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Article

Complete Chloroplast Genome Sequence and Phylogenetic Analysis of Aster tataricus

by
Xiaofeng Shen
1,†,
Shuai Guo
2,†,
Yu Yin
3,
Jingjing Zhang
4,
Xianmei Yin
5,
Conglian Liang
6,
Zhangwei Wang
7,
Bingfeng Huang
7,
Yanhong Liu
7,
Shuiming Xiao
1,8,* and
Guangwei Zhu
1,8,*
1
Artemisinin Research Center, Institute of Chinese Materia Medical, China Academy of Chinese Medical Sciences, Beijing 100700, China
2
College of Agricultural (College of Tree Peony), Henan University of Science and Technology, Luoyang 471023, China
3
School of Computer Science and Technology, Shandong University, Jinan 250101, China
4
College of Pharmacy, Hubei University of Chinese Medicine, Wuhan 430065, China
5
College Pharmacy, Chengdu University of Chinese Medicine, Chengdu 611137, China
6
College of Pharmacy, Shandong University of Traditional Chinese Medicine, Jinan 250355, China
7
State Key Laboratory of Innovative Natural Medicine and TCM Injections, Ganzhou 341000, China
8
State Key Laboratory of Innovative Natural Medicine and TCM Injections, Jiangxi qingfeng pharmaceutical co. LTD, Ganzhou 341000, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Molecules 2018, 23(10), 2426; https://doi.org/10.3390/molecules23102426
Submission received: 17 August 2018 / Revised: 17 September 2018 / Accepted: 19 September 2018 / Published: 21 September 2018
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Abstract

:
We sequenced and analyzed the complete chloroplast genome of Aster tataricus (family Asteraceae), a Chinese herb used medicinally to relieve coughs and reduce sputum. The A. tataricus chloroplast genome was 152,992 bp in size, and harbored a pair of inverted repeat regions (IRa and IRb, each 24,850 bp) divided into a large single-copy (LSC, 84,698 bp) and a small single-copy (SSC, 18,250 bp) region. Our annotation revealed that the A. tataricus chloroplast genome contained 115 genes, including 81 protein-coding genes, 4 ribosomal RNA genes, and 30 transfer RNA genes. In addition, 70 simple sequence repeats (SSRs) were detected in the A. tataricus chloroplast genome, including mononucleotides (36), dinucleotides (1), trinucleotides (23), tetranucleotides (1), pentanucleotides (8), and hexanucleotides (1). Comparative chloroplast genome analysis of three Aster species indicated that a higher similarity was preserved in the IR regions than in the LSC and SSC regions, and that the differences in the degree of preservation were slighter between A. tataricus and A. altaicus than between A. tataricus and A. spathulifolius. Phylogenetic analysis revealed that A. tataricus was more closely related to A. altaicus than to A. spathulifolius. Our findings offer valuable information for future research on Aster species identification and selective breeding.

1. Introduction

Aster tataricus is a tall perennial herb of the genus Aster (family Asteraceae). It has been used as a therapeutic traditional medicine for eliminating phlegm and relieving cough for thousands of years [1,2], and cultivated as a high-value medicinal plant. A number of bioactive compounds have been isolated from A. tataricus, such as shionone, epifriedelinol, quercetin, emodin, caffeoylquinic acid, kaempferol, and some other triterpenes or saponins [3,4]. Modern pharmacological studies [5,6,7] have shown that A. tataricus exhibits diverse pharmacological effects, including antibacterial, antiviral, antitumor, and diuretic activities; consequently, it is recorded as a basic clinical herb in the Chinese Pharmacopoeia. Furthermore, as a late-blooming aster, A. tataricus is an appealing ornamental plant in some East Asian countries. However, genomic research on A. tataricus—both nuclear genome sequencing and plastid genome sequencing—has been relatively scarce. This lack of genetic information has hindered the basic research into, and applications of, this valuable plant, such as molecular authentication, breeding, cultivation, and bioactive compound biosynthesis.
The chloroplast, the photosynthetic organelle of most green plants, is involved in both developmental processes and secondary metabolic activities [8], as well as coordination of gene expression between organelle and nuclear genome [9]. The chloroplast (cp) genome is considered to have originated from an ancestral endosymbiotic cyanobacteria [10] and is organized into large clusters of polycistronic transcribed genes [11]. Therefore, it has a highly conserved tetrad structure, with a large single-copy (LSC) region, a small single-copy (SSC) region, and two inverse repeats (IRs) regions. As conserved matrilineal genetic information, chloroplasts play a part in cytoplasmic male sterility (CMS) [12], genetic diversity in populations [13,14,15], and especially, phylogenetic analysis [16,17]. In addition, the comparison of chloroplast sequences has been successfully used to study the evolution [18] and athentication markers to molecular identification at genus levels [19]. Evolutionary events, such as IR contraction and expansion, and re-inversion of SSC, have been found in the comparison of chloroplast genome [20,21]. Moreover, the chloroplast DNA sequences offers adequate information to study the phylogenetics and phylogeography of angiosperms at lower taxonomic levels [8]. In past decades, there have been great advances in our understanding of chloroplasts [22,23,24,25], in terms of their origin, structure, evolution, forward and reverse genetics, and genetic engineering. Moreover, the emergence of second-generation sequencing technology means that there is now less demand for research into chloroplast genomics [26,27]. Therefore, a draft cp genome assembly for A. tataricus is of great significance for exploring molecular identification, phylogenetic relationships, and evolutionary events studies among Asteraceae species.
Here, we reported the first whole chloroplast genome sequence for A. tataricus, together with the characterization of its gene annotations and repeat compositions. We also compared this chloroplast genome with that of other Aster species, which revealed significant variation in genome size and highly divergent regions in intergenic spacers. This comprehensive cp genomic analysis would provide a basis for molecular identification and further understanding of the evolutionary history of Aster species.

