2, large inversion 2; Inv3, large inversion 3. The IR rearrangement is also indicated

Fig. 2

ProgressiveMauve alignment among Akebia, Circaeaster and Kingdonia showing the structural rearrangements in Circaeaster and Kingdonia. Colored blocks represent locally collinear blocks (LCBs) and are connected by lines to similarly colored LCBs, indicating homology

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).

Phylogenetic analyses

The final 79-gene, 99-taxon alignment used for ML analyses was 62,238 bp in length after character exclusion. The best partitioning scheme identified under the Bayesian information criteria (BIC) using relaxed clustering analysis in PartitionFinder (ln L = −1,173,388.00241; BIC 2353123.26941) contained 35 partitions. The tree with the highest ML score (ln L = −1,178,285.119460) produced by the 35-partition ML analysis (Fig. 3) shared an identical topology with the best tree from unpartitioned analysis (ln L = −1,200,753.541175) (Additional file 7), except for the relationships among Trochodendrales, Buxales and Gunneridae. The 35-partition analysis supported the sister relationship between Buxales and Gunneridae, but the support value was low (52%); while the unpartitioned analysis strongly supported the sister relationship between Trochodendrales and Gunneridae. Within Ranunculales, Eupteleaceae was found to be the earliest-diverging lineage, and Papaveraceae was sister to the clade comprised of Berberidaceae, Ranunculaceae, Menispermaceae, Lardizabalaceae and Circaeasteraceae. Lardizabalaceae and Circaeasteraceae formed a strongly supported clade that was sister to the clade of Berberidaceae, Ranunculaceae and Menispermaceae.
Fig. 3

Phylogram of the best tree determined by RAxML for the 79-gene, 99-taxon data set using the 35-partition scheme recovered as optimal by PartitionFinder. Numbers associated with branches are ML bootstrap support values. Branches with no bootstrap values listed have 100% bootstrap support

Discussion

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, 5254]. 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 [56], 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 [58]. 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 [59] 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 [54]. 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. [45]), including within early-diverging eudicots, which have been found to possess a number of expansions and contractions [23]. 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. [23], 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 [61], Lobeliaceae [62], Campanulaceae [52, 63, 64], Acorus [65], Oleaceae [66], Pelargonium [67], and Lolium perenne [68]. Likewise, infA is also known to be a pseudogene in numerous other angiosperms, including two Ranunculales (Ranunculus macranthus and Epimedium sagittatum) [23], tobacco [69], and numerous rosids [70]. 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) [7476], from mycoheterotrophs including several orchids [77] and Petrosavia (Petrosaviaceae) [78], and from autotrophs including Gnetales, conifers, Najas (Hydrocharitaceae), Carnegiea (Cactaceae), and Erodium (Geraniaceae) [7984]. 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 [77] and Najas flexilis [82] 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 [1], the rank and position of Kingdonia have long been in dispute [38]. 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.

Conclusions

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.

Methods

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. [88]. The sequencing libraries were constructed and quantified following the methods introduced by Sun et al. [23]. 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. [23], 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 [89] and through comparison with the sequences of published early-diverging eudicot plastomes. Physical maps were drawn using GenomeVx [90], followed by subsequent manual editing with Adobe Illustrator CS5. Boundaries for tRNAs were identified with tRNAscan-SE 1.21 [91] 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 [92], 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. [23] 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 [93] 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 [94], with a minimum size of 30 bp and a Hamming distance of 1. Before performing the analysis, one copy of the IR was removed.

Phylogenetic analyses

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. [23], resulting in a data set with complete coverage of early-diverging eudicot families sensu APG IV [1]. 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 [95], 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 [96] 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.

Declarations

Acknowledgments

The authors would like to thank Gen-lu Bai for helping with collecting plant materials.

Funding

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).

