PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of plosonePLoS OneView this ArticleSubmit to PLoSGet E-mail AlertsContact UsPublic Library of Science (PLoS)
 
PLoS One. 2017; 12(2): e0172924.
Published online 2017 February 27. doi:  10.1371/journal.pone.0172924
PMCID: PMC5328339

The complete chloroplast genome sequences of Lychnis wilfordii and Silene capitata and comparative analyses with other Caryophyllaceae genomes

Shihui Yang, Editor

Abstract

The complete chloroplast genomes of Lychnis wilfordii and Silene capitata were determined and compared with ten previously reported Caryophyllaceae chloroplast genomes. The chloroplast genome sequences of L. wilfordii and S. capitata contain 152,320 bp and 150,224 bp, respectively. The gene contents and orders among 12 Caryophyllaceae species are consistent, but several microstructural changes have occurred. Expansion of the inverted repeat (IR) regions at the large single copy (LSC)/IRb and small single copy (SSC)/IR boundaries led to partial or entire gene duplications. Additionally, rearrangements of the LSC region were caused by gene inversions and/or transpositions. The 18 kb inversions, which occurred three times in different lineages of tribe Sileneae, were thought to be facilitated by the intermolecular duplicated sequences. Sequence analyses of the L. wilfordii and S. capitata genomes revealed 39 and 43 repeats, respectively, including forward, palindromic, and reverse repeats. In addition, a total of 67 and 56 simple sequence repeats were discovered in the L. wilfordii and S. capitata chloroplast genomes, respectively. Finally, we constructed phylogenetic trees of the 12 Caryophyllaceae species and two Amaranthaceae species based on 73 protein-coding genes using both maximum parsimony and likelihood methods.

Introduction

Chloroplasts are important photosynthetic organelles that provide energy for the synthesis of glucose, fatty acids, and amino acids [1,2]. The chloroplast genome is the smallest of the plant genomes, ranging from 135 to 160 kb in most plants [35]. Most angiosperm chloroplast genomes have a quadripartite circular structure and contain two copies of inverted repeat (IR) regions, separating a large single copy (LSC) region and small single copy (SSC) region [5]. Recently, with the rapid development of next-generation sequencing platforms, many chloroplast genome sequences have been reported and used to help resolve plant phylogenies [6,7]. Chloroplast genomic data are widely used in various studies, such as those on molecular phylogeny, molecular identification (DNA barcoding), and genetic diversity [810]. The structure and gene order of the chloroplast genome are stable, and the rates of nucleotide substitution are generally slow in angiosperms [1114].

Rearrangements in the chloroplast genome were considered to have occurred rarely enough in evolution that they can be used to demarcate major groups [4]; however, recently some lineages have revealed various patterns of changes in chloroplast genomes, for example large-scale rearrangements, gene duplications, and even loss of IR regions [1520]. Scattered angiosperm lineages show extensive rearrangement of plastid genomes, and these gene order changes are correlated with increased rates of nucleotide substitutions and gene and intron losses [6]. Rearrangements of the chloroplast genome are often associated with repeated sequences [5].

The family Caryophyllaceae consists of 75–80 genera and approximately 2,000 species, which are widely distributed, mainly in the temperate or warm-temperate regions of the northern hemisphere [21]. The genera Lychnis and Silene are sister genera belonging to tribe Sileneae, but the taxonomic identities and limitations between these two genera remain unclear [2123], which is why the genus Lychnis was nested within Silene using nuclear ribosomal internal transcribed spacer (nrITS), five chloroplast genes, and intergenic spacers (IGS) [24]. Previous studies have shown that the Sileneae underwent accelerated plastid genome evolution, including inversions, shifts in IR boundaries, large indels, intron losses, and rapid rates of amino acid sequence substitution [25,26]. Interestingly, the psaA-ycf3:psaI-ycf4 inversion and intron losses in clpP-1 and clpP-2 were suggested to be independent events that occurred three times [26].

A total of ten Caryophyllaceae chloroplast genomes have been reported [2528]. In the genus Lychnis, only the chloroplast genome of L. chalcedonica has been reported [26], whereas in Silene, chloroplast genomes from a total of six species have been reported [25,26]. Therefore, in this study, we sequenced the complete chloroplast genomes of L. wilfordii and S. capitata and then analyzed them to identify their genetic characteristics and differences compared with other Caryophyllaceae species. The specific goals of the present study were to (1) present the complete chloroplast genome sequences of two Sileneae species, (2) investigate any significant characteristics suggesting extensive genome rearrangement in this tribe, and (3) explore significant changes in gene content and intron losses in the tribe Sileneae.

