Comparative chloroplast genomics and phylogenetics of Fagopyrum esculentum ssp. ancestrale– A wild ancestor of cultivated buckwheat
© Logacheva et al; licensee BioMed Central Ltd. 2008
Received: 27 February 2008
Accepted: 20 May 2008
Published: 20 May 2008
Chloroplast genome sequences are extremely informative about species-interrelationships owing to its non-meiotic and often uniparental inheritance over generations. The subject of our study, Fagopyrum esculentum, is a member of the family Polygonaceae belonging to the order Caryophyllales. An uncertainty remains regarding the affinity of Caryophyllales and the asterids that could be due to undersampling of the taxa. With that background, having access to the complete chloroplast genome sequence for Fagopyrum becomes quite pertinent.
We report the complete chloroplast genome sequence of a wild ancestor of cultivated buckwheat, Fagopyrum esculentum ssp. ancestrale. The sequence was rapidly determined using a previously described approach that utilized a PCR-based method and employed universal primers, designed on the scaffold of multiple sequence alignment of chloroplast genomes. The gene content and order in buckwheat chloroplast genome is similar to Spinacia oleracea. However, some unique structural differences exist: the presence of an intron in the rpl2 gene, a frameshift mutation in the rpl23 gene and extension of the inverted repeat region to include the ycf1 gene. Phylogenetic analysis of 61 protein-coding gene sequences from 44 complete plastid genomes provided strong support for the sister relationships of Caryophyllales (including Polygonaceae) to asterids. Further, our analysis also provided support for Amborella as sister to all other angiosperms, but interestingly, in the bayesian phylogeny inference based on first two codon positions Amborella united with Nymphaeales.
Comparative genomics analyses revealed that the Fagopyrum chloroplast genome harbors the characteristic gene content and organization as has been described for several other chloroplast genomes. However, it has some unique structural features distinct from previously reported complete chloroplast genome sequences. Phylogenetic analysis of the dataset, including this new sequence from non-core Caryophyllales supports the sister relationship between Caryophyllales and asterids.
Chloroplasts are hypothesized to have evolved from ancient endosymbiotic cyanobacteria. They are semi-autonomous possessing their own genome that codes for a set of proteins, which orchestrate the process of photosynthesis and other house-keeping functions. The non-meiotic and mostly uniparental inheritance of chloroplast genes render them as most informational entities in plant phylogenetic studies. Technological enhancements and consequent reduction of time in sequence capture have enabled sequencing of several chloroplast genomes recently. The discipline of plant phylogenetics has been the largest beneficiary of these technological advances. The phylogenetic trees derived from the analysis of whole genome sequences are completely or near-completely resolved, with highly supported nodes. Further, analysis of chloroplast gene-evolution rates can be informative about nodal support as recently demonstrated in Saxifragales where slow evolving genes from the chloroplast inverted repeat region provided support for deep level divergences . Despite the availability of these datasets, complete chloroplast genome sequence-based phylogenies are prone to artifacts caused by incomplete taxon sampling [2–4]. Therefore, availability of complete chloroplast genome sequences from additional taxa is highly desirable for robust phylogenetic studies.
This study reports the complete chloroplast genome sequence from Fagopyrum esculentum ssp. ancestrale, a wild ancestor of cultivated buckwheat . This species belongs to the family Polygonaceae. According to APGII  Polygonaceae is a member of the order Caryophyllales; however this family represents a separate group within it, the so called non-core Caryophyllales  and sometimes it is treated as a separate order, Polygonales . Both phylogenetic and genomic studies are lacking for this group. In addition, the affinities of the order Caryophyllales as a whole also remain debatable. All chloroplast genome sequence-based phylogenies obtained till date place Spinacia (the only representative of Caryophyllales with a known chloroplast genome sequence) as sister to asterids (for example see [9, 10]). Other studies incorporating lesser number of genes but broader taxon sampling placed them at the base of the clade which includes asterids and rosids [6, 11]. To validate if the sister relationship of Caryophyllales and asterids is due to taxon undersampling in Caryophyllales, additional sequence information is highly desirable. Therefore, inclusion of the buckwheat chloroplast genome sequence in a comprehensive phylogenetic analysis is expected to aid in addressing the affinity issue of the Caryophyllales.