Authors’ contributions

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.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences
(2)
Department of Biology, Oberlin College
(3)
University of Chinese Academy of Sciences
(4)
South China Botanical Garden, Chinese Academy of Sciences
(5)
Hubei Key Laboratory of Shennongjia Golden Monkey Conservation Biology, Administration of Shennongjia National Park

References

  1. Angiosperm Phylogeny Group. An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc. 2016;181:1–20.View ArticleGoogle Scholar
  2. Dahlgren G. A revised system of classification of the angiosperms. Bot J Linn Soc. 1980;80:91–124.View ArticleGoogle Scholar
  3. Dahlgren R. General aspects of angiosperm evolution and macro-systematics. Nord J Bot. 1983;3:119–49.View ArticleGoogle Scholar
  4. Takhtajan A. Diversity and classification of flowering plants. New York: Columbia University Press; 1997.Google Scholar
  5. Angiosperm Phylogeny Group. An ordinal classification for the families of flowering plants. Ann Mo Bot Gard. 1998;85:531–53.View ArticleGoogle Scholar
  6. Angiosperm Phylogeny Group. An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG II. Bot J Linn Soc. 2003;141:399–436.View ArticleGoogle Scholar
  7. Hutchinson J. The families of flowering plants arranged according to a new system based on their probable phylogeny. Oxford: Clarendon Press; 1973.Google Scholar
  8. Thorne RF. Classification and geography of the flowering plants. Bot Rev. 1992;58:225–348.View ArticleGoogle Scholar
  9. Kubitzki K, Rohwer JC, Bittrich V. The families and genera of vascular plants II. Berlin: Springer; 1973.Google Scholar
  10. Wu ZY, Lu AM, Tang YC, Chen ZD, Li DZ. Synopsis of a new “polyphyletic–polychronic–polytopic” system of the angiosperms. Acta Phytotaxon Sin. 2002;40:289–322.Google Scholar
  11. Crane PR, Friis EM, Pedersen KR. Paleobotanical evidence on the early radiation of magnoliid angiosperms. Plant Syst Evol [Supplement l]. 1994;8:51–72.Google Scholar
  12. Drinnan AN, Crane PR, Hoot SB. Patterns of floral evolution in the early diversification of non-magnoliid dicotyledons (eudicots). Plant Syst Evol [Supplement 8]. 1994;8:93–122.Google Scholar
  13. Moore MJ, Dhingra A, Soltis PS, Shaw R, Farmerie WG, Folta KM, Soltis DE. Rapid and accurate pyrosequencing of angiosperm plastid genomes. BMC Plant Biol. 2006;6:17.View ArticlePubMedPubMed CentralGoogle Scholar
  14. Hansen DR, Dastidar SG, Cai ZQ, Penaflor C, Kuehl JV, Boore JL, Jansen RK. Phylogenetic and evolutionary implications of complete chloroplast genome sequences of four early-diverging angiosperms: Buxus (Buxaceae), Chloranthus (Chloranthaceae), Dioscorea (Dioscoreaceae), and Illicium (Schisandraceae). Mol Phylogenet Evol. 2007;45:547–63.View ArticlePubMedGoogle Scholar
  15. Raubeson LA, Peery R, Chumley TW, Dziubek C, Fourcade HM, Boore JL, Jansen RK. Comparative chloroplast genomics: analyses including new sequences from the angiosperms Nuphar advena and Ranunculus macranthus. BMC Genomics. 2007;8:174.View ArticlePubMedPubMed CentralGoogle Scholar
  16. Kim YK, Park CW, Kim KJ. Complete chloroplast DNA sequence from a Korean endemic genus, Megaleranthis saniculifolia, and its evolutionary implications. Mol Cells. 2009;27:365–81.View ArticlePubMedGoogle Scholar
  17. Ma J, Yang BX, Zhu W, Sun LL, Tian JK, Wang X. The complete chloroplast genome sequence of Mahonia bealei (Berberidaceae) reveals a significant expansion of the inverted repeat and phylogenetic relationship with other angiosperms. Gene. 2013;528:120–31.View ArticlePubMedGoogle Scholar
