Complete nucleotide sequence of the Cryptomeria japonicaD. Don. chloroplast genome and comparative chloroplast genomics: diversified genomic structure of coniferous species
© Hirao et al; licensee BioMed Central Ltd. 2008
Received: 23 January 2008
Accepted: 23 June 2008
Published: 23 June 2008
The recent determination of complete chloroplast (cp) genomic sequences of various plant species has enabled numerous comparative analyses as well as advances in plant and genome evolutionary studies. In angiosperms, the complete cp genome sequences of about 70 species have been determined, whereas those of only three gymnosperm species, Cycas taitungensis, Pinus thunbergii, and Pinus koraiensis have been established. The lack of information regarding the gene content and genomic structure of gymnosperm cp genomes may severely hamper further progress of plant and cp genome evolutionary studies. To address this need, we report here the complete nucleotide sequence of the cp genome of Cryptomeria japonica, the first in the Cupressaceae sensu lato of gymnosperms, and provide a comparative analysis of their gene content and genomic structure that illustrates the unique genomic features of gymnosperms.
The C. japonica cp genome is 131,810 bp in length, with 112 single copy genes and two duplicated (trnI-CAU, trnQ-UUG) genes that give a total of 116 genes. Compared to other land plant cp genomes, the C. japonica cp has lost one of the relevant large inverted repeats (IRs) found in angiosperms, fern, liverwort, and gymnosperms, such as Cycas and Gingko, and additionally has completely lost its trnR-CCG, partially lost its trnT-GGU, and shows diversification of accD. The genomic structure of the C. japonica cp genome also differs significantly from those of other plant species. For example, we estimate that a minimum of 15 inversions would be required to transform the gene organization of the Pinus thunbergii cp genome into that of C. japonica. In the C. japonica cp genome, direct repeat and inverted repeat sequences are observed at the inversion and translocation endpoints, and these sequences may be associated with the genomic rearrangements.
The observed differences in genomic structure between C. japonica and other land plants, including pines, strongly support the theory that the large IRs stabilize the cp genome. Furthermore, the deleted large IR and the numerous genomic rearrangements that have occurred in the C. japonica cp genome provide new insights into both the evolutionary lineage of coniferous species in gymnosperm and the evolution of the cp genome.
Since the first reports of the complete nucleotide sequences of the tobacco  and liverwort  chloroplast (cp) genomes, a number of other land plant cp genomic sequences have been determined. These complete cp genomic sequences have enabled various comparative analyses, including phylogenetic studies, that are based on these data [3–7]. In contrast, however, the complete cp genome nucleotide sequences of only three gymnosperm species, Cycas taitungensis , Pinus thunbergii , and Pinus koraiensis  have been determined.
The cp genomes of gymnosperms, especially in coniferous species, have distinctive features compared with those of angiosperms, including paternal inheritance [11–17], relatively high levels of intra-specific variation [18–21], and a different pattern of RNA editing . Generally, the cp genomes of angiosperms range in size from 130 to 160 kb, and contain two identical inverted repeats (IRs) that divide the genomes into large (LSC) and small single copy (SSC) regions. The relative sizes of these LSC, SSC and IRs remain constant, with both gene content and gene order being highly conserved [23, 24]. On the other hand, the relative sizes of the gymnosperm IRs vary significantly among taxa [25–27]; for example, the IRs of Ginkgo biloba are 17 kbp , those of Cycas taitungensis are 23 kbp , whereas those of Pinus thunbergii are very short, at just 495 bp [9, 29]. It has been suggested that, like P. thunbergii, some coniferous species also lack the large IRs that exist in other gymnosperms [25, 26, 30, 31]. This lack of IRs is considered to have preceded the extensive genomic rearrangements of the conifer cp genome . Steane  compared the complete cp genome of Eucalyptus globulus with that of other angiosperm taxa and P. thunbergii, and found that the cp genome of P. thunbergii was arranged very differently to that of angiosperms. However, there is only limited information available about the cp genomic sequences of coniferous species, with the complete cp genome nucleotide sequences of only two species of pine, Pinus thunbergii  and Pinus koraiensis  in the family Pinaceae, having been determined. The cp genomes of these two pine species were very similar in terms of both gene content and gene order and so provided little information about the complexity of the conifer cp genome.