The sequence of Fagopyrum chloroplast genome, besides its phylogenetic implications, may provide useful information for more practical aspects. Common buckwheat (F. esculentum) is a widely cultivated multipurpose crop . Access to the chloroplast genome sequence may highlight other physiologically important traits in buckwheat. In addition, the chloroplast genome sequence can be utilized for developing species specific transformation vectors (for review see [13, 14]). Therefore, the knowledge of the nucleotide sequence of buckwheat chloroplast genome opens up an avenue for the application of plastid genetic engineering to this plant.
The seeds of Fagopyrum species used in this study were obtained from All-Russia Research Institute of Legumes and Groat Crops. Plant material for Persicaria, Rheum, Reynoutria and Coccoloba was obtained from Moscow State University Botanical garden.
DNA extraction, amplification and sequencing
Total cellular DNA was isolated from fresh leaf tissue using NucleoSpin Plant DNA kit (Macherey-Nagel) following manufacturer's instructions. PCR amplification was performed on PTC-220 DNA Engine Dyad (MJ Research) using Encyclo PCR kit (Evrogen JSC, Moscow, Russia). For amplification, PCR conditions recommended in , i. e. 35 cycles of touchdown PCR with the decrease of annealing temperature from 55 to 50 deg C, were used. For some primer pairs, PCR was performed with optimization of gradient PCR involving altered annealing temperatures. For Long PCR, extension was performed at 68 deg C for 5 – 7 minutes, depending on the expected amplicon size. PCR products were purified using Gel Extraction & PCR Cleanup Kit (Cytokine Ltd, S.Petersburg, Russia). Automated sequencing was performed on ABI 3100 sequencer using the Big Dye Terminator v.3.1 sequencing kit (ABI, USA).
Sequencing strategy and primer design
The sequence of buckwheat chloroplast genome was obtained using a PCR based approach, similar to the ASAP method described earlier in . The inverted repeat region of the Fagopyrum chloroplast genome was amplified and sequenced with the ASAP primers; the large and small single copy regions were amplified using PCR primers developed from the multiple alignment of known chloroplast genome sequences of angiosperms (primers are listed in Additional file 1). These universal primers enabled amplification of the entire chloroplast genome of Fagopyrum with overlapping PCR fragments ranging in size from 0.5 to 9 kb. Long fragments had to be generated due to a lack of sequence conservation in the aligned chloroplast genomes and few structural changes (for example, in the IR-LSC and IR-SSC junctions). The larger fragments were amplified and sequenced with taxon-specific primers using a primer walking approach (complete list of taxon-specific primers is available in Additional file 2).
Contig assembly and annotation
Sequences generated from a primer pair were first aligned using Blast 2 sequences (bl2seq) tool , available at NCBI website to develop contigs which were then assembled using the BioEdit software . Draft genome annotation was generated using the organelle annotation package DOGMA . The predicted annotations were further verified using BLAST similarity search .
Taxa included in phylogenetic analysis with GenBank accession numbers and references.
GenBank accession number
Leebens-Mack et al., 2005 
Wakasugi et al., 1994 
Goremykin et al., 2003a 
Hansen et al., 2007 
Hansen et al., 2007 
Raubeson et al. 2007 
Goremykin et al., 2004 
Goremykin et al., 2003b 
Cai et al., 2006 
Cai et al., 2006 
Cai et al., 2006 
Goremykin et al., 2005 
Hansen et al., 2007 
Mardanov et al. 2008 
Hiratsuka et al., 1989 
Chang et al., 2006 
Leebens-Mack et al., 2005 
Leebens-Mack et al., 2005 
Maier et al., 1995 
Sato et al., 1999 
Schmitz-Linneweber et al., 2002 
Hansen et al., 2007 
Bausher et al., 2006 
Nalapalli et al., 2007 
Kim et al., 2006 
Ruhlman et al., 2006 
Steane, 2005 
Saski et al., 2005 
Lee et al., 2006 
Timme et al., 2007 
Lee et al., 2007 
Kanamoto et al., unpublished
Kato et al., 2000 
Ravi et al., 2006 
Moore et al., 2006 
Shinozaki et al., 1986 
Hupfer et al., 2000 
Kim, Lee, 2004 
Moore et al., 2006 
Okumura et al., 2006 
Raubeson et al., 2007 
Schmitz-Linneweber et al., 2001 
Jansen et al., 2006 
Gene sequences were parsed to detect frameshift mutations and edited when necessary. Sequences were translated into derived amino acid sequences, which were further aligned using MUSCLE ver. 3.6  followed by manual correction. Nucleotide sequence alignment was overlaid on the amino acid sequence alignment.