  18. Sun YX, Moore MJ, Meng AP, Soltis PS, Soltis DE, Li JQ, Wang HC. Complete plastid genome sequencing of Trochodendraceae reveals a significant expansion of the inverted repeat and suggests a Paleogene divergence between the two extant species. PLoS One. 2013;8:e60429.View ArticlePubMedPubMed CentralGoogle Scholar
  19. Nock CJ, Baten A, King GJ. Complete chloroplast genome of Macadamia integrifolia confirms the position of the Gondwanan early-diverging eudicot family Proteaceae. BMC Genomics. 2014;15:S13.View ArticlePubMedPubMed CentralGoogle Scholar
  20. Wu ZH, Gui ST, Quan ZW, Pan L, Wang SZ, Ke WD, Liang DQ, Ding Y. A precise chloroplast genome of Nelumbo nucifera (Nelumbonaceae) evaluated with sanger, Illumina MiSeq, and PacBio RS II sequencing platforms: insight into the plastid evolution of early-diverging eudicots. BMC Plant Biol. 2014;14:289.View ArticlePubMedPubMed CentralGoogle Scholar
  21. Lim C, Kim G, Baek S, Han S, Yu H, Mun J. The complete chloroplast genome of Aconitum chiisanense Nakai (Ranunculaceae). Mitochondr DNA. 2015;28:1–2.Google Scholar
  22. Park S, Jansen R, Park S. Complete plastome sequence of Thalictrum coreanum (Ranunculaceae) and transfer of the rpl32 gene to the nucleus in the ancestor of the subfamily Thalictroideae. BMC Plant Biol. 2015;15:40.View ArticlePubMedPubMed CentralGoogle Scholar
  23. Sun YX, Moore MJ, Zhang SJ, Soltis PS, Soltis DE, Zhao TT, Meng AP, Li XD, Li JQ, Wang HC. Phylogenomic and structural analyses of 18 complete plastomes across nearly all families of early-diverging eudicots, including an angiosperm-wide analysis of IR gene content evolution. Mol Phylogenet Evol. 2016;96:93–101.View ArticlePubMedGoogle Scholar
  24. Zhang Y, Du L, Liu A, Chen J, Wu L, Hu W, Zhang W, Kim K, Lee S, Yang T, Wang Y. The complete chloroplast genome sequences of five Epimedium species: lights into phylogenetic and taxonomic analyses. Front Plant Sci. 2016;7:306.PubMedPubMed CentralGoogle Scholar
  25. Hoot SB, Crane PR. Interfamilial relationships in the Ranunculidae based on molecular systematics. Plant Syst Evol (Suppl.). 1995;9:119–31.Google Scholar
  26. Hoot SB, Magallón S, Crane PR. Phylogeny of basal eudicots based on three molecular data sets: atpB, rbcL, and 18S nuclear ribosomal DNA sequences. Ann Mo Bot Gard. 1999;86:1–32.View ArticleGoogle Scholar
  27. Qiu YL, Dombrovska O, Lee J, Li L, Whitlock BA, Bernasconi-Quadroni F, Rest JS, Davis CC, Borsch T, Hilu KW, Renner SS, Soltis DE, Soltis PS, Zanis MJ, Cannone JJ, Gutell RR, Powell M, Savolainen V, Chatrou LW, Chase MW. Phylogenetic analysis of basal angiosperms based on nine plastid, mitochondrial, and nuclear genes. Int J Plant Sci. 2005;166:815–42.View ArticleGoogle Scholar
  28. Qiu YL, Li L, Hendry TA, Li R, Taylor DW, Issa MJ, Ronen AJ, Vekaria ML, White AM. Reconstructing the basal angiosperm phylogeny: evaluating information content of the mitochondrial genes. Taxon. 2006;55:837–56.View ArticleGoogle Scholar
  29. Savolainen V, Fay MF, Albach DC, Backlund A, van der Bank M, Cameron KM, Johnson SA, Lledó MD, Pintaud JC, Powell M, Sheanan MC, Soltis PS, Soltis DE, Weston P, Whitten WM, Wurdack KJ, Chase MW. Phylogeny of the eudicots: a nearly complete familial analysis based on rbcL gene sequences. Kew Bull. 2000a;55:257–309.View ArticleGoogle Scholar
  30. Savolainen V, Chase MW, Hoot SB, Morton CM, Soltis DE, Bayer C, Fay MF, De Brujin A, Sullivan S, Qiu YL. Phylogenetics of flowering plants based upon a combined analysis of plastid atpB and rbcL gene sequences. Syst Biol. 2000b;49:306–62.View ArticlePubMedGoogle Scholar