In previous phylogenetic studies, of the four extant gymnosperm groups (Cycads, Conifers, Ginkgoales, and Gnetales), the conifers were considered to be divisible into two distinct groups; a Pinaceae group and a group consisting of five other families (Cupressaceae sensu lato, Taxaceae, Podocarpaceae, Araucariaceae, and Sciadopityaceae) [33, 34]. The cp nucleotide sequences from this five member group, excluding the Pinaceae group, can provide interesting information about the conifer cp genome, not only in terms of genome structure but also concerning their evolutionary history. Despite the lack of complete cp genome sequences from any family member of the Cupressaceae sensu lato, Tsumura et al.  suggested, on the basis of physical maps and Southern hybridization analyses, that the cp genome of Cryptomeria japonica differs from that of other land plants, including pine species, in terms of genome size and gene order as well as in the absence of the large IRs. Thus, the complete cp genome sequence of C. japonica would drastically increase our understanding of the divergence of coniferous cp genome structures and gene content, and additionally clearly identify the differences with the Pinaceae group.
There are two particular questions that need to be addressed using the complete cp genome sequence of C. japonica: (1) how different is the C. japonica cp genome from those of other plants, including gymnosperms, and (2) is the loss of the large IRs involved with the instability and diversification of the cp genome, especially between coniferous groups? To respond to these questions, we present in this paper the complete nucleotide sequence of the cp genome of C. japonica [DDBJ: AP009377], and compare its overall gene content and genomic structure with those of two other angiosperms (Eucalyptus globulus and Oryza sativa), a liverwort (Marchantia polymorpha), a fern (Adiantum capillus), and two gymnosperms (Cycas taitungensis and Pinus thunbergii).
Results and Discussion
General characteristics of the C. japonicacp genome
List of genes found in C. japonica chloroplast genome (see Figure 1)
Category for genes
Group of gene
Name of gene
Ribosomal RNA genes
Transfer RNA genes
trn A-UGC *
trn G-UCC *
trn I-CAU × 2
trn I-GAU *
trn K-UUU *
trn L-UAA *
trn Q-UUG × 2
trn V-UAC *
Small subunit of ribosome
rps 16 *
Large subunit of ribosome
rpl 2 *
rpl 16 *
DNA dependent RNA polymerase
rpo C1 *
Translational initiation factor
Genes for photosynthesis
Subunits of photosystem I
Subunits of photosystem II
Subunits of Cytochrome
pet B *
pet D *
Subunits of ATP synthase
atp F *
Large subunit of Rubisco
Subunits of NADH dehydrogenase
ndh B *
Envelop membrane protein
Subunit of Acetyl-CoA-carboxylase
c-type cytochrome synthesis gene
Genes of Unknown function
Conserved Open Reading Frames
ycf 3 *
A marked difference in gene content between gymnosperms including C. japonica
There are marked differences in several genes between gymnosperms, even though the C. japonica cp genome shares several common features with other plants, and some of these are described below. For example, there is considerable difference in gene content between C. japonica and P. thunbergii; the 11 intact ndh (NADH dehydrogenase) genes found in C. japonica, as well as in five other plants, are absent from P. thunbergii . The loss of these ndh genes is thought to be due to specific mutations in the Pinus cp genome.
The trnP-GGG and trnR-CCG genes are considered to be pseudogenes, possibly relics of plastid genome evolution in gymnosperms and moss [22, 42, 43]. The trnP-GGG gene is found in C. japonica, as well as in the two gymnosperms, P. thunbergii and C. taitungensis, in the liverwort, M. polymorpha, and in the fern, A. capillus, but not in angiosperm cp genomes. The gene is also found in Gnetum and Ginkgo of gymnosperms , suggesting that this is a relic gene in a large number of gymnosperms. In contrast, the trnR-CCG gene, which is found in P. thunbergii, C. taitungensis, M. polymorpha, and A. capillus, is absent from the C. japonica and angiosperm cp genomes, suggesting that trnR-CCG is not conserved in all gymnosperm cp genomes and might have been completely lost in taxa, such as Cupressaceae sensu lato, that have relatively recently diverged during the long evolutionary history of plants.
Diversification of genes in the C. japonicacp genome
Loss of large IR region within coniferous cp genomes
Structural differences between cp genomes of C. japonicaand other land plants
Minimum rearrangements via inversions in pairwise comparisons of seven chloroplast genomes
one gene inversion**
loss of a large IR
C. japonica vs P. thunbergii
C. japonica vs C. taitungensis
C. japonica vs A. capillus
C. japonica vs M. polymorpha
C. japonica vs E. globulus
C. japonica vs O. sativa
P. thunbergii vs C. taitungensis
P. thunbergii vs A. capillus
P. thunbergii vs M. polymorpha
P. thunbergii vs E. globulus
P. thunbergii vs O. sativa
C. taitungensis vs A. capillus
C. taitungensis vs M. polymorpha
C. taitungensis vs E. globulus
C. taitungensis vs O. sativa
A. capillus vs M. polymorpha
A. capillus vs E. globulus
A. capillus vs O. sativa
M. polymorpha vs E. globulus
M. polymorpha vs O. sativa
E. globulus vs O. sativa
The large IR is thought to stabilize the cp genome against major structural rearrangements [53–55]. Among angiosperm species, structural changes in the cp genome have occurred within tribes of the legume family (Fabaceae), which have also lost their IR, and so it appears that most genomes that have lost their IRs have undergone more rearrangements than those that have not [53, 56]. With respect to other conifers, it has been shown that Douglas fir (Pseudotsuga menziesii) and radiata pine (Pinus radiata) lack the large IR, and that both of these conifer genomes have undergone a greater number of rearrangements relative to ferns, angiosperms, and even Ginkgo, a gymnosperm . The differences in genome structure between C. japonica and other land plants, including pines, strongly confirms that the presence of large IRs plays a role in the structural stability of the cp genome.