2. Results and Discussion

2.1. Features of A. tataricus cpDNA

The complete cp genome sequence of A. tataricus was 152,992 bp (GenBank accession number MH669275). The structure of the A. tataricus cp genome was analogous to those from other Aster species [28], and included an LSC region (84,698 bp; covering 55.4%), an SSC region (18,250 bp; covering 11.9%), and a pair of inverted repeats (IRA/IRB, 25,022 bp; covering 16.4%) (Table 1). The content of DNA G + C in the LSC, SSC, and IR regions, and the whole genome, was 35.2%, 31.3%, 43%, and 37.3%, respectively. The DNA G + C content is a very significant indicator when evaluating species affinity, and the cpDNA G + C content of A. tataricus is identical to that of other Aster species [28]. The DNA G + C content of the IR regions in A. tataricus was greater than that of other regions (LSC, SSC); this phenomenon is very common in other plants too [16,17]. The relatively high DNA G + C content of the IR regions is generally attributable to the rRNA genes and tRNA genes [29,30,31].
In the A. tataricus cp genome, 115 functional genes were observed, including four rRNA genes, 30 tRNA genes, and 81 protein-coding genes (Table 2). Furthermore, 18 genes—seven tRNA, all four rRNA, and seven protein-coding genes—were repeated in the IR regions (Figure 1). The LSC region contained 62 protein-coding and 22 tRNA genes, while the SSC region comprised one tRNA gene and 12 protein-coding genes.
The sequences of the tRNA and protein-coding genes were studied, and the frequency of codon usage was inferred and summarized for the A. tataricus chloroplast genome. Our study revealed that 23,441 codons characterize the coding capacity of 81 protein-coding and 30 tRNA genes in A. tataricus (Table 3). Of these codons, 4065 (17.34%) were found to code for leucine and 204 (0.87%) for tryptophan, which represented the maximum and minimum prevalent number of amino acids in the A. tataricus chloroplast genome, respectively. A- and U-ending codons were ordinary.
There were 18 intron-containing genes in total: 12 protein-coding genes and six tRNA genes (Table 4). Fifteen genes (nine protein-coding and six tRNA genes) comprised one intron, and two genes (ycf3 and clpP) comprised two introns (Table 4). The intron of the trnK-UUU gene contains the matK gene, and the size of the intron was 2497 bp. The rps12 gene was a trans-spliced gene, with the 5′ end located in the LSC region and the copied 3′ end located in the IR regions. Earlier studies have reported that ycf3 is essential for the constant accumulation of the photosystem I compound [32]. Therefore, we suppose that the intron gain in ycf3 of A. tataricus may be valuable information in terms of further studies of the mechanism of photosynthesis evolution. We compared the length of exons and introns in genes with introns in the A. tataricus and A. spathulifolius chloroplast genomes (Table 4). While these were found to be broadly similar, some differences were noted: (1) in the A. spathulifolius chloroplast genome, the rpl16 gene had no intron; (2) there was significant variation in rps12 and rps16 intron length between the two species; and (3) in A. spathulifolius, the rpl12 gene had no intron.
Advances in phylogenetic research have revealed that chloroplast genome evolution encompasses both structural changes and nucleotide substitutions [33,34,35]. A few examples of these changes, including intron or gene losses [21,36], have been discovered in chloroplast genomes. Introns play an important role in regulating gene expression. They can increase gene expression at a particular position and at a specific time [37]. Intron regulation mechanisms have been reported in other species. More experimental work is required to study the relationship between intron loss and gene expression introns in A. tataricus.

2.2. Simple Sequence Repeat (SSR) Analysis

Simple sequence repeats (SSRs) of 10 bp or longer are inclined toward slipped-strand mispairing, which is known to be the main mutational mechanism utilized in SSR polymorphisms. SSRs in the chloroplast genome can be extremely variable at the intra-specific level and are often used as genetic markers in population genetics and evolutionary studies [38,39,40,41]. In this research, we investigated the SSRs in the chloroplast genome of A. tataricus and in that of two other Aster species (Figure 2). The cp genome of Aster tataricus, Aster altaicus, and Aster spathulifolius contained 70, 58, and 36 SSRs, respectively. The level of mononucleotide repeat content was high (A. tataricus, 51.4%; A. altaicus, 62.1%; A. spathulifolius, 77.8%) in all the above species. These results will provide chloroplast SSR markers that can be used to study genetics, select germplasm for breeding, and facilitate the molecular identification of species.

2.3. Comparative Chloroplast Genomic Analysis

Comparative analysis of genomes is a tremendously important step in genomics [42,43]. Comparing the structural changes amongst Aster chloroplast genomes revealed that the chloroplast genome A. spathulifolius was the smallest of the three whole Aster chloroplast genomes (Table 1). A. spathulifolius had the fewest IR regions (17,973 bp) among these sequenced Aster chloroplast genomes. We supposed that the dissimilar length of the IR regions was the principal reason for the change in sequence length. To explicate the level of genome differences, the sequence identity of the Aster chloroplast DNAs was computed using mVISTA software, with A. tataricus as a reference (Figure 3). The results of this comparison showed that the IR (A/B) regions exhibited fewer differences than the LSC and SSC regions. Moreover, the non-coding regions showed more variability than the coding regions, and the marked differences in regions among the three chloroplast genomes were evident in the intergenic spacers. Of the three Aster chloroplast genomes, A. tataricus and A. altaicus exhibited the fewest differences.

2.4. Inverted Repeat (IR) Contraction and Expansion in the A. tataricus Chloroplast Genome

Contractions and expansions of the IR regions at the borders are ordinary evolutionary events and represent the main reasons for changes in the size of chloroplast genomes; they play a significant role in evolution [44,45,46]. For A. altaicus, A. spathulifolius and A. tataricus, we conducted an exhaustive comparison of four junctions, LSC-IRA (JLA), LSC-IRB (JLB), SSC-IRA (JSA), and SSC-IRB (JSB), between the two IRs (IRA and IRB) and the two single-copy regions (LSC and SSC) (Figure 4). The JSA junction was placed in the ycf1 pseudogene region in all the Aster species chloroplast genomes and outspread to different lengths (A. altaicus, 563 bp; A. spathulifolius, 608 bp; A. tataricus, 563 bp) within the IRA region of all the genomes; the IRB region contained 563, 567, and 565 bp of the ycf1 gene, respectively. Recently, it was reported that ycf1 is required for plant viability and codes Tic214, a significant component of the ArabidopsisTic complex member [47,48]. Correspondingly, the trnH gene was placed in the LSC region, 3, 22, and 3 bp away from the IRB/LSC border in the three Aster chloroplast genomes, respectively. The JLA in the Aster species was overlapped by rps19. The ndhF gene was found to be 22, 5, and 22 bp away from the IRA/SSC border in the Aster species.
Although the gene order in chloroplasts is generally conserved in most green plants, it has been reported that many sequences are rearranged in chloroplast genomes from an extensive variety of different plant species, including inversions in the LSC region, IR contractions or expansions with inversions, and re-inversion in the SSC region [49,50,51,52,53]. Sequence rearrangements that convert chloroplast genome structure in related species may also reveal information about genetic diversity that could be used for molecular classification and evolution studies.