Phylogenetic analyses using maximum parsimony (MP) method was performed using PAUP* ver. 4.0b8 . Bayesian inference of phylogeny was explored using the MrBayes program ver. 3.1.2 . Alternative topologies test was performed with the Tree-Puzzle program .
MP analysis involved a heuristic search using tree bisection and reconnection (TBR) branch swapping and 100 random addition replicates. Non-parametric bootstrap analysis  was performed with 100 replicates with TBR branch swapping. Both nucleotide and amino acid sequences were included in the analysis.
Bayesian analysis was also performed using both amino acid and nucleotide sequence datasets. For nucleotide sequence analyses different partitioning strategies were employed: each gene as a separate partition (61 partitions), combination of genes according to their function (4 partitions: photosynthetic metabolism, photosynthetic apparatus, gene expression and others) and partitioning according to codon position (3 partitions). For each of the 61 amino acid partitions, the most appropriate model of substitutions was determined by the BIC (Bayesian Information Criterion) in Modelgenerator ver. 0.43 . Similarly for each nucleotide partition, the most appropriate model of nucleotide substitution was determined by the AIC (Akaike Information Criterion) in Modeltest ver. 3.7 .
Bayesian analysis was performed with three chains in each of the two runs. Each chain started with a random tree, 2500000 replicates for amino acid data and 5000000 replicates for nucleotide data were generated. The trees thus obtained were sampled every 100 generations. The proportion of invariable sites and the shape of gamma-distribution rates were unlinked across partitions. The number of discarded trees was determined using convergence diagnostics.
Results and Discussion
Overall structure and gene content of buckwheat chloroplast genome
The GenBank accession number for the nucleotide sequence reported in this study is EU254477. Complete chloroplast genome of Fagopyrum esculentum ssp. ancestrale is composed of 159599 nucleotide bases. This exceeds the average size of flowering plants chloroplast genomes ~155 Kb and, in particular, almost 9 Kb larger then the chloroplast genome of its closest relative Spinacia oleracea (150725 bp). The observed increase in size is due to the expansion of the inverted repeat (IR) region. The size of the IR region is 30684, the large single copy (LSC) and the small single copy (SSC) regions are 84888 and 13343 bp respectively. Overall AT-content of the entire plastome is 62%, the LSC and SSC are 63% and 68% AT respectively and inverted repeat is 59% AT rich. This is comparable with the other land plant chloroplast genomes (Spinacia oleracea – 63%, Nicotiana sylvestris – 62%, Lotus japonicus – 64%, Zea mays – 62%). The lower AT% of the IR region reflects the lower AT-content of ribosomal RNA genes.
Another feature that is shared between Fagopyrum and Spinacia plastomes is the presence of two genes – psbL and ndhD – with an ACG initiation codon. C to U RNA editing-mediated creation of the AUG initiation codon from the original ACG codon is a common phenomenon observed in case of chloroplast genome-derived transcripts. RNA editing has been experimentally demonstrated for psbL  and ndhD genes in tobacco. The editing of ndhD gene has also been reported in spinach and snapdragon . Since psbL and ndhD genes code for proteins essential for chloroplast function, it is safe to assume that their transcripts are edited in Fagopyrum. This can be substantiated with the help of cDNA sequencing or other experimental evidence in future studies. Interestingly, there are two structural features that are unique to the Fagopyrum plastome. First is the position of the IR-SSC borders relative to other plastid genomes. In Spinacia the IRa/SSC border resides with in the 3' region of ycf1 gene. The remaining ycf1 gene lies in the SSC; a copy of the 3'region of ycf1 gene located in the IRb produces the ycf1 pseudogene at the IRb/SSC border. Buckwheat possesses an expanded IR region and two full-length copies of ycf1 gene are thus generated.