Materials and methods

Plant materials, DNA extraction, sequencing and genome assembly

Leaf materials from Lychnis wilfordii and Silene capitata were obtained from living plants by seed germination in a greenhouse at the Korean Botanical Garden. The voucher specimens of L. wilfordii (NIBRVP0000542331) and S. capitata (NIBRVP0000542433) were deposited in the National Institute of Biological Resources Herbarium (KB). Total genomic DNA was extracted using the Genome Wizard kit (Promega, Madison, WI, USA). Sequencing libraries were prepared using the NEXTflex Rapid DNA-seq kit (Bioo Scientific, Austin, TX, USA). Paired-end sequencing libraries containing insert sizes of approximately 350–450 bp were sequenced on the Illumina Hiseq 2500 platform (Illumina Inc., San Diego, CA, USA) at the National Instrumentation Center for Environmental Management (Seoul, South Korea), yielding 27,739,600 reads from L. wilfordii and 22,127,152 reads from S. capitata, each with a read length of 250 bp. These paired-end reads were aligned with sequences from Silene vulgaris (JF715057). After screening these paired-end reads through alignment with S. vulgaris plastid genome, 585,206 (2.1%) reads of L. wilfordii and 661,807 (2.9%) reads of S. capitata were extracted with mean of coverage 980× and 1082×, respectively. De novo assembly was performed using Geneious v. 7.1.3 (Biomatters, Auckland, New Zealand). The consensus sequences were extracted and gap-filled by PCR amplification using specific primers based on the gaps between sequences. The PCR products were purified and sequenced by Sanger sequencing.

Genome annotation and comparative analyses

The initial annotation of the two Caryophyllaceae chloroplast genomes was performed using Dual Organellar GenoMe Annotator (DOGMA) [29]. From this initial annotation, putative starts, stops, and intron positions were determined by comparison with homologous genes in other Caryophyllaceae chloroplast genomes. The tRNA genes were annotated using DOGMA and tRNAscan-SE [30]. The circular chloroplast genome map was drawn using the OGDraw program [31]. The complete chloroplast genomes of L. wilfordii and S. capitata were compared with those of ten other Caryophyllaceae species using the mVISTA program in Shuffle-LAGAN mode (Table 1) [32]. Agrostemma githago (KF527884) was used as a reference.

Table 1
GenBank accession numbers and references used in this study.

Repeat sequence analysis

Simple sequence repeats (SSRs or microsatellites; mono-, di-, tri-, tetra-, penta-, and hexanucleotide repeats) were detected using Phobos v. 3.3.12 [33] with thresholds of ten repeat units for mononucleotide SSRs, five repeat units for di- and trinucleotide SSRs, and three repeat units for tetra-, penta-, and hexanucleotide SSRs. REPuter [34] was also used to analyze the repeat sequences, which included forward, reverse, palindromic, and complementary sequences with a minimal length of 30 bp and 90% sequence identities (Hamming distance of three). Moreover, we constructed a phylogenetic trees based on the sequences of the pairs of repeat regions to investigate the relationship between the distributions of repeat sequences and structural inversions. Maximum parsimony (MP) analysis was conducted using PAUP v. 4.0a150 [35], and branch support was assessed using 1000 bootstrap replicates.

Phylogenetic analysis

Phylogenetic analyses based on 73 protein-coding genes were also performed for 12 Caryophyllaceae species, using two Amaranthaceae species (Beta vulgaris and Salicornia europaea) as the outgroup (Table 1). Among 77 whole protein-coding genes, ycf1, ycf2, accD, clpP genes were excluded from data matrix, since those genes were reported fast evolving genes with high substitution rate within tribe Sileneae [26]. Consequently, a total of 54,271 bp were aligned using MAFFT [36]. MP analysis was conducted using PAUP v. 4.0a150 [35], and branch support was assessed using 1000 bootstrap replicates. Before Maximum likelihood (ML) analysis, a search for the best fitting substitution model was performed using jModeltest v. 2.1.5 [37]. Based on the Akaike Information Criterion (AIC) and Akaike Information Criterion with Correction (AICc), GTR+I+G was the best model. ML analysis was performed using RAxML v. 7.4.2 with 1000 bootstrap replicates and the GTR+I+G model [38]. Bayesian inference was performed using MrBayes 3.2 [39].

