Skip to main content
SpringerLink
Log in

Characterization and comparison of chloroplast genomes from two sympatric Hippophae species (Elaeagnaceae)

  • Original Paper
  • Published:
Journal of Forestry Research Aims and scope Submit manuscript

Abstract

The genus Hippophae includes deciduous shrubs or small trees, which provide many ecological, economic, and social benefits. We assembled and annotated the chloroplast genomes of sympatric Hippophae gyantsensis (Rousi) Lian and Hippophae rhamnoides Linn subsp. yunnanensis Rousi and comparatively analyzed their sequences. The full-length chloroplast genomes of H. gyantsensis and H. rhamnoides subsp. yunnanensis were 155,260 and 156,415 bp, respectively; both featured a quadripartite structure with two copies of a large inverted repeat (IR) separated by small (SSC) and large (LSC) single-copy regions. Each Hippophae chloroplast genome contained 131 genes, comprising 85 protein-coding, 8 ribosomal RNA, and 38 transfer RNA genes. Of 1302 nucleotide substitutions found between these two genomes, 824 (63.29%) occurred in the intergenic region or intron sequences, and 478 (36.71%) were located in the coding sequences. The SSC region had the highest mutation rate, followed by the LSC region and IR regions. Among the protein-coding genes, three had a ratio of nonsynonymous to synonymous substitutions (Ka/Ks) > 1 yet none were significant, and 66 had Ka/Ks < 1, of which 46 were significant. We found 20 and 16 optimal codons, most of which ended with A or U, for chloroplast protein-coding genes of H. gyantsensis and H. rhamnoides subsp. yunnanensis, respectively. Phylogenetic analysis of five available whole chloroplast genome sequences in the family Elaeagnaceae—using one Ziziphus jujube sequence as the outgroup—revealed that all five plant species formed a monophyletic clade with two subclades: one subclade consisted of three Hippophae species, while the other was formed by two Elaeagnus species, supported by 100% bootstrap values. Together, these results suggest the chloroplast genomes among Hippophae species are conserved, both in structure and gene composition, due to general purifying selection; like many other plants, a significant AT preference was discerned for most protein-coding genes in the Hippophae chloroplast genome. This study provides a valuable reference tool for future research on the general characteristics and evolution of chloroplast genomes in the genus Hippophae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bal LM, Meda V, Naik SN, Satya S (2011) Sea buckthorn berries: a potential source of valuable nutrients for nutraceuticals and cosmoceuticals. Food Res Int 44(7):1718–1727

    Article  CAS  Google Scholar 

  • Bartish IV (2002) Phylogeny of Hippophae (Elaeagnaceae) inferred from parsimony analysis of chloroplast DNA and morphology. Syst Bot 27(1):47–54

    Google Scholar 

  • Chen SY, Zhang XZ (2017) Characterization of the complete chloroplast genome of seabuckthorn (Hippophae rhamnoides L.). Conserv Genet Resour 9(4):623–626

    Article  Google Scholar 

  • Cheng K (2008) Study on genetic diversity and protection of Hipppophae gyantsensis and Hippophae rhamnenoide subsp. yunnanensis. Master dissertation, Sichuan Agricultural University

  • Choi KS, Son O, Park S (2015) The chloroplast genome of Elaeagnus macrophylla and trnH duplication event in Elaeagnaceae. PLoS ONE 10(9):e0138727

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Datwyler SL, Weiblen GD (2004) On the origin of the fig: phylogenetic relationships of Moraceae from ndhF sequences. Am J Bot 91(5):767–777

    Article  PubMed  Google Scholar 

  • Dhyani D, Maikhuri RK, Dhyani S (2011) Seabuckthorn: an underutilized resource for the nutritional security and livelihood improvement of rural communities in Uttarakhand Himalaya. Ecol