  31. Soltis DE, Soltis PS, Chase MW, Mort ME, Albach DC, Zanis M, Savolainen V, Hahn WH, Hoot SB, Fay MF, Axtell M, Swensen SM, Nixon KC, Farris JS. Angiosperm phylogeny inferred from a combined data set of 18S rDNA, rbcL, and atpB sequences. Bot J Linn Soc. 2000;133:381–461.View ArticleGoogle Scholar
  32. Soltis DE, Senters AE, Zanis MJ. Kim S, Thompson JD, Soltis PS, Ronse de Craene LP, Endress PK, Farris JS. Gunnerales are sister to other core eudicots: implications for the evolution of pentamery. Am J Bot. 2003;90:461–70.View ArticlePubMedGoogle Scholar
  33. Nickrent DL, Blarer A, Qiu YL, Soltis DE, Soltis PS, Zanis M. Molecular data place Hydnoraceae with Aristolochiaceae. Am J Bot. 2002;89:1809–17.View ArticlePubMedGoogle Scholar
  34. Hilu KW, Borsch T, Müller K, Soltis DE, Soltis PS, Savolainen V, Chase MW, Powell MP, Alice LA, Evans R, Sauquet H, Neinhuis C, Slotta TAB, Rohwer JG, Campbell CS, Chatrou LW. Angiosperm phylogeny based on matK sequence information. Am J Bot. 2003;90:1758–76.View ArticlePubMedGoogle Scholar
  35. Zanis MJ, Soltis PS, Qiu YL, Zimmer E, Soltis DE. Phylogenetic analyses and perianth evolution in basal angiosperms. Ann Mo Bot Gard. 2003;90:129–50.View ArticleGoogle Scholar
  36. Kim S, Soltis DE, Soltis PS, Zanis MJ, Suh Y. Phylogenetic relationships among early-diverging eudicots based on four genes: were the eudicots ancestrally woody? Mol Phylogenet Evol. 2004a;31:16–30.View ArticlePubMedGoogle Scholar
  37. Worberg A, Quandt D, Barnikse AM, Löhne C, Hilu KW, Borsch T. Towards understanding early eudicot diversification: insights from rapidly evolving and non-coding DNA. Org Divers Evol. 2007;7:55–77.View ArticleGoogle Scholar
  38. Wang W, Lu A, Ren Y, Endress ME, Chen Z. Phylogeny and classification of Ranunculales: evidence from four molecular loci and morphological data. Perspect Plant Ecol. 2009;11:81–110.View ArticleGoogle Scholar
  39. Soltis DE, Smith SA, Cellinese N, Wurdack KJ, Tank DC, Brockington SF, Refulio-Rodriguez NF, Walker JB, Moore MJ, Carlsward BS, Bell CD, Latvis M, Crawley S, Black C, Diouf D, Xi Z, Rushworth CA, Gitzendanner MA, Sytsma KJ, Qiu YL, Hilu KW, Davis CC, Sanderson MJ, Beaman RS, Olmstead RG, Judd WS, Donoghue MJ, Soltis PS. Angiosperm phylogeny: 17 genes, 640 taxa. Am J Bot. 2011;98:704–30.View ArticlePubMedGoogle Scholar
  40. Ruhlman TA, Jansen RK. The plastid genomes of flowering plants. Methods Mol Biol. 2014;1132:3–38.View ArticlePubMedGoogle Scholar
  41. Daniell H, Lin CS, Yu M, Chang WJ. Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol. 2016;17:134.View ArticlePubMedPubMed CentralGoogle Scholar
  42. Palmer JD, Stein DB. Conservation of chloroplast genome structure among vascular plants. Curr Genet. 1986;10:823–33.View ArticleGoogle Scholar
  43. Goulding SE, Olmstead RG, Morden CW, Wolfe KH. Ebb and flow of the chloroplast inverted repeat. Mol Gen Genet. 1996;252:195–206.View ArticlePubMedGoogle Scholar
  44. Plunkett GM, Downie SR. Expansion and contraction of the chloroplast inverted repeat in Apiaceae subfamily Apioideae. Syst Bot. 2000;25:648–67.View ArticleGoogle Scholar
  45. Downie SR, Jansen RK. A comparative analysis of whole plastid genomes from the Apiales: expansion and contraction of the inverted repeat, mitochondrial to plastid transfer of DNA, and identification of highly divergent noncoding regions. Syst Bot. 2015;40:336–51.View ArticleGoogle Scholar
  46. Palmer JD, Herbon LA. Plant mitochondrial-DNA evolves rapidly in structure, but slowly in sequence. J Mol Evol. 1988;28:87–97.View ArticleGoogle Scholar