Tsumura et al.  suggested that the cp genome structure of C. japonica differs significantly from that of pine species, implying that independent changes have occurred and that no simple evolutionary path can be determined. In fact, phylogenetic studies have revealed the significant divergence of Coniferales [33, 34], with a phylogenetic tree using the rbcL gene in one of these studies indicating that C. japonica (Cupressaceae sensu lato) and pine species (Pinaceae) are not very closely related and are in fact located in different clade (additional file 2 in this study). In a study of 18 Campanulaceae species, Cosner et al.  suggested that data regarding cp genome rearrangements were useful for inferring phylogenetic relationships, and actually found that the results of analysis using gene order closely paralleled the results of phylogenetic analysis using Internal Transcribed Spacer (ITS) and rbcL sequence data. Hence, data on rearrangements in the conifer cp genome might reflect phylogenetic relationships and serve as a new evolutionary-related parameter. Furthermore, insights obtained from these studies will provide a clearer detail of the process of cp genome evolution. However, in order to better understand the complex changes in the cp genome structure that have occurred during the long process of evolution, data on the cp genomes of other coniferous taxa, such as Taxaceae, Sciadopityaceae, Podocarpaceae, and Araucariaceae will be required.
The vestiges of genome rearrangement within the C. japonicacp genome
Within the large inversion from trnT-UGU to trnQ-UUG, we found another vestige of the genome rearrangement. As mentioned above, the incomplete loss of trnT-GGU (halfway between trnE-UUC and psbD in the C. japonica cp genome, Figure 9) from the C. japonica cp genome may have been the result of genome rearrangement. In grasses, such as O. sativa, it has been suggested that rearrangements in the region surrounding trnT-GGU were derived from two independent inversions [49, 61, 62]. In the A. capillus cp genome, the segment from trnT-GGU to trnG-GCC is inverted when compared to that of E. globulus. In the P. thunbergii cp genome, a translocation and inversion event occurred at the segment from trnT-GGU to the pseudogene ndhC (as indicated within gene segment I in additional file 1B). It is worth noting that trnT-GGU is located at the borders of the sites of the genome rearrangements. Although the rearrangement associated with trnT-GGU was not found in the C. japonica cp genome when compared to that of E. globulus, the incomplete loss of trnT-GGU in the C. japonica cp genome suggests the possibility of a re-inversion event.
This study has revealed that the coniferous species, C. japonica, has a distinct cp genome compared to previously reported land plant cp genomes. In terms of gene content, several genes in the C. japonica cp genome differ significantly, having either been lost or diverged, from those of other land plants, while the gene order and genome structure also differ significantly. The deleted large IRs and the numerous genome rearrangements that have occurred in the C. japonica cp genome have provided new insights into the evolutionary lineage of conifers. However, as the complete cp genome nucleotide sequences of only three conifer species that belong to two distinct genera have been determined, our present results will certainly advance our understanding of the complex evolutionary history of the coniferous cp genome.
Isolation of chloroplast DNA
Open-pollinated C. japonica seeds were collected from several clones, and were germinated and grown for 1 month in a greenhouse. C. japonica chloroplasts were isolated from the needle tissues of these seedlings using the sucrose density gradient method . The chloroplast pellet was resuspended in 250 ml of Kool's buffer A (50 mM Tris-HCl, pH 8.0, 0.35 M sucrose, 7 mM EDTA, 5 mM 2-mercaptoethanol) containing 0.1% bovine serum albumin, and the suspension was filtered through layers of cheesecloth and Miracloth (Calbiochem; without squeezing). The filtrate was centrifuged, and the resulting green pellet was resuspended in 2.5 ml of Kool's buffer A. This second suspension was then loaded onto a stepwise 20–45–55% sucrose gradient in 50 mM Tris-HCl, pH 8.0, 0.3 M sorbitol, 7 mM EDTA, and centrifuged for 30 min. The green band at the 20–45% sucrose interphase was collected, diluted 1:3 with Kool's buffer B (50 mM Tris-HCl, pH 8.0, 20 mM EDTA), centrifuged for 10 min, and the chloroplast pellet then resuspended in Kool's buffer B. The chloroplasts were lysed by adding SDS to a final concentration of 3%. A 1/20th volume of 10 mg/ml pronase E was added to the solution, and the mixture incubated overnight at 37°C. DNA was extracted twice from the lysate with phenol and once with phenol/chloroform/isoamyl alcohol (25:24:1), and the DNA was precipitated with 0.1 volumes of 3 M sodium acetate and 2.5 volumes of ethanol. The precipitate was washed twice with 70% ethanol and dissolved in water. The extracted DNAs were further purified using the DNeasy Plant Mini Kit (QIAGEN) and treated with ATP-dependent DNase (TOYOBO) to remove linear double- or single-stranded DNA.