Results and discussion

Genome organization and features

The complete sizes of the L. wilfordii and S. capitata chloroplast genomes are 152,320 and 150,224 bp, respectively (Fig 1, Table 2). The size of the L. wilfordii chloroplast genome is the longest among the reported Caryophyllaceae species. The L. wilfordii and S. capitata genomes include a pair of IRs of 27,709 bp and 25,371 bp separated by a SSC region of 12,914 bp and 17,313 bp and a LSC region of 83,988 bp and 82,169 bp, respectively (Fig 1, Table 2), similar to the published Caryophyllaceae chloroplast genomes [2528]. The L. wilfordii chloroplast genome contains 110 unique genes, 17 of which are duplicated in the IR region, giving a total of 127 genes (Fig 1, Table 2, S1 Table). The S. capitata chloroplast genome contains 111 unique genes, 19 of which are duplicated in the IR region, giving a total of 130 genes (Fig 1, Table 2, S2 Table). The chloroplast genomes of these two species contain 30 distinct tRNAs, seven of which are duplicated in the IR region. Seventeen genes contain one or two introns: 14 contain one intron and three (rps12, clpP, and ycf3) two introns. Six of the genes containing one intron are tRNAs (S1 and S2 Tables).

Fig 1
The chloroplast genomes of Lychnis wilfordii and Silene capitata.
Table 2
Summary of chloroplast genome characteristics of two caryophyllaceae genomes.

In addition, while the L. wilfordii and S. capitata chloroplast genomes both have lost the infA gene, the accD gene was pseudogenized only in L. wilfordii. The lack or pseudogenization of the infA gene has been discovered in many taxa outside of Caryophyllaceae, such as the Brassicaceae, Fabaceae, Liliaceae, Malvaceae, and Onagraceae [25,26,4044]. Loss or pseudogenization of the accD gene in the plastid genome or accD gene transfer to the nucleus has also been reported in various angiosperm lineages, including Poaceae, Orobanchaceae, Ericaceae, and Primulaceae [4548].

Comparative chloroplast genomic analysis

We compared gene arrangements in the chloroplast genomes of L. wilfordii and S. capitata with those of the ten previously reported Caryophyllaceae species (Fig 2). The chloroplast genome of S. capitata has an identical gene order with those of the genera Agrostemma, Colobanthus, and Dianthus, but the chloroplast genome of L. wilfordii has unique structural changes compared with previously reported Caryophyllaceae chloroplast genomes (Fig 2). The gene rearrangements present in the LSC regions were a result of inversions and/or transpositions (Fig 2). The chloroplast genome of L. wilfordii revealed an inversion of the trnV-rbcL region compared with the genomes of other genera (Fig 2), whereas the L. chalcedonica genome had twice the number of inversions and transpositions in the accD-psaI and ycf3 regions compared with the genomes of other genera (Fig 2). Interestingly, truncated partial sequences of clpP-2 and accD were found in the IGS region between trnV and psaI. The 5’ upstream non-genic region and a partial 348 bp sequence of the accD gene, as well as the exon 1 and partial intron 1 sequences of clpP-2, have remained, but the downstream regions of both genes were truncated in the L. wilfordii chloroplast genome. Compared with the gene orders in other chloroplast genomes, these disruptions in the accD and clpP-2 genes may have occurred by inversion of the trnV-rbcL fragment. Thus, we deduced that duplication of clpP occurred before diversification of L. chalcedonica from L. wilfordii, and that transposition of psaI-accD and the loss of introns in clpP-1 and clpP-2 in L. chalcedonica may have occurred after species diversification.

Fig 2
Comparison of gene rearrangements in the large single copy region among 12 Caryophyllaceae.

In the genus Silene, we identified three types of chloroplast genomes (Fig 2). These are a) the common type of chloroplast genome observed in most Caryophyllaceae (Agrostemma, Colobanthus, and Dianthus) (seen in S. capitata, S. latifolia, and S. vulgaris); b) chloroplast genomes exhibiting an inversion of the ycf3-psaI regions (seen in S. paradoxa, S. conoidea, and S. conica); c) chloroplast genomes exhibiting transpositions and/or inversions of the psbD-accD, petL-clpP, trnD-T, and psaI-psbE regions (seen in S. noctiflora). Silene noctiflora currently has the most complicated chloroplast genome among the Caryophyllaceae.

Overall sequence identity was analyzed with mVISTA program the among the 12 chloroplast genomes of Caryophyllaceae, using the Agrostemma githago genome as a reference (Fig 3). The results revealed higher divergence in the LSC regions than in the IRs and SSCs, as a result of gene rearrangements (Figs (Figs22 and and3),3), and greater conservation in the coding regions than in the non-coding regions (Fig 3). The most divergent coding regions were the ycf1, ycf2, accD, and clpP genes, which are similar to results from previous studies [25,26,49], showing lower (under 50%) similarity compared with other protein-coding regions (Fig 3). Consequently, we suggest that these genes evolve rapidly in Caryophyllaceae (including the tribe Sileneae). These genes are either absent or highly variable in the genomes of Campanulaceae, Geraniaceae, and Poaceae [6].

Fig 3
Sequence alignment of 12 Caryophyllaceae genomes in mVISTA, using the Agrostemma githago genome as a reference.