  47. Perry AS, Brennan S, Murphy DJ, Kavanagh TA, Wolfe KH. Evolutionary re-organisation of a large operon in adzuki bean chloroplast DNA caused by inverted repeat movement. DNA Res. 2002;9:157–62.View ArticlePubMedGoogle Scholar
  48. Magee AM, Aspinall S, Rice DW, Cusack BP, Sémon M, Perry AS, Stefanović S, Milbourne D, Barth S, Palmer JD, Gray JC, Kavanagh TA, Wolfe KH. Localized hypermutation and associated gene losses in legume chloroplast genomes. Genome Res. 2010;20:1700–10.View ArticlePubMedPubMed CentralGoogle Scholar
  49. Tangphatsornruang S, Sangsrakru D, Chanprasert J, Uthaipaisanwong P, Yoocha T, Jomchai N, Tragoonrung S. The chloroplast genome sequence of mungbean (Vigna radiata) determined by highthroughput pyrosequencing: structural organization and phylogenetic relationships. DNA Res. 2010;17:11–22.View ArticlePubMedGoogle Scholar
  50. Martin E, Rousseau-Gueutin M, Cordonnier S, Lima O, Michon-Coudouel S, Naquin D, de Carvalho JF, Malika A, Salmon A, Aïnouche A. The first complete chloroplast genome of the Genistoid legume Lupinus luteus: evidence for a novel major lineage-specific rearrangement and new insights regarding plastome evolution in the legume family Guillaume. Ann Bot. 2014;113:1197–210.View ArticlePubMedPubMed CentralGoogle Scholar
  51. Jansen RK, Cai Z, Raubeson LA, Daniell H, Depamphilis CW, Leebens-Mack J, Müller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee S, Peery R, JR MN, Kuehl JV, Boore JL. Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. P Natl Acad Sci USA. 2007;104:19369–74.View ArticleGoogle Scholar
  52. Cosner ME, Raubeson LA, Jansen RK. Chloroplast DNA rearrangements in Campanulaceae: phylogenetic utility of highly rearranged genomes. BMC Evol Biol. 2004;4:27.View ArticlePubMedPubMed CentralGoogle Scholar
  53. Kim KJ, Choi KS, Jansen RK. Two chloroplast DNA inversions originated simultaneously during the early evolution of the sunflower family (Asteraceae). Mol Biol Evol. 2005;22:1783–92.View ArticlePubMedGoogle Scholar
  54. Raubeson LA, Jansen RK. Chloroplast genomes of plants. In: Henry R, editor. Diversity and evolution of plants-genotypic variation in higher plants. Oxfordshire: CABI Publishing; 2005. p. 45–68.View ArticleGoogle Scholar
  55. Jansen RK, Palmer JD. A chloroplast DNA inversion marks an ancient evolutionary split in the sunflower family (Asteraceae). P Natl Acad Sci USA. 1987;84:5818–22.View ArticleGoogle Scholar
  56. Bruneau A, Doyle JJ, Palmer JD. A chloroplast DNA structural mutation as a subtribal character in the Phaseoleae (Leguminosae). Syst Bot. 1990;15:378–86.View ArticleGoogle Scholar
  57. Crisp M, Gilmore S, van Wyk B. Molecular phylogeny of the Genistoid tribes of Papilionoid legumes. London: Royal Botanic Gardens, Kew; 2000.Google Scholar
  58. Jansen RK, Ruhlman TA. Plastid genomes of seed plants. In: Bock R, Knoop V, editors. Genomics of chloroplast and mitochondria. New York: Springer; 2012. p. 103–26.View ArticleGoogle Scholar
  59. Woodbury NW, Roberts LL, Palmer JD, Thompson WF. A transcription map of the pea chloroplast genome. Curr Genet. 1988;14:75–89.View ArticleGoogle Scholar
  60. Timmis JN, Ayliffe MA, Huang CY, Martin W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet. 2004;5:123–35.View ArticlePubMedGoogle Scholar
  61. Katayama H, Ogihara Y. Phylogenetic affinities of the grasses to other monocots as revealed by molecular analysis of chloroplast DNA. Curr Genet. 1996;29:5.View ArticleGoogle Scholar
  62. Knox EB, Palmer JD. The chloroplast genome arrangement of lobelia thuliniana lobeliaceae: expansion of the inverted repeat in an ancestor of the campanulales. Plant Syst Evol. 1999;214:49–64.View ArticleGoogle Scholar