2.5. Phylogenetic Analysis

The availability of a completed A. tataricus cp genome provided us with sequence information that can be used to study the phylogeny of A. tataricus among Asteraceae. We performed multiple sequence alignments using the whole cp genome sequences in 16 Asteraceae species. One additional cp genome, Paeonia ostii (Paeoniaceae), was included as an outgroup (Figure 5). The method of maximum likelihood (ML) was used to construct a phylogenetic tree. The results strongly supported the finding that A. altaicus and A. tataricus are sister species, and A. tataricus is closer to A. altaicus than to A. spathulifolius.

3. Materials and Methods

3.1. DNA Sequencing, Chloroplast Genome Assembly, and Validation

The A. tataricus was planted in the China Academy of Chinese Medical Sciences (N 39°56′, E 116°25′, Beijing, China). Fresh leaves were gathered and covered with tin foil, frozen in liquid nitrogen, and maintained at −80 °C. An improved cetyltrimethylammonium bromide (CTAB) method was used to obtain the whole genomic DNA of A. tataricus [54]. The concentration of DNA was estimated using an ND-2000 spectrometer (Nanodrop Technologies, Wilmington, DE, USA) [55]. A 250-bp shotgun library was constructed according to the manufacturer’s instructions (Vazyme Biotech Co. Ltd., Nanjing, China). The library was sequenced using an Illumina X Ten platform (Illumina, San Diego, CA, USA) double terminal sequencing method (150 pair-ends). The sample contained 5 G of raw data, and over 34 million paired-end reads (SRA accession: SRP154896) were obtained.
The raw data was filtered using Skewer-0.2.2 (Institute of Plant Quarantine Research, Chinese Academy of Inspection and Quarantine, Beijing, China, https://sourceforge.net/projects/skewer/) [56]. BLAST searches were used to abstract chloroplast-like reads from clean-reads in comparison with reference sequences (A. altaicus). Lastly, we used the chloroplast-like reads to assemble sequences using SOAPdenovo-2.04 (BGI·tech, Shenzhen, China, https://sourceforge.net/projects/soapdenovo2/files/SOAPdenovo2/) [57]. SSPACE-3.0 (Leiden University, Leiden, The Netherlands https://www.baseclear.com/services/bioinformatics/basetools/sspace-standard/) [58] and GapCloser-1.12 (BGI·tech, Shenzhen, China, https://sourceforge.net/projects/ oapdenovo2/files/GapCloser/) [59] were used to outspread sequences and fill gaps. PCR amplification and Sanger sequencing were used to confirm the four junction regions between the IR regions and the LSC/SSC regions, to confirm the assembly (Table S1).

3.2. Gene Annotation and Sequence Analyses

CpGAVAS [60] was used to annotate the sequences; DOGMA [61] and BLAST were used to check the annotation findings. tRNAscanSEv1.21 [62], with default settings, was used to identify all tRNA genes. OGDRAWv1.2 [63] was used to show the structural features of the chloroplast genomes. Relative synonymous codon usage (RSCU) values were defined using MEGA5.2 [64].

3.3. Genome Comparison

mVISTA [65] (Shuffle-LAGAN mode) was used to compare the whole chloroplast genome of A. tataricus, A. altaicus (KX352465), and A. spathulifolius (KF279514), with the annotation of A. tataricus as the reference. Phobos version 3.3.12 [66] was employed to detect SSRs within the cp genome, with the search parameters set at 10 repeat units for mononucleotides, _8 repeat units for dinucleotides,_4 repeat units for trinucleotides and tetranucleotides, and _3 repeat units for pentanucleotide and hexanucleotide SSRs.

3.4. Phylogenetic Analysis

We downloaded 16 whole chloroplast genome sequences of Asteraceae species from the National Center for Biotechnology Information (NCBI) Organelle Genome and Nucleotide Resources database. The whole chloroplast genome sequences were used to analyze the phylogenetics. The software clustalw2 (The Conway Institute of Biomolecular and Biomedical Research, Dublin, Ireland) was used to align sequences. MEGA5.2 was used to analyze and plot the phylogenetic tree with ML (maximum likelihood). We used 1000 replicates and TBR (tree bisection and reconnection) branch exchange to complete the bootstrap analysis. Furthermore, Paeonia ostii was set as the outgroup.

4. Conclusions

To our knowledge, we were the first to complete the sequencing and analysis of the whole chloroplast genome of A. tataricus, showing that the quadruple structure, gene order, DNA G + C content, and codon usage features were similar to those of the other Aster chloroplast genomes studied. Compared with the chloroplast genomes of the other two Aster species, the chloroplast genome of A. tataricus was the largest, while the genome structure and composition were found to be similar. Of the three Aster chloroplast genomes, A. tataricus and A. altaicus exhibited the fewest differences. Examination of the phylogenetic relationships among the three Aster species revealed that A. tataricus was more closely related to A. altaicus than to A. spathulifolius. The findings of this study offer an assembly of a whole chloroplast genome of A. tataricus, which would be valuable for molecular identification, breeding, and further biological discoveries.

Supplementary Materials

The following are available online. Table S1. Primers used for assembly validation.

Author Contributions

Data curation, X.S. and S.G.; Formal analysis, S.G. and Z.W.; Investigation, C.L. and X.Y.; Methodology, S.X. and Y.L.; Resources, Y.Y. and J.Z.; Supervision, S.X. and G.Z.; Writing—original draft, X.S.; Writing—review and editing, G.Z. and B.H. All authors read and approved the final manuscript.