Second, buckwheat plastid genome is comprised of 18 intron-containing genes compared to spinach in which the number of these genes is reduced to 17. This difference is due to the loss of rpl2 intron in spinach . The loss of intron in rpl2 gene has occurred independently in several lineages of flowering plants  and it is considered to be a characteristic feature observed in the members of the core Caryophyllales. Thus, the presence of the rpl2 intron in buckwheat (Polygonaceae) emphasizes the distinction of this group from the core Caryophyllales. The rpl2 intron has also been reported in Rumex, another representative of Polygonaceae, and in the members of Plumbaginaceae, a family that is close to Polygonaceae and often associated with Caryophyllales .
Expansion of the inverted repeat region in buckwheat chloroplast genome
The size and thus the boundary of the chloroplast genome inverted repeat (IR) region is variable amongst different plant species . Previous studies on IR borders have mainly focused on the IR and the LSC junction [34, 35] that revealed multiple instances of expansion and contraction in the IR region, ranging from a few base pairs to more than 15 Kb.
The expanded IR region in buckwheat represents an average increase of 5 Kb when compared with other flowering plants. The observed expansion and the sequence of the enhanced IR region in other Fagopyrum species has been reported previously [36, 37]. This region was shown to be highly similar to the small single copy (SSC) region adjacent to IRa in other dicot chloroplast genomes which enabled the conclusion that this expansion is due to the inclusion of the SSC sequences.
It is interesting to note that the sequence of the expanded region in Fagopyrum esculentum ssp. ancestrale is different from the sequence reported by Aii et al. . The authors had reported a 3711 bp inversion within this region. This inversion affected the transcriptional continuity of ycf1 gene, causing an interruption in its reading frame. The observed difference in the sequence reported in this study could be plausibly explained by the use of different genotypes of buckwheat. However, the reported inversion could be potentially employed for tracing the origin of various buckwheat cultivars. Importantly, the set of buckwheat-specific primers reported in this work are expected to enable future studies of this and other potentially interesting structural features.
We further investigated the expansion of the IR in other species related to Fagopyrum esculentum spp. ancestrale using a PCR based approach with two sets of primers (for details see Additional file 4). One primer in each set annealed to the ndhF and rps15 genes within the SSC. The other primer is common to both sets and anneals to the ycf1 gene. It has only one annealing site within the SSC in chloroplast genomes that do not possess the IR expansion (e. g., Spinacia), but two annealing sites (in the direct and reverse orientations) in the IR of the species which have two copies of ycf1 due to the IR expansion (like Fagopyrum).
In order to determine the relative position of Fagopyrum amongst angiosperms comparative phylogenetic analyses of available plastid genome sequences was performed. The data set consisted of 61 concatenated protein-coding gene sequences from 44 different taxa, including two gymnosperm species as outgroups. Nucleotide and amino acid data sets contained 42504 and 14168 characters respectively after the exclusion of ambiguous alignment positions.
It has been demonstrated previously that the partitioning of complex datasets greatly improves the performance of Bayesian inference [44–46]. Thus, we employed different partitioning schemes (61 partitions, 4 partitions and 3 partitions) in our analyses however, comparison of the resulting trees showed no difference in the resulting tree topologies. At the same time dividing the dataset into 3 partitions seemed more logical if harmonic means of marginal likelihoods were compared (-455638.67, -455391.40, -449073.19 for 61, 4 and 3 partitions, respectively).