Boundaries between single copy and inverted repeat regions

The size variations among angiosperm chloroplast genomes are mostly the result of expansion or contraction of the IR region [50]. Additionally, the expansion or contraction of the IR region differs among various plant species [51]. In this study, the LSC-IR and IR-SSC boundaries of the 12 sequenced Caryophyllaceae genomes were compared (Fig 4). IR locations have changed substantially in Lychnis and Silene as a result of movement of the boundaries between the IR and SC regions (Fig 4). The IR and SC boundaries of S. capitata are consistent with those of the S. vulgaris and S. latifolia genomes, as well as the Caryophyllaceae genera Agrostemma, Colobanthus, and Dianthus (Fig 4).

Fig 4
Comparison of the large single copy, inverted repeat, and small single copy border regions among 12 Caryophyllaceae chloroplast genomes.

The expansion of the IR at the SSC/IR boundary that duplicates the entire ycf1 gene was found only in the genome of L. wilfordii and three Silene species (S. conica, S. conoidea, and S. noctiflora). This event was observed in non-core Caryophyllales [52]. In the S. noctiflora chloroplast genome, the ycf1 and rps15 genes are duplicated within the IR region (Fig 4), and this species contains the longest IR region (29,891 bp) among the 12 Caryophyllaceae species. However, the contraction of the IR at the LSC/IR boundary that duplicates a part of the rpl2 gene was found only in Silene (S. conica, S. conoidea, and S. noctiflora) and Lychnis (L. wilfordii and L. chalcedonica). Lychnis chalcedonica has the shortest IR region (23,540 bp) among 12 Caryophyllaceae species due to contraction of the IR region at the LSC/IR boundary and lack of expansion of the IR region at the IR/SSC boundary.

Repeat sequence analysis and short inverted repeats as inversion hotspots

We analyzed repeat sequences from the chloroplast genomes of L. wilfordii and S. capitata and observed forward, reverse, palindromic, and complementary repeats using REPuter. Lychnis wilfordii contains 17 forward repeats and 22 palindromic repeats, whose lengths range from 40 to 462 bp (Fig 5, S3 Table). Silene capitata contains 15 forward repeats, 27 palindromic repeats, and only one reverse repeat, whose lengths range from 30 to 64 bp (Fig 5, S4 Table). Most of the L. wilfordii repeats are located in IGS regions (56.4%), and less than half were located in genes (30.8%; ycf1 and ycf2) and introns (12.8%; ndhA and clpP intron). In contrast, the majority of S. capitata repeats are located in genes (44.0%; ycf2, ycf4, psaA, psaB, ccsA, trnS-GGA, trnS-GCU, trnS-UGA, trnG-UCC, and trnG-GCC), with fewer located in IGSs (40.0%) and introns (16.0%; ycf3, rpl16, rpoC1, and ndhA introns).

Fig 5
Frequency of repeat sequences in the chloroplast genomes of Lychnis wilfordii and Silene capitata using REPuter.

We then analyzed the SSRs (or microsatellites), which are increasingly evaluated in molecular genetic studies because of their high reproducibility, ease of scoring, and fast throughput compared with other marker techniques [53]. In the L. wilfordii and S. capitata chloroplast genomes, the most abundant SSRs were A or T mononucleotide repeats, which accounted for approximately 77.6% and 76.8% of the total SSRs, followed by tetranucleotides (10.4% and 16.1%) and dinucleotides (10.4% and 7.1%), respectively (Table 3, S5 and S6 Tables). SSRs in the chloroplast genome are commonly composed of A or T repeats and rarely G or C repeats [54,55]. Furthermore, the majority of L. wilfordii and S. capitata SSRs are located in IGS regions (49.3% and 55.4%), followed by genes (37.3% and 26.8%) and introns (13.4% and 17.9%), respectively (S5 and S6 Tables). SSRs located in coding regions were found mainly in ycf1 and rpoC2, with the remaining SSRs found in matK, rpoA, psbF, atpB, and atpF. Among the SSRs in genes, part or all of those in matK, rpoC2, rpoA, psbF, ycf1, and rrn23 were shared by the two Caryophyllaceae species.

Table 3
The types and number of SSRs in chloroplast genomes of L. wilfordii and S. capitata.