Funding

This research was funded by the Major Project of “Research on modernization of traditional Chinese medicine”, grant under 2017YFC1702100; the Open Project of State Key Laboratory of Innovative Natural Medicine and TCM Injections, grant under QFSKL2018004.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Zhao, D.X.; Hu, B.Q.; Zhang, M.; Zhang, C.F.; Xu, X.H. Simultaneous separation and determination of phenolic acids, pentapeptides, and triterpenoid saponins in the root of Aster tataricus by high-performance liquid chromatography coupled with electrospray ionization quadrupole time-of-flight mass spectrometry. J. Sep. Sci. 2015, 38, 571–575. [Google Scholar] [CrossRef] [PubMed]
  2. Yu, P.; Cheng, S.; Xiang, J.; Yu, B.; Zhang, M.; Zhang, C.; Xu, X. Expectorant, antitussive, anti-inflammatory activities and compositional analysis of Aster tataricus. J. Ethnopharmacol. 2015, 164, 328–333. [Google Scholar] [CrossRef] [PubMed]
  3. Fang, H.; Shan, G.; Qin, G.; Zhen, L.N.; Li, M.H.; Hao, J.L. Advances on chemical components and pharmacological actions of Aster tataricus. Med. Res. Educ. 2012, 29, 73–77. [Google Scholar]
  4. Zhou, W.B.; Tao, J.Y.; Xu, H.M.; Tan, N.H. Three new antiviral triterpenes from Aster tataricus. Z. Naturforschung B 2010, 65, 1393–1396. [Google Scholar] [CrossRef]
  5. Tang, X.W.; Liu, X.X.; Tang, Y.L.; Liu, Y.L.; Xu, K.H. Analysis of effective constituents from Aster tataricus L. and extracting of alkaloid and its antibacterial test in vitro. J. Tradit. Chin. Vet. Med. 2006, 1, 16–18. [Google Scholar]
  6. Du, L.; Mei, H.F.; Yin, X.; Xing, Y.Q. Delayed growth of glioma by a polysaccharide from Aster tataricus, involve upregulation of Bax/Bcl-2 ratio, activation of caspase-3/8/9, and downregulation of the Akt. Tumour Biol. 2014, 35, 1819–1825. [Google Scholar] [CrossRef] [PubMed]
  7. Morita, H.; Nagashima, S.; Takeya, K.; Itokawa, H. Solution forms of antitumor cyclic pentapeptides with 3,4-dichlorinated proline residues, astins a and c, from Aster tataricus. Chem. Pharm. Bull. 1995, 43, 1395–1397. [Google Scholar] [CrossRef] [PubMed]
  8. Wicke, S.; Schneeweiss, G.M.; Depamphilis, C.W.; Kai, F.M.; Quandt, D. The evolution of the plastid chromosome in land plants: Gene content, gene order, gene function. Plant Mol. Biol. 2011, 76, 273–297. [Google Scholar] [CrossRef] [PubMed]
  9. Woodson, J.D.; Chory, J. Coordination of gene expression between organellar and nuclear genomes. Nat. Rev. Gene 2008, 9, 383–395. [Google Scholar] [CrossRef] [PubMed]
  10. Yoon, H.S.; Hackett, J.D.; Bhattacharya, D. A genomic and phylogenetic perspective on endosymbiosis and algal origin. J. Appl. Phycol. 2006, 18, 475–481. [Google Scholar] [CrossRef]
  11. Kanno, A.; Hirai, A. A transcription map of the chloroplast genome from rice (Oryza sativa). Curr. Genet. 1993, 23, 166–174. [Google Scholar] [CrossRef] [PubMed]
  12. Nielsen, A.Z.; Ziersen, B.; Jensen, K.; Lassen, L.M.; Olsen, C.E.; Moller, B.L.; Jensen, P.E. Redirecting photosynthetic reducing power toward bioactive natural product synthesis. ACS Synth. Biol. 2013, 2, 308–315. [Google Scholar] [CrossRef] [PubMed]
  13. Echt, C.S.; Deverno, L.L.; Anzidei, M.; Vendramin, G.G. Chloroplast microsatellites reveal population genetic diversity in red pine, Pinus resinosa Ait. Mol. Ecol. 1998, 7, 307–316. [Google Scholar] [CrossRef]
  14. Wang, Y.; Ghouri, F.; Shahid, M.Q.; Naeem, M.; Baloch, F.S. The genetic diversity and population structure of wild soybean evaluated by chloroplast and nuclear gene sequences. Biochem. Syst. Ecol. 2017, 71, 170–178. [Google Scholar] [CrossRef]
  15. Alvespereira, A.; Clement, C.R.; Picanço-Rodrigues, D.; Veasey, E.A.; Dequigiovanni, G.; Ramos, S.L.F.; Pinheiro, J.B.; Zucchi, M.I. Patterns of nuclear and chloroplast genetic diversity and structure of manioc along major Brazilian Amazonian rivers. Ann. Bot. 2018, 121, 625–639. [Google Scholar] [CrossRef] [PubMed]
  16. Shen, X.; Wu, M.; Liao, B.; Liu, Z.; Bai, R.; Xiao, S.; Li, X.; Zhang, B.; Xu, J.; Chen, S. Complete chloroplast genome sequence and phylogenetic analysis of the medicinal plant Artemisia annua. Molecules 2017, 22, 1330. [Google Scholar] [CrossRef] [PubMed]
  17. Guo, S.; Guo, L.; Zhao, W.; Xu, J.; Li, Y.; Zhang, X.; Shen, X.; Wu, M.; Hou, X. Complete chloroplast genome sequence and phylogenetic analysis of Paeonia ostii. Molecules 2018, 23, 246. [Google Scholar] [CrossRef] [PubMed]
  18. Zhang, Y.J.; Du, L.W.; Liu, A.; Chen, J.J.; Wu, L.; Hu, W.M.; Zhang, W.; Kim, K.H.; Lee, S.C.; Yang, T.J.; et al. The complete chloroplast genome sequences of five epimedium species: Lights into phylogenetic and taxonomic analyses. Front. Plant Sci. 2016, 7, 696. [Google Scholar] [CrossRef] [PubMed]
  19. Nguyen, V.B.; Park, H.S.; Lee, S.C.; Lee, J.; Park, J.Y.; Yang, T.J. Authentication markers for five major Panax species developed via comparative analysis of complete chloroplast genome sequences. J. Agric. Food Chem. 2017, 65, 6298–6306. [Google Scholar] [CrossRef] [PubMed]