  63. Cosner ME, Jansen RK, Palmer JD, Downie SR. The highly rearranged chloroplast genome of Trachelium caeruleum (Campanulaceae): multiple inversions, inverted repeat expansion and contraction, transposition, insertions/deletions, and several repeat families. Curr Genet. 1997;31:419–29.View ArticlePubMedGoogle Scholar
  64. Haberle RC, Fourcade HM, Boore JL, Jansen RK. Extensive rearrangements in the chloroplast genome of Trachelium caeruleum are associated with repeats and tRNA genes. J Mol Evol. 2008;66:350–61.View ArticlePubMedGoogle Scholar
  65. Goremykin VV, Holland B, Hirsch-Ernst KI, Hellwig FH. Analysis of Acorus Calamus chloroplast genome and its phylogenetic implications. Mol Biol Evol. 2005;22:1813–22.View ArticlePubMedGoogle Scholar
  66. Lee H, Jansen RK, Chumley TW, Kim K. Gene relocations within chloroplast genomes of Jasminum and Menodora (Oleaceae) are due to multiple, overlapping inversions. Mol Biol Evol. 2007;24:1161–80.View ArticlePubMedGoogle Scholar
  67. Chumley TW, Palmer JD, Mower JP, Matthew Fourcade H, Calie PJ, Boore J, Jansen RK. The complete chloroplast genome sequence of Pelargonium x hortorum: organization and evolution of the largest and most highly rearranged chloroplast genome of land plants. Mol Biol Evol. 2006;23:2175–90.View ArticlePubMedGoogle Scholar
  68. Diekmann K, Hodkinson TR, Wolfe KH, van den Bekerom R, Dix P, Barth S. Complete chloroplast genome sequence of a major allogamous forage species, perennial ryegrass (Lolium perenne L.). DNA Res. 2009;16:165–76.View ArticlePubMedPubMed CentralGoogle Scholar
  69. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayshida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 1986;5:2043–9.PubMedPubMed CentralGoogle Scholar
  70. Millen RS, Olmstead RG, Adams KL, Palmer JD, Lao NT, Heggie L, Kavanagh TA, Hibberd JM, Gray JC, Morden CW, Calie PJ, Jermiin LS, Wolfe KH. Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell. 2001;13:645–58.View ArticlePubMedPubMed CentralGoogle Scholar
  71. Martin M, Sabater B. Plastid ndh genes in plant evolution. Plant Physiol Bioch. 2010;48:636–45.View ArticleGoogle Scholar
  72. Ruhlman TA, Chang WJ, Chen JJW, Huang YT, Chan MT, Zhang J, Liao DC, Blazier JC, Jin X, Shih MC, Jansen RK, Lin CS. NDH expression marks major transitions in plant evolution and reveals coordinate intracellular gene loss. BMC Plant Biol. 2015;15:100.View ArticlePubMedPubMed CentralGoogle Scholar
  73. Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ. Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J. 1998;17:868–76.View ArticlePubMedPubMed CentralGoogle Scholar
  74. Funk HT, Berg S, Krupinska K, Maier UG, Krause K. Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol. 2007;7:45.View ArticlePubMedPubMed CentralGoogle Scholar
  75. Haberhausen G, Zetsche K. Functional loss of all ndh genes in an otherwise relatively unaltered plastid genome of the holoparasitic flowering plant Cuscuta reflexa. Plant Mol Biol. 1994;24:217–22.View ArticlePubMedGoogle Scholar
  76. Wolfe KH, Morden CW, Palmer JD. Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. P Natl Acad Sci USA. 1992;89:10648–52.View ArticleGoogle Scholar
  77. Kim HT, Kim JS, Moore MJ, Neubig KM, Williams NH, Whitten WM, Kim JH. Seven new complete plastome sequences reveal rampant independent loss of the ndh gene family across orchids and associated instability of the inverted repeat/small single-copy region boundaries. PLoS One. 2015;10:e0142215.View ArticlePubMedPubMed CentralGoogle Scholar