Under the assumption that the common chloroplast types observed in most Caryophyllaceae (Agrostemma, Colobanthus, and Dianthus, S. capitata, S. latifolia, and S. vulgaris) are ancestral, the inversion of the ycf3-psaI fragment might have occurred independently at least three times: in L. chalcedonica, S. notiflora, and the lineage containing S. conoidea and S. conica, consistent with previous results [26]. Interestingly, loss of introns in the clpP gene is always coupled with these inversions. In Caryophyllaceae, all 12 species possess imperfect palindromic repeats on both sides of the ycf3-psaI fragment (Fig 2), whereas only one homologous sequence corresponding to these repeats was found in the intergenic region between psaI and ycf4 in two Amaranthaceae species. In all cases, the repeat sequences were overlapped by partial ycf4 coding region sequences (63 bp). Thus, the partial ycf4 and upstream sequences might have been duplicated in the IGS between psaA and ycf3 before diversification of Caryophyllaceae. Even in the repeats between psaA and ycf3, expected to be non-genic sequences, intermolecular duplicated sequences were grouped together in A. githago, C. quitensis, D. longicalix, and S. paradoxa based on the maximum parsimony tree (Fig 6). The intermolecular duplicated sequences were not grouped together in the other Silene species. A large fragment inversion mediated by short IRs was reported in several plant species. The 22 kb inversion in Asteraceae [56], the 42 kb inversion in Abies of the Pinaceae [57], the 21 kb inversion in Jasminae of the Oleaceae [16], and the 36 kb inversion in the core Genistoids are thought to be induced by IRs in tRNAs or repeat elements several base pairs long. These dispersed repeats were shown to promote inversions via intermolecular recombination [5,58,59]. Thus, we suggest that this short IR in Caryophyllaceae might mediate intramolecular flip-flop recombination events, and thus, independent identical inversion events of the ycf3-psaI 18 kb fragment might be facilitated independently in different lineages.

Fig 6
A phylogenetic tree of the inverted repeats at the end of the 18 kb inversion of the psaI-ycf3 fragment.

Phylogenetic analysis

Both the MP and ML trees of the 12 Caryophyllaceae species and two Amaranthaceae species based on 73 protein-coding genes showed consistent phylogenetic patterns (Fig 7, S1 Fig). In the ML tree, bootstrap analysis indicated that eight of ten nodes were supported by bootstrap values ≥ 99% and the other two nodes by values > 65%. In previous studies, the genus Lychnis was shown to be nested within the genus Silene based on internal transcribed spacer (ITS) sequences of nuclear genome and chloroplast DNA data [24,60] and based on chloroplast genome data [26]. Lychnis species were nested within Silene, close to S. paradoxa in the subgenus Silene, which is consistent with previous studies [26] (Fig 7). The subgenus Behenantha and monophyly of sect. Melandrium (S. capitata and S. latifolia) were not supported, whereas S. conoidea and S. conica of sect. Conoimorpha form a monophyletic group were found to be closely related to S. noctiflora of sect. Elisanthe (Fig 7). However, we need additional chloroplast genome data from more Sileneae species to resolve the relationship between Lychnis and Silene, as well as the infrageneric relationships of Silene.

Fig 7
Phylogenetic tree of 14 taxa based on 73 protein-coding genes using the maximum likelihood method.

Supporting information

S1 Fig

Phylogenetic tree of 14 taxa based on 73 protein-coding genes obtained using the maximum parsimony (MP) method in PAUP.

Bootstrap values greater than 50% are shown above the nodes.

(TIF)

S1 Table

List of genes present in the chloroplast genome of Lychnis wilfordii.

(DOCX)

S2 Table

List of genes present in the chloroplast genome of Silene capitata.

(DOCX)

S3 Table

List of repeat sequences in the chloroplast genome of Lychnis wilfordii.

(DOCX)

S4 Table

List of repeat sequences in the chloroplast genome of Silene capitata.

(DOCX)

S5 Table

List of simple sequence repeats in the chloroplast genome of Lychnis wilfordii.

(DOCX)

S6 Table

List of simple sequence repeats in the chloroplast genome of Silene capitata.

(DOCX)

Acknowledgments

This work was supported by a grant from the National Institute of Biological Resources (NIBR) funded by the Ministry of Environment of the Republic of Korea (NIBR201503102). The authors thank Young Chul Kim for help with collecting the samples.

Funding Statement

This work was supported by a grant from the National Institute of Biological Resources (NIBR) funded by the Ministry of Environment of the Republic of Korea (NIBR201503102).

Data Availability

Data Availability

All relevant data are within the paper and its Supporting Information files.