  20. Li, Y.; Huo, N.; Dong, L.; Wang, Y.; Zhang, S.; Young, H.A.; Feng, X.; Gu, Y.Q. Complete chloroplast genome sequences of Mongolia medicine Artemisia frigida and phylogenetic relationships with other plants. PLoS ONE 2013, 8, e57533. [Google Scholar] [CrossRef] [PubMed]
  21. He, L.; Qian, J.; Li, X.; Sun, Z.; Xu, X.; Chen, S. Complete chloroplast genome of medicinal plant lonicera japonica: Genome rearrangement, intron gain and loss, and implications for phylogenetic studies. Molecules 2017, 22, 249. [Google Scholar] [CrossRef] [PubMed]
  22. Daniell, H.; Khan, M.S.; Allison, L. Milestones in chloroplast genetic engineering: An environmentally friendly era in biotechnology. Trends Plant. Sci. 2002, 7, 84–91. [Google Scholar] [CrossRef]
  23. Daniell, H.; Kumar, S.; Dufourmantel, N. Breakthrough in chloroplast genetic engineering of agronomically important crops. Trends Biotechnol. 2005, 23, 238–245. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Sang, T.; Crawford, D.J.; Stuessy, T.F. Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). Am. J. Bot. 1997, 84, 1120–1136. [Google Scholar] [CrossRef] [PubMed]
  25. Grosche, C.; Funk, H.T.; Maier, U.G.; Zauner, S. The chloroplast genome of Pellia endiviifolia: Gene content, RNA-editing pattern, and the origin of chloroplast editing. Genome. Biol. Evol. 2012, 4, 1349–1357. [Google Scholar] [CrossRef] [PubMed]
  26. Yang, J.B.; Li, D.Z.; Li, H.T. Highly effective sequencing whole chloroplast genomes of angiosperms by nine novel universal primer pairs. Mol. Ecol. Res. 2015, 14, 1024–1031. [Google Scholar] [CrossRef] [PubMed]
  27. Li, R.; Ma, P.F.; Wen, J.; Yi, T.S. Complete sequencing of five Araliaceae chloroplast genomes and the phylogenetic implications. PLoS ONE 2013, 8, e78568. [Google Scholar] [CrossRef] [PubMed]
  28. Choi, K.S.; Park, S.J. The complete chloroplast genome sequence of Aster spathulifolius (Asteraceae); genomic features and relationship with Asteraceae. Gene 2015, 572, 214–221. [Google Scholar] [CrossRef] [PubMed]
  29. Liu, H.Y.; Yu, Y.; Deng, Y.Q.; Li, J.; Huang, Z.X.; Zhou, S.D. The Chloroplast Genome of Lilium henrici: Genome Structure and Comparative Analysis. Molecules 2018, 23, 1276. [Google Scholar] [CrossRef] [PubMed]
  30. Zhou, J.; Cui, Y.; Chen, X.; Li, Y.; Xu, Z.; Duan, B.; Li, Y.; Song, J.; Yao, H. Complete Chloroplast Genomes of Papaver rhoeas and Papaver orientale: Molecular Structures, Comparative Analysis, and Phylogenetic Analysis. Molecules 2018, 23, 437. [Google Scholar] [CrossRef] [PubMed]
  31. Meng, J.; Li, X.; Li, H.; Yang, J.; Wang, H.; He, J. Comparative Analysis of the Complete Chloroplast Genomes of Four Aconitum Medicinal Species. Molecules 2018, 23, 1015. [Google Scholar] [CrossRef] [PubMed]
  32. Boudreau, E.; Takahashi, Y.; Lemieux, C.; Turmel, M.; Rochaix, J.D. The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. Embo. J. 1997, 16, 6095–6104. [Google Scholar] [CrossRef] [PubMed]
  33. Carbonell-Caballero, J.; Alonso, R.; Ibañez, V.; Terol, J.; Talon, M.; Dopazo, J. A Phylogenetic Analysis of 34 Chloroplast Genomes Elucidates the Relationships between Wild and Domestic Species within the Genus Citrus. Mol. Biol. Evol. 2015, 32, 2015–2035. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Li, P.; Zhang, S.; Li, F.; Zhang, S.; Zhang, H.; Wang, X.; Sun, R.; Bonnema, G.; Borm, T.J. A Phylogenetic Analysis of Chloroplast Genomes Elucidates the Relationships of the Six Economically Important Brassica Species Comprising the Triangle of U. Front. Plant Sci. 2017, 8, 1–13. [Google Scholar] [CrossRef] [PubMed]
  35. Kong, W.; Yang, J. The complete chloroplast genome sequence of Morus mongolica, and a comparative analysis within the Fabidae clade. Curr. Genet. 2016, 62, 165–172. [Google Scholar] [CrossRef] [PubMed]
  36. Doyle, J.J. Multiple Independent Losses of Two Genes and One Intron from Legume Chloroplast Genomes. Syst. Bot. 1995, 20, 272–294. [Google Scholar] [CrossRef]
  37. Nguyen, D.S.; Sai, T.Z.; Nawaz, G.; Lee, K.; Kang, H. Abiotic stresses affect differently the intron splicing and expression of chloroplast genes in coffee plants (Coffea arabica) and rice (Oryza sativa). J. Plant Physiol. 2016, 201, 85–94. [Google Scholar] [CrossRef] [PubMed]
  38. Mohammad-Panah, N.; Shabanian, N.; Khadivi, A.; Rahmani, M.-S.; Emami, A. Genetic structure of gall oak (Quercus infectoria) characterized by nuclear and chloroplast SSR markers. Tree Genet. Genomes 2017, 13, 70–82. [Google Scholar] [CrossRef]
  39. Park, S.H.; Sang, I.P.; Gil, J.; Hwangbo, K.; Um, Y.; Kim, H.B.; Jung, C.S.; Kim, S.C.; Lee, Y. Development of Chloroplast SSR Markers to Distinguish Codonopsis Species. Korean Soc. Hortic. Sci. 2017, 5, 207–208. [Google Scholar]
  40. Zeng, J.; Chen, X.; Wu, X.F.; Jiao, F.C.; Xiao, B.G.; Li, Y.P.; Tong, Z.J. Genetic diversity analysis of genus Nicotiana based on SSR markers in chloroplast genome and mitochondria genome. Acta Tab. Sin. 2016, 22, 89–97. [Google Scholar]