  78. Logacheva MD, Schelkunov MI, Nuraliev MS, Samigullin TH, Penin AA. The plastid genome of mycoheterotrophic monocot Petrosavia stellaris exhibits both gene losses and multiple rearrangements. Genome Biol Evol. 2014;6:238–46.View ArticlePubMedPubMed CentralGoogle Scholar
  79. Blazier J, Guisinger MM, Jansen RK. Recent loss of plastid-encoded ndh genes within Erodium (Geraniaceae). Plant Mol Biol. 2011;76:263–72.View ArticleGoogle Scholar
  80. Braukmann TWA, Kuzmina M, Stefanovic S. Loss of all plastid ndh genes in Gnetales and conifers: extent and evolutionary significance for the seed plant phylogeny. Curr Genet. 2009;55:323–37.View ArticlePubMedGoogle Scholar
  81. McCoy SR, Kuehl JV, Boore JL, Raubeson LA. The complete plastid genome sequence of Welwitschia mirabilis: an unusually compact plastome with accelerated divergence rates. BMC Evol Biol. 2008;8:130.View ArticlePubMedPubMed CentralGoogle Scholar
  82. Peredo EL, King UM, Les DH. The plastid genome of Najas flexilis: adaptation to submersed environments is accompanied by the complete loss of the NDH complex in an aquatic angiosperm. PLoS One. 2013;8:e68591.View ArticlePubMedPubMed CentralGoogle Scholar
  83. Sanderson MJ, Copetti D, Búrquez A, Bustamante E, Charboneau JLM, Eguiarte LE, Kumar S, Lee HO, Lee J, McMahon M, Steele K, Wing R, Yang TJ, Zwickl D, Wojciechowski MF. Exceptional reduction of the plastid genome of saguaro cactus (Carnegiea gigantea): loss of the ndh gene suite and inverted repeat. Am J Bot. 2015;102:1115–27.View ArticlePubMedGoogle Scholar
  84. Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiura M. Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. P Natl Acad Sci USA. 1994;91:9794–8.View ArticleGoogle Scholar
  85. Cronquist A. The evolution and classification of flowering plants. second ed. New York: New York Botanical Garden; 1988.Google Scholar
  86. Thorne RF. An updated classification of the class Magnoliopsida (“Angiospermae”). Bot Rev. 2007;73:67–182.View ArticleGoogle Scholar
  87. Oxelman B, Lidén M. The position of Circaeaster – evidence from nuclear ribosomal DNA. Plant Syst Evol (Suppl). 1995;9:189–93.Google Scholar
  88. Shi C, Hu N, Huang H, Gao J, Zhao Y, Gao L. An improved chloroplast DNA extraction procedure for whole plastid genome sequencing. PLoS One. 2012;7:e31468.View ArticlePubMedPubMed CentralGoogle Scholar
  89. Wyman SK, Jansen RK, Boore JL. Automatic annotation of organellar genomes with DOGMA. Bioinformatics. 2004;20:3252–5.View ArticlePubMedGoogle Scholar
  90. Conant GC, Wolfe KH. GenomeVx: simple web-based creation of editable circular chromosome maps. Bioinformatics. 2008;24:861–2.View ArticlePubMedGoogle Scholar
  91. Schattner P, Brooks AN, Lowe TM. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 2005;33:W686–9.View ArticlePubMedPubMed CentralGoogle Scholar
  92. Darling AE, Mau B, Perna NT. ProgressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One. 2010;5:e11147.View ArticlePubMedPubMed CentralGoogle Scholar
  93. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 2004;32:W273–9.View ArticlePubMedPubMed CentralGoogle Scholar
  94. Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R. REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 2001;29:4633–42.View ArticlePubMedPubMed CentralGoogle Scholar
  95. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.View ArticlePubMedPubMed CentralGoogle Scholar
  96. Lanfear R, Calcott B, Ho SYW, Guindon S. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol. 2012;29:1695–701.View ArticlePubMedGoogle Scholar

Copyright

© The Author(s). 2017