In general, our inferred chloroplast phylogenies are very similar to recently published molecular trees, in which the interrelationships and the monophyly of magnoliids, monocots and eudicots were strongly supported [9, 10, 47, 48]. In all the derived phylogenetic trees, Fagopyrum and Spinacia (both represent Caryophyllales sensu lato) form a sister clade to asterids. To determine if alternative topologies with placement of Caryophyllales as a sister group to rosids (AT1) or to rosids and asterids (AT2) can be distinguished, a Shimodaira-Hasegawa test  was conducted and expected-likelihood weights  were calculated using RELL optimization . According to the results of these tests, the alternative placement of Caryophyllales is significantly worse than the optimal topology, supporting a close relationship of Caryophyllales and asterids (p < 0.001, c<0.001 for both AT1 and AT2).
A clade of rosids, with grape being basal among them, is sister to asterids and Caryophyllales. Notably in our dataset inclusion of Morus sequence leads to stabilization of Cucumis position and in all our analyses the eurosids I are monophyletic. In the most recently published phylogenetic trees based on chloroplast sequences, the placement of Cucumis was unstable. It either united with Myrtaceae (Eucalyptus, Oenothera) in the bayesian trees or nested within eurosids I in the MP trees [9, 47, 52]. A close relationship of Morus and Cucumis has been demonstrated previously  and in our Bayesian trees these species form a cluster with a high posterior probability value. Such grouping is questionable based on our MP analysis and a previously reported analysis of 64 plastid genomes  that place them as a grade. However, it is obvious that eurosids I may be considered monophyletic.
Ranunculus and Nandina appear to constitute the basal most clade within eudicots. Buxus is the closest ally to core eudicots in all the derived trees, whereas the position of Platanus among basal eudicots cannot be firmly determined. Its intermediate position is not supported in the MP analysis with bootstrap resampling of amino acid sequences.
Amborella, Nymphaeales, Chloranthales and magnoliids remain the most problematic groups in angiosperm phylogeny. Their phylogenetic relationships are still equivocal and are dependent on the method and data used during analyses. None of the alternative hypotheses concerning Amborella (a sister to Nymphaeales or to all other angiosperms) and Chloranthus (a sister to magnoliids only or to magnoliids, monocots and eudicots) can be rejected on the basis of phylogenetic analysis of the chloroplast genome sequences [9, 10]. Obviously, limited taxon sampling is the first weakness of the chloroplast phylogeny analyses at the current stage, therefore the problem cannot be resolved until additional representatives from basal angiosperms and gymnosperms are included in the analyses to obtain robust relationships. The same holds true for monocots and eudicots as long as many important lineages are missing. One should not be deluded by high bootstrap or posterior probability values, because high support for a doubtful clade is often obtained when a very large number of characters (like whole chloroplast genome sequences) but small number of taxa are used in phylogenetic analysis. For example, Calycanthus in some trees was placed as a sister to eudicots with high or moderate support [53–57] until additional magnoliids were included in the analyses . To overcome the issue of taxon sampling, it is worth identifying genes that are most efficient for phylogenetic analysis and then to analyze these genes in more taxa. Recently RPO genes, coding for plastid RNA-polymerase subunits, have been shown to generate the topology of a phylogenetic tree similar to the whole plastid genomes phylogeny . Another example is the use of slowly evolving genes encoded in the chloroplast inverted repeat region that have helped to resolve phylogenetic relationships within Saxifragales .
Distribution of ACG initiation codon in rpl2, psbL and ndhD genes in angiosperms in the phylogenetic context
Several chloroplast genes in angiosperm plastomes are known to possess an atypical initiation codon ACG. For some species (tobacco, snapdragon, spinach, maize) there is strong experimental evidence that this codon is edited to the standard AUG codon [30, 31, 59] suggesting that similar mechanism may exist in other species. Since RNA editing patterns are thought to be the subjects of extensive parallel evolution, they are not necessarily phylogenetically informative . However, for three plastid genes – rpl2, psbL and ndhD – a correlation between RNA editing and phylogeny has been reported . This study was based on sequences from 7 angiosperms plastomes; it was concluded that RNA editing in psbL gene emerged in a common ancestor of angiosperms that was then lost in monocots. Editing of rpl2 gene emerged only in monocots and for ndhD gene it was observed only in dicots .