  41. Park, S.; Sang, I.P.; Gil, J.; Um, Y.; Jung, C.S.; Lee, J.H.; Kim, S.C.; Kim, H.B.; Lee, Y. Development of Simple Sequence Repeat SSR Markers Based on Chloroplast DNA to Distinguish 3 Angelica Species. Korean Soc. Hortic. Sci. 2016, 10, 226. [Google Scholar]
  42. Zhihai, H.; Jiang, X.; Shuiming, X.; Baosheng, L.; Yuan, G.; Chaochao, Z.; Xiaohui, Q.; Wen, X.; Shilin, C. Comparative optical genome analysis of two pangolin species: Manis pentadactyla and Manis javanica. Gigascience 2016, 5, 1–5. [Google Scholar] [CrossRef] [PubMed]
  43. Xu, J.; Chu, Y.; Liao, B.; Xiao, S.; Yin, Q.; Bai, R.; Su, H.; Dong, L.; Li, X.; Qian, J.; et al. Panax ginseng genome examination for ginsenoside biosynthesis. Gigascience 2017, 6, 1–15. [Google Scholar] [CrossRef] [PubMed]
  44. Kode, V.; Mudd, E.A.; Iamtham, S.; Day, A. The tobacco plastid accD gene is essential and is required for leaf development. Plant J. Cell Mol. Biol. 2005, 44, 237–244. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Raubeson, L.A.; Peery, R.; Chumley, T.W.; Dziubek, C.; Fourcade, H.M.; Boore, J.L.; Jansen, R.K. Comparative chloroplast genomics: Analyses including new sequences from the angiosperms Nuphar advena and Ranunculus macranthus. BMC Genomics 2007, 8, 174–201. [Google Scholar] [CrossRef] [PubMed]
  46. Yao, X.; Tang, P.; Li, Z.; Li, D.; Liu, Y.; Huang, H. The first complete chloroplast genome sequences in actinidiaceae: Genome structure and comparative analysis. PLoS ONE 2015, 10, e0129347. [Google Scholar] [CrossRef] [PubMed]
  47. Dong, W.; Xu, C.; Li, C.; Sun, J.; Zuo, Y.; Shi, S.; Cheng, T.; Guo, J.; Zhou, S. Ycf1, the most promising plastid DNA barcode of land plants. Sci. Rep. 2015, 5, 1–5. [Google Scholar] [CrossRef] [PubMed]
  48. Kikuchi, S.; Bédard, J.; Hirano, M.; Hirabayashi, Y.; Oishi, M.; Imai, M.; Takase, M.; Ide, T.; Nakai, M. Uncovering the protein translocon at the chloroplast inner envelope membrane. Science 2013, 339, 571–574. [Google Scholar] [CrossRef] [PubMed]
  49. Doyle, J.J.; Davis, J.I.; Soreng, R.J.; Garvin, D.; Anderson, M.J. Chloroplast DNA inversions and the origin of the grass family (Poaceae). Proc. Natl. Acad. Sci. USA 1992, 89, 7722–7726. [Google Scholar] [CrossRef] [PubMed]
  50. Jansen, R.K.; Palmer, J.D. A chloroplast DNA inversion marks an ancient evolutionary split in the sunflower family (Asteraceae). Proc. Natl. Acad. Sci. USA 1987, 84, 5818–5822. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  51. Kumar, S.; Hahn, F.M.; McMahan, C.M.; Cornish, K.; Whalen, M.C. Comparative analysis of the complete sequence of the plastid genome of Parthenium argentatum and identification of DNA barcodes to differentiate Parthenium species and lines. BMC Plant Biol. 2009, 9, 131–143. [Google Scholar] [CrossRef] [PubMed]
  52. Palmer, J.D.; Nugent, J.M.; Herbon, L.A. Unusual structure of geranium chloroplast DNA: A triple-sized inverted repeat, extensive gene duplications, multiple inversions, and two repeat families. Proc. Natl. Acad. Sci. USA 1987, 84, 769–773. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Raubeson, L.A.; Jansen, R.K. Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 1992, 255, 1697–1699. [Google Scholar] [CrossRef] [PubMed]
  54. Shams, S.S.; Vahed, S.Z.; Soltanzad, F.; Kafil, V.; Barzegari, A.; Atashpaz, S.; Barar, J. Highly effective DNA extraction method from fresh, frozen, dried and clotted blood samples. Bioimpacts 2011, 1, 183–187. [Google Scholar]
  55. Simbolo, M.; Gottardi, M.; Corbo, V.; Fassan, M.; Mafficini, A.; Malpeli, G.; Lawlor, R.T.; Scarpa, A. DNA Qualification Workflow for Next Generation Sequencing of Histopathological Samples. PLoS ONE 2013, 8, e62692. [Google Scholar] [CrossRef] [PubMed]
  56. Jiang, H.; Lei, R.; Ding, S.W.; Zhu, S. Skewer: A fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinform. 2014, 15, 182–194. [Google Scholar] [CrossRef] [PubMed]
  57. Luo, R.; Liu, B.; Xie, Y.; Li, Z.; Huang, W.; Yuan, J.; He, G.; Chen, Y.; Pan, Q.; Liu, Y.; et al. SOAPdenovo2: An empirically improved memory-efficient short-read de novo assembler. Gigascience 2012, 1, 18–24. [Google Scholar] [CrossRef] [PubMed]
  58. Boetzer, M.; Henkel, C.V.; Jansen, H.J.; Butler, D.; Pirovano, W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011, 27, 578–579. [Google Scholar] [CrossRef] [PubMed]
  59. Acemel, R.D.; Tena, J.J.; Irastorzaazcarate, I.; Marlétaz, F.; Gómez-Marín, C.; de la Calle-Mustienes, E.; Bertrand, S.; Diaz, S.G.; Aldea, D.; Aury, J.M.; et al. A single three-dimensional chromatin compartment in amphioxus indicates a stepwise evolution of vertebrate Hox bimodal regulation. Nat. Genet. 2016, 48, 336–341. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  60. Liu, C.; Shi, L.; Zhu, Y.; Chen, H.; Zhang, J.; Lin, X.; Guan, X. CpGAVAS, an integrated web server for the annotation, visualization, analysis, and GenBank submission of completely sequenced chloroplast genome sequences. BMC Genomics 2012, 13, 715–722. [Google Scholar] [CrossRef] [PubMed]