References

1. Neuhaus HE, Emes MJ. Nonphotosynthetic metabolism in plastids. Annu Rev Plant Biol. 2000; 51: 111–140. [PubMed]
2. Rodríguez-Ezpeleta N, Brickmann H, Burey SC, Roure B, Burger G, Löffelhardt W, et al. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Current Biology. 2005; 15(14): 1325–1330. doi: 10.1016/j.cub.2005.06.040 [PubMed]
3. Downie SR, Palmer JD. Use of chloroplast DNA rearrangements in reconstructing plant phylogeny In: Soltis PS, Soltis DE, Doyle JJ. Molecular Systematics of Plants, Springer US; 1992. pp. 14–35.
4. Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ. Plant systematics: a phylogenetic approach. 2nd ed. Sinauer Associates, Inc., Sunderland, Massachusetts. USA; 2002.
5. Palmer JD. Plastid chromosomes: structure and evolution In: Vasil LK, Bogorad L. Cell Culture and Somatic Cell Genetics in Plants, the Molecular Biology of Plastid 7A. Academic Press, San Diego; 1991. pp. 5–53.
6. Jansen RK, Cai Z, Raubeson LA, Daniell H, dePamphilis CW, Leebens-Mack J, et al. Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci. U.S.A. 2007; 104, 19369–19374. doi: 10.1073/pnas.0709121104 [PubMed]
7. Shaw J, Shafer HL, Leonard OR, Kovach MJ, Schorr M, Morris AB. Chloroplast DNA sequence utility for the lowest phylogenetic and phylogeographic inferences in angiosperms: the tortoise and the hare IV. American Journal of Botany. 2014; 101: 1987–2004. doi: 10.3732/ajb.1400398 [PubMed]
8. Burke SV, Grennan CP, Duvall MR. Plastome sequences of two New World bamboos—Arundinaria gigantea and Cryptochloa strictiflora (Poaceae)—extend phylogenomic understanding of Bambusoideae. American Journal of Botany. 2012; 99(12): 1951–1961. doi: 10.3732/ajb.1200365 [PubMed]
9. Huang H, Shi C, Liu Y, Mao SY, Gao LZ. Thirteen Camellia chloroplast genome sequences determined by high-throughput sequencing: genome structure and phylogenetic relationships. BMC Evol Biol. 2014; 14: 151 doi: 10.1186/1471-2148-14-151 [PMC free article] [PubMed]
10. Walker JF, Zanis MJ, Emery NC. Comparative analysis of complete chloroplast genome sequence and inversion variation in Lasthenia burkei (Madieae, Asteraceae). American Journal of Botany. 2014; 101(4), 722–729. doi: 10.3732/ajb.1400049 [PubMed]
11. Wolfe KH, Li WH, Sharp PM. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences. 1987; 84(24): 9054–9058. [PubMed]
12. Raubeson LA, Jansen RK. Chloroplast genomes of plants In: Henry RJ. Plant Diversity and Evolution: Genotypic and Phenotypic Variation in Higher Plants. CABI, Wallingford, UK; 2005. pp. 45–68.
13. Drouin G, Daoud H, Xia J. Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Molecular Phylogenetics and Evolution. 2008; 49(3): 827–831. doi: 10.1016/j.ympev.2008.09.009 [PubMed]
14. Bell CD, Soltis DE, Soltis PS. The age and diversification of the angiosperms re-revisited. American Journal of Botany 2010; 97(8): 1296–1303. doi: 10.3732/ajb.0900346 [PubMed]
15. Cosner ME, Raubeson LA, Jansen RK. Chloroplast DNA rearrangements in Campanulaceae: phylogenetic utility of highly rearranged genomes. BMC Evol Biol. 2004; 4(1): 1. [PMC free article] [PubMed]
16. Lee HL, Jansen RK, Chumley TW, Kim KJ. Gene relocations within chloroplast genomes of Jasminum and Menodora (Oleaceae) are due to multiple, overlapping inversions. Mol Biol Evol. 2007; 24: 1161–1180. doi: 10.1093/molbev/msm036 [PubMed]
17. Cai Z, Guisinger M, Kim HG, Ruck E, Blazier JC, McMurtry V, et al. Extensive reorganization of the plastid genome of Trifolium subterraneum (Fabaceae) is associated with numerous repeated sequences and novel DNA insertions. Journal of Molecular Evolution. 2008; 67(6): 696–704. doi: 10.1007/s00239-008-9180-7 [PubMed]
18. Guisinger MM, Chumley TW, Kuehl JV, Boore JL, Jansen RK. Implications of the plastid genome sequence of Typha (Typhaceae, Poales) for understanding genome evolution in Poaceae. Journal of Molecular Evolution. 2010; 70(2): 149–166. doi: 10.1007/s00239-009-9317-3 [PMC free article] [PubMed]
19. Guisinger MM, Kuehl JV, Boore JL, Jansen RK. Extreme reconfiguration of plastid genomes in the angiosperm family Geraniaceae: rearrangements, repeats, and codon usage. Molecular Biology and Evolution. 2011; 28(1): 583–600. doi: 10.1093/molbev/msq229 [PubMed]