The availability of a large number of complete chloroplast genome sequences from angiosperms and improved knowledge about flowering plant phylogeny allows re-evaluation of this conclusion. We performed a survey of the potential RNA editing sites in the initiation codons of rpl2, psbL and ndhD in 44 seed plant chloroplast genomes sequenced till date (including Fagopyrum) and studied its distribution in different evolutionary lineages using phylogenetic trees reported in this article as a framework (Additional file 5). Foremost, our analyses indicate that among seed plants the ACG initiation codon in rpl2 gene is not only a characteristic of monocots, but also of some early divergent angiosperms (Amborella, Chloranthus and magnoliids) and lower eudicots (Ranunculales and Platanus). However, it is absent in Illicium and Nymphaeales that are also the representatives of basal lineages of angiosperms. Thus, it is difficult to conclude that the RNA editing at this site emerged in a common ancestor of angiosperms and then was lost in Illicium and Nymphaeales. Alternatively, it may have evolved later, after the divergence of the members of ANITA grade and its occurrence in Amborella may be due to parallel evolution. The editing in ndhD gene seemed to have evolved in a common ancestor of angiosperms and then lost in Nymphaea and in some monocots. In all the grasses studied till date ndhD gene has a standard ATG initiation codon [62–65] suggesting that it may be common for all the members of this family. The pattern of distribution of the ACG initiation codon in psbL gene is more complex. Its presence is characteristic for most of the early divergent angiosperms (except for Chloranthus and Calycanthus), but absent in all sampled monocots and in several different lineages of eudicots. We assume that the presence of the ACG initiation codon (and, presumably, RNA editing) in this gene is an ancestral character state for angiosperms and its absence is due to multiple parallel losses. However this observation needs to be verified further using broader taxon sampling.
Complete sequence of buckwheat (Fagopyrum esculentum ssp. ancestrale) chloroplast DNA has been generated using a PCR based approach validating the utility of this approach especially for non-rearranged angiosperm chloroplast genomes. This represents the first sequenced plastid genome of the family Polygonaceae and of non-core Caryophyllales. Gene content and order of buckwheat plastome is similar to that of Spinacia oleracea, its relative from core Caryophyllales. However two structural differences have been revealed. First of them is the presence of an intron in rpl2 gene and the second is the expansion of inverted repeat region. The exact structure of the expanded region is different from previously reported data and includes an intact ORF for the ycf1 gene.
Phylogenetic analysis of 61 protein-coding genes in 44 taxa, including newly obtained chloroplast genome sequence (Fagopyrum) provides strong support for the sister relationships of Caryophyllales sensu lato (including Polygonaceae) and asterids. Most of other conclusions from previous phylogenetic studies of chloroplast genomes are also confirmed, in particular the placement of Amborella (or Amborella + Nymphaeales) as a basalmost angiosperm, sister relationships of Chloranthus and magnoliids and the position of Ranunculales (Ranunculus + Nandina) as the earliest diverging lineage of eudicots.
The study of distribution of the potential RNA editing sites in the initiation codon of rpl2, psbL and ndhD genes in angiosperms reveals some correlations with the phylogeny though confirms that the evolution of RNA editing is a subject of extensive parallel changes.
Angiosperm phylogeny group
Amplification, sequencing, annotation of plastomes
Dual organellar genome annotator
large single copy
Open reading frame
Polymerase chain reaction
small single copy
This study was supported by Russian Foundation for Basic Research (project No06-04-96315 for MDL and AAP), Program for Support of Leading Scientific Schools (project No 140.2008.4 for AAP and 1275.2008.4 for MDL and MK-920.2007.4 for AAP. The authors are grateful to A.N. Fesenko (All Russia Scientific Research Institute of Legumes and Groat Crops, Orel, Russia) for providing seeds of Fagopyrum species, S. V. Kuptsov (Moscow State University Botanical garden, Moscow, Russia) for providing plant material of other Polygonaceae, N. V. Ravin (Centre ≪Bioengineering≫ RAS, Moscow, Russia) for sharing data on Lemna minor chloroplast genome sequence prior its publication and to A. B. Shipunov (Idaho State University, Moscow, Idaho, USA) for helpful comments on the initial draft.
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