  61. Wyman, S.K.; Jansen, R.K.; Boore, J.L. Automatic annotation of organellar genomes with DOGMA. Bioinformatics 2004, 20, 3252–3255. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  62. Schattner, P.; Brooks, A.N.; Lowe, T.M. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 2005, 33, 686–689. [Google Scholar] [CrossRef] [PubMed]
  63. Lohse, M.; Drechsel, O.; Bock, R. Organellar Genome DRAW (OGDRAW): A tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr. Genet. 2007, 52, 267–274. [Google Scholar] [CrossRef] [PubMed]
  64. Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28, 2731–2739. [Google Scholar] [CrossRef] [PubMed]
  65. Frazer, K.A.; Pachter, L.; Poliakov, A.; Rubin, E.M.; Dubchak, I. VISTA: Computational tools for comparative genomics. Nucleic Acids Res. 2004, 32, 273–279. [Google Scholar] [CrossRef] [PubMed]
  66. Kraemer, L.; Beszteri, B.; Gäbler-Schwarz, S.; Held, C.; Leese, F.; Mayer, C.; Pöhlmann, K.; Frickenhau, S. STAMP: Extensions to the STADEN sequence analysis package for high throughput interactive microsatellite marker design. BMC Bioinform. 2009, 10, 41. [Google Scholar] [CrossRef] [PubMed]
Sample Availability: Sequence data of Aster tataricus are available from the authors.
Molecules 23 02426 g001 550
Figure 1. Gene map of the A. tataricus chloroplast genome. Genes drawn inside the circle are transcribed clockwise, and those outside are transcribed counterclockwise. Genes belonging to different functional groups are color-coded. The darker gray in the inner circle corresponds to DNA G + C content, while the lighter gray corresponds to A + T content.
Figure 1. Gene map of the A. tataricus chloroplast genome. Genes drawn inside the circle are transcribed clockwise, and those outside are transcribed counterclockwise. Genes belonging to different functional groups are color-coded. The darker gray in the inner circle corresponds to DNA G + C content, while the lighter gray corresponds to A + T content.
Molecules 23 02426 g001
Molecules 23 02426 g002 550
Figure 2. Analysis of simple sequence repeats (SSRs) in the three Aster chloroplast genomes.
Figure 2. Analysis of simple sequence repeats (SSRs) in the three Aster chloroplast genomes.
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Molecules 23 02426 g003 550
Figure 3. Comparison of three chloroplast genomes using mVISTA. Gray arrows and thick black lines above the alignment indicate gene orientation. Purple bars represent exons, blue bars represent untranslated regions (UTRs), pink bars represent conserved non-coding sequences (CNS), and gray bars represent mRNA. The y-axis represents the percentage identity (shown: 50–100%).
Figure 3. Comparison of three chloroplast genomes using mVISTA. Gray arrows and thick black lines above the alignment indicate gene orientation. Purple bars represent exons, blue bars represent untranslated regions (UTRs), pink bars represent conserved non-coding sequences (CNS), and gray bars represent mRNA. The y-axis represents the percentage identity (shown: 50–100%).
Molecules 23 02426 g003
Molecules 23 02426 g004 550
Figure 4. Comparison of border distance between adjacent genes and junctions of the LSC, SSC, and two IR regions among the chloroplast genomes of three Aster species. Boxes below the main line indicate the adjacent border genes. The figure is not to scale with respect to sequence length and only shows relative changes at or near the IR/SC borders.
Figure 4. Comparison of border distance between adjacent genes and junctions of the LSC, SSC, and two IR regions among the chloroplast genomes of three Aster species. Boxes below the main line indicate the adjacent border genes. The figure is not to scale with respect to sequence length and only shows relative changes at or near the IR/SC borders.
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Molecules 23 02426 g005 550
Figure 5. Maximum likelihood (ML) phylogenetic tree reconstruction including 17 species based on concatenated sequences from all chloroplast genomes. The position of A. tataricus is indicated in red text. Paeonia ostii was used as the outgroup.
Figure 5. Maximum likelihood (ML) phylogenetic tree reconstruction including 17 species based on concatenated sequences from all chloroplast genomes. The position of A. tataricus is indicated in red text. Paeonia ostii was used as the outgroup.
Molecules 23 02426 g005
Table
Table 1. Summary of complete chloroplast genomes for three Aster species.
Table 1. Summary of complete chloroplast genomes for three Aster species.
SpeciesAster altaicusAster spathulifoliusAster tataricus
Large single-copy (LSC)
Length (bp)84,24081,99884,698
G + C (%)35.331.435.2
Length (%)55.354.955.4
Small single-copy (SSC)
Length (bp)18,19617,97318,250
G + C (%)31.335.831.3
Length (%)11.912.011.9
IR
Length (bp)25,00524,75125,022
G + C (%)43.043.243.0