20. Martin GE, Rousseau-Gueutin M, Cordonnier S, Lima O, Michon-Coudouel S, Naquin D, et al. 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. Annals of Botany. 2014; 113(7): 1197–1210. doi: 10.1093/aob/mcu050 [PMC free article] [PubMed]
21. Lu D, Wu Z, Zhou L, Chen S, Gilbert MG. Caryophyllaceae. In: Wu ZY, Raven RH, Hong DY (eds). www.eFloras.org, Flora of China, vol. 6. Accessed 2016 August 20th.
22. Greuter W. Silene (Caryophyllaceae) in Greece: a subgeneric and sectional classification. Taxon. 1995; 44(4): 543–581.
23. Lidén M, Popp M, Oxelman B. A revised generic classification of the tribe Sileneae (Caryophyllaceae). Nordic Journal of Botany. 2000; 20(5): 513–518.
24. Greenberg AK, Donoghue MJ. Molecular systematics and character evolution in Caryophyllaceae. Taxon. 2011; 60(6): 1637–1652.
25. Sloan DB, Alverson AJ, Wu M, Palmer JD, Taylor DR. Recent acceleration of plastid sequence and structural evolution coincides with extreme mitochondrial divergence in the angiosperm genus Silene. Genome Biol Evol. 2012; 4(3): 294–306. doi: 10.1093/gbe/evs006 [PMC free article] [PubMed]
26. Sloan DB, Triant DA, Forrester NJ, Bergner LM, Wu M, Taylor DR. A recurring syndrome of accelerated plastid genome evolution in the angiosperm tribe Sileneae (Caryophyllaceae). Molecular Phylogenetics and Evolution. 2014; 72: 82–89. doi: 10.1016/j.ympev.2013.12.004 [PubMed]
27. Kang Y, Lee H, Kim MK, Shin SC, Park H, Lee J. The complete chloroplast genome of Antarctic pearlwort, Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae). Mitochondrial DNA. 2015. [PubMed]
28. Gurusamy R, Lee DH, Park SJ. The complete chloroplast genome sequence of Dianthus superbus var. longicalycinus. Mitochondrial DNA Part A. 2016; 27(3): 2015–2017. [PubMed]
29. Wyman SK, Jansen RK, Boore JL. Automatic annotation of organellar genomes with DOGMA. Bioinformatics. 2004; 20(17): 3252–3255. doi: 10.1093/bioinformatics/bth352 [PubMed]
30. Schattner P, Brooks AN, Lowe TM. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Research. 2005; 33, W686–W689. doi: 10.1093/nar/gki366 [PMC free article] [PubMed]
31. Lohse M, Drechsel O, Kahlau S, Bock R. OrganellarGenomeDRAW—a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res. 2013. [PMC free article] [PubMed]
32. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 2004; 32, W273–W279. doi: 10.1093/nar/gkh458 [PMC free article] [PubMed]
33. Mayer C. Phobos Version 3.3.12. A tandem repeat search program. 20 p. 2010; Available:http://www.rub.de/spezzoo/cm/cm_phobos.htm. Accessed 2016 September 30th.
34. Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R. REPuter: the manifold applications of repeat analysis on a genome scale. Nucleic Acids Res. 2001; 29(22): 4633–4642. [PMC free article] [PubMed]
35. Swofford DL. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sunderland, MA: Sinauer Associates; 2003.
36. Katoh K, Misawa K, Kuma KI, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002; 30: 3059–3066. [PMC free article] [PubMed]
37. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Meth. 2012; 9: 772. [PMC free article] [PubMed]
38. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006; 22(21): 2688–2690. doi: 10.1093/bioinformatics/btl446 [PubMed]
39. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology. 2012; 61(3): 539–542. doi: 10.1093/sysbio/sys029 [PMC free article] [PubMed]
40. Sato S, Nakamura Y, Kaneko T, Asamizu E, Tabata S. Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Research. 1999; 6(5): 283–290. [PubMed]
41. Hupfer H, Swiatek M, Hornung S, Herrmann RG, Maier RM, Chiu WL, et al. Complete nucleotide sequence of the Oenothera elata plastid chromosome, representing plastome I of the five distinguishable Euoenothera plastomes. Molecular and General Genetics MGG. 2000; 263(4): 581–585. [PubMed]
42. Kato T, Kaneko T, Sato S, Nakamura Y, Tabata S. Complete structure of the chloroplast genome of a legume, Lotus japonicas. DNA Res. 2000; 7(6): 323–330. [PubMed]