Chloroplast DNA sequencing and genome assembly
The cp DNA isolated was sheared by ultrasonication, and the sheared fragments then blunted and cloned into pBluescript II vector. The cp DNA fragments were shotgun sequenced using the BigDye Terminator Cycle Sequencing v3.1™ Kit with an ABI 3100 Genetic Analyzer (both PE Applied Biosystems). Sequencher 3.1 (Gene Codes Corporation) software was used for sequence analysis and assembly. The sonication-derived cloned fragments were found to cover 80% of the whole genome after contig assembly. Any remaining sequence gaps were amplified by PCR and sequenced directly from the amplification products.
The cp genome of C. Japonica was annotated using DOGMA [Dual Organellar GenoMe Annotator, 64] after a FASTA-formatted file of the complete cp genome was uploaded to the program's server. Gene annotation and comparative genome analyses (BLASTN, BLASTX) were performed against a custom database of 11 previously published cp genomes using default parameters of 60% for protein coding genes and 85% for tRNAs and rRNAs. For genes with low amino acid sequence identity, manual annotation was performed using a percentage identity threshold of 25–50%. The fully annotated cp genome of Cryptomeria japonica was submitted to DDBJ GenBank with the following accession number [DDBJ: AP009377].
Exploration of the differences in gene contents and diversified genes
Exploration of the differences in gene contents and diversified genes between the C. japonica cp genome and the six previously published cp genomes was performed using PipMaker . The six cp genomes compared are as follows: the dicot angiosperm, E. globulus (Myrtaceae, 160,286 bp, AY780259); the monocot angiosperm, O. sativa (Poaceae, 134,525 bp, X15901); the liverwort, M. polymorpha (Marchantiaceae, 121,024 bp, NC001319); the fern, A. capillus (Pteridaceae, 150,568 bp, AY178864); and the two gymnosperms, C. taitungensis (Cycadaceae, 163,403 bp, AP009339) and P. thunbergii (Pinaceae, 119,707 bp, D17510). The variable genes identified within the C. japonica cp genome by gene annotations were aligned with the corresponding coding genes of the six land plant cp genomes using ClustalX  followed by screening for nucleotide and amino acid sequence differences.
Comparative analysis of genome structure
Comparative analysis of the genome structure of the seven cp genomes, including that of the C. japonica cp genome, was performed using the Harr-plot analysis of PipMaker . For estimates of genome rearrangement, the GRIMM web server  was used to identify the minimum number of rearrangements by inversion in pairwise comparisons of the cp genome. GRIMM cannot deal with duplicated genes and requires that the genomes that are compared have the same gene content, so that one of the two IR copies and their genes were arbitrarily excluded.
Examination of dispersed repeat sequences
FASTPCR software  was used to locate and count the direct (forward) and inverted (palindromic) repeats within the C. japonica cp genome. The identification of repeat sequences was assessed with the following parameters: options at a minimum length of 50 bp and 90% or greater sequence identity.
Phylogenetic analysis using the rbcL gene of chloroplast genome
Based on the rbcL gene sequence of the C. japonica cp genome, the rbcL gene nucleotide sequences of 132 gymnosperm species and eight out-group species were obtained by a FASTA search of GenBank. The DNA sequences were aligned using ClustalX , with excluded gap regions. Phylogenetic analysis using the neighbor-joining (NJ) method was performed using ClustalW from the DDBJ web server . The Kimura-2-parameter model of molecular evolution was used in the NJ method of the nucleotide sequences. Bootstrap analysis was performed for the NJ method with 100 replicates.
- cp genome:
small single copy
large single copy
hypothetical chloroplast reading frame
We thank Dr. Yasukazu Nakamura at Kazusa DNA Research Institute for helpful advice on the annotation of the cp genome, and Dr. Shohab Youssefian at Akita Prefectural University for helpful discussions, comments and advice.
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