Length (%)16.416.616.4
Total
Length (bp)152,446149,473152,992
G + C (%)37.337.737.3
Table
Table 2. Genes in the A. tataricus chloroplast genome.
Table 2. Genes in the A. tataricus chloroplast genome.
CategoryGene GroupGene Names
Self-replicationLarge subunit of ribosomal proteinsrpl2 **,a, 14, 16 **, 20, 22, 23 a, 32, 33, 36
Small subunit of ribosomal proteinsrps2, 3, 4, 7a, 8, 11, 12 **,a, 14, 16 **, 18, 19
DNA-dependent RNA polymeraserpoA, B, C1 **, C2
rRNA genesrrn16Sa, rrn23Sa, rrn4.5Sa, rrn5Sa
tRNA genestrnA-UGC **,a, trnC-GCA, trnD-GUC, trnE-UUC, trnF-GAA, trnfM-CAU, trnG-UCC **, trnG-GCC, trnH-GUG, trnI-CAU, trnI-GAU **,a, trnK-UUU **, trnL-CAA, trnL-UAA **, trnL-UAG, trnM-CAU, trnN-GUU, trnP-UGG, trnQ-UUG, trnR-ACG, trnR-UCU, trnS-GCU, trnS-GGA, trnS-UGA, trnT-GGU, trnT-UGU, trnV-GAC, trnV-UAC **, trnW-CCA, trnY-GUA
PhotosynthesisPhotosystem IpsaA, B, C, I, J
Photosystem IIpsbA, B, C, D, E, F, H, I, J, K, L, M, N, T, Z,
NADH oxidoreductasendhA **, B **,a, C, D, E, F, G, H, I, J, K
Cytochrome b6/f complexpetA, B **, D **, G, L, N
ATP synthaseatpA, B, E, F **, H, I
RubiscorbcL
Other genesMaturasematK
ProteaseclpP **
Envelope membrane proteincemA
Subunit acetyl-CoA-carboxylaseAccD
c-Type cytochrome synthesis geneCcsA
Conserved open reading framesycf1, 2a, 3 **, 4, 15
** Genes containing introns. a Duplicated gene (genes present in the inverted repeat (IR) regions).
Table
Table 3. Codon–anticodon recognition patterns and codon usage for the A. tataricus chloroplast genome.
Table 3. Codon–anticodon recognition patterns and codon usage for the A. tataricus chloroplast genome.
Amino AcidCodonNo.RSCU *tRNAAmino AcidCodonNo.RSCU *tRNA
PheUUU10641.34 TyrUAU7931.39
PheUUC5280.66trnF-GAATyrUAC3480.61trnY-GUA
LeuUUA5541.55trnL-UAAStopUAA5081.09
LeuUUG4921.37trnL-CAAStopUAG3680.79
LeuCUU4591.28 HisCAU3741.36
LeuCUC2050.57 HisCAC1750.64trnH-GUG
LeuCUA2720.76trnL-UAGGlnCAA4821.4trnQ-UUG
LeuCUG1690.47 GlnCAG2060.6
IleAUU7981.46 AsnAAU7921.39
IleAUC3970.73trnI-GAUAsnAAC3470.61trnN-GUU
IleAUA4410.81trnI-UAULysAAA9141.42trnK-UUU
MetAUG4151trn(f)M-CAULysAAG3760.58
ValGUU3641.45 AspGAU4711.43
ValGUC1760.7trnV-GACAspGAC1870.57trnD-GUC
ValGUA3181.26trnV-UACGluGAA5501.39trnE-UUC
ValGUG1480.59 GluGAG2410.61
SerUCU5091.37 CysUGU3451.15
SerUCC3290.89trnS-GGACysUGC2530.85trnC-GCA
SerUCA4931.33trnS-UGAStopUGA5241.12
SerUCG2920.79 TrpUGG4911trnW-CCA
ProCCU2591.29 ArgCGU2040.73trnR-ACG
ProCCC1560.78trnP-GGGArgCGC1080.39
ProCCA2241.12trnP-UGGArgCGA2821.01
ProCCG1640.82 ArgCGG1730.62
ThrACU3211.22 ArgAGA3290.89trnR-UCU
ThrACC2460.93trnT-GGUArgAGG2770.75
ThrACA3141.19trnT-UGUSerAGU5782.06
ThrACG1740.66 SerAGC3371.2trnS-GCU
AlaGCU2501.25 GlyGGU3150.95
AlaGCC1690.85 GlyGGC2050.62trnG-GCC
AlaGCA2421.21trnA-UGCGlyGGA4661.4trnG-UCC
AlaGCG1380.69 GlyGGG3421.03
* RSCU: relative synonymous codon usage.
Table
Table 4. A comparison of exon and intron length in genes with introns in the A. tataricus and A. spathulifolius chloroplast genomes.
Table 4. A comparison of exon and intron length in genes with introns in the A. tataricus and A. spathulifolius chloroplast genomes.
GeneLocationExon I (bp)Intron I (bp)Exon II (bp)Intron II (bp)Exon III (bp)
trnK-UUULSC37249738
37250235
trnG-UCCLSC2373248
2372347
trnL-UAALSC3444150
3742350
trnV-UACLSC3657537
3857337
trnI-GAUIR3878135
4377635
trnA-UGCIR3882035
3882035
rps12 *LSC23453525——114
114——243——243
rps16LSC23482040
39826216
rpl16LSC402100810
——————
rpl2IR391671434
393668435
rpoC1LSC4317091639
4297211641
ndhASSC5521055540
5531105540
ndhBIR777674756
777670756
ycf3LSC124690228739155
124697230739153
petBLSC6754658
6745642
atpFLSC144718411
145699410
clpPLSC71812291614229
71800291623229
petDLSC9645526
9724474
Exon and intron lengths in genes with introns in the A. tataricus chloroplast genome (gray background), and in the A. spathulifolius chloroplast genome (normal background) * The rps12 gene is a trans-spliced gene with the 5′ end located in the LSC region and the duplicated 3′ ends located in the IR regions.

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Shen, X.; Guo, S.; Yin, Y.; Zhang, J.; Yin, X.; Liang, C.; Wang, Z.; Huang, B.; Liu, Y.; Xiao, S.; et al. Complete Chloroplast Genome Sequence and Phylogenetic Analysis of Aster tataricus. Molecules 2018, 23, 2426. https://doi.org/10.3390/molecules23102426

AMA Style

Shen X, Guo S, Yin Y, Zhang J, Yin X, Liang C, Wang Z, Huang B, Liu Y, Xiao S, et al. Complete Chloroplast Genome Sequence and Phylogenetic Analysis of Aster tataricus. Molecules. 2018; 23(10):2426. https://doi.org/10.3390/molecules23102426

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Shen, Xiaofeng, Shuai Guo, Yu Yin, Jingjing Zhang, Xianmei Yin, Conglian Liang, Zhangwei Wang, Bingfeng Huang, Yanhong Liu, Shuiming Xiao, and et al. 2018. "Complete Chloroplast Genome Sequence and Phylogenetic Analysis of Aster tataricus" Molecules 23, no. 10: 2426. https://doi.org/10.3390/molecules23102426

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