43. Ibrahim RIH, Azuma JI, Sakamoto M. Complete nucleotide sequence of the cotton (Gossypium barbadense L.) chloroplast genome with a comparative analysis of sequences among 9 dicot plants. Genes & Genetic Systems. 2006; 81(5): 311–321. [PubMed]
44. Do HDK, Kim JS, Kim JH. Comparative genomics of four Liliales families inferred from the complete chloroplast genome sequence of Veratrum patulum O. Loes. (Melanthiaceae). Gene. 2013; 530(2): 229–235. doi: 10.1016/j.gene.2013.07.100 [PubMed]
45. Harris ME, Meyer G, Vandergon T, Vandergon VO. Loss of the acetyl-CoA carboxylase (accD) gene in Poales. Plant Molecular Biology Reporter. 2013; 31(1): 21–31.
46. Li X, Zhang TC, Qiao Q, Ren Z, Zhao J, Yonezawa T, et al. Complete chloroplast genome sequence of holoparasite Cistanche deserticola (Orobanchaceae) reveals gene loss and horizontal gene transfer from its host Haloxylon ammodendron (Chenopodiaceae). PLoS One (2013; 8(3): e58747 doi: 10.1371/journal.pone.0058747 [PMC free article] [PubMed]
47. Martínez-Alberola F, del Campo EM, Lázaro-Gimeno D, Mezquita-Claramonte S, Molins A, Mateu-Andrés I, et al. Balanced gene losses, duplications and intensive rearrangements led to an unusual regularly sized genome in Arbutus unedo chloroplasts. PLoS One. 2013; 8(11): e79685 doi: 10.1371/journal.pone.0079685 [PMC free article] [PubMed]
48. Liu TJ, Zhang CY, Yan HF, Zhang L, Ge XJ, Hao G. Complete plastid genome sequence of Primula sinensis (Primulaceae): structure comparison, sequence variation and evidence for accD transfer to nucleus. PeerJ. 2016; 4: e2101 doi: 10.7717/peerj.2101 [PMC free article] [PubMed]
49. Erixon P, Oxelman B. Reticulate or tree-like chloroplast DNA evolution in Sileneae (Caryophyllaceae)?. Molecular Phylogenetics and Evolution. 2008; 48: 313–325. doi: 10.1016/j.ympev.2008.04.015 [PubMed]
50. Ravi V, Khurana JP, Tyagi AK, Khurana P. An update on chloroplast genomes. Plant Systematics and Evolution. 2008; 271: 101–122.
51. Ni L, Zhao Z, Xu H, Chen S, Dorje G. The complete chloroplast genome of Gentiana straminea (Gentianaceae), an endemic species to the Sino-Himalayan subregion. Gene. 2016; 577(2): 281–288. doi: 10.1016/j.gene.2015.12.005 [PubMed]
52. Logacheva MD, Penin AA, Valiejo-Roman CM, Antonov AS. Structure and evolution of junctions between inverted repeat and small single copy regions of chloroplast genome in non-core Caryophyllales. Molecular Biology. 2009; 43: 757–765. [PubMed]
53. Sun QB, Li LF, Li Y, Wu GJ, Ge XJ. SSR and AFLP markers reveal low genetic diversity in the biofuel plant in China. Crop Science. 2008; 48(5): 1865–1871.
54. Kuang DY, Wu H, Wang YL, Gao LM, Zhang SZ, Lu L. Complete chloroplast genome sequence of Magnolia kwangsiensis (Magnoliaceae): implications for DNA barcoding and population genetics. Genome. (2011; 54(8): 663–673. doi: 10.1139/G11-026 [PubMed]
55. Qian J, Song J, Gao H, Zhu Y, Xu J, Pang X, et al. The complete chloroplast genome sequence of the medicinal plant Salvia miltiorrhiza. PLoS One. 2013; 8(2): e57607 doi: 10.1371/journal.pone.0057607 [PMC free article] [PubMed]
56. Kim KJ, Choi KS, Jansen RK. Two chloroplast DNA inversions originated simultaneously during the early evolution of the sunflower family (Asteraceae). Molecular Biology and Evolution. 2005; 22(9): 1783–1792. doi: 10.1093/molbev/msi174 [PubMed]
57. Tsumura Y, Suyama Y, Yoshimura K. Chloroplast DNA inversion polymorphism in populations of Abies and Tsuga. Molecular Biology and Evolution. 2000; 17(9): 1302–1312. [PubMed]
58. Ogihara Y, Terachi T, Sasakuma T. Intramolecular recombination of chloroplast genome mediated by short direct-repeat sequences in wheat species. Proceedings of the National Academy of Sciences. 1988; 85(22): 8573–8577. [PubMed]
59. Knox EB, Downie SR, Palmer JD. Chloroplast genome rearrangements and the evolution of giant lobelias from herbaceous ancestors. Molecular Biology and Evolution. 1993; 10(2): 414–430.
60. Fior S, Karis PO, Casazza G, Minuto L, Sala F. Molecular phylogeny of the Caryophyllaceae (Caryophyllales) inferred from chloroplast matK and nuclear rDNA ITS sequences. American Journal of Botany. 2006; 93(3): 399–411. doi: 10.3732/ajb.93.3.399 [PubMed]

Articles from PLoS ONE are provided here courtesy of Public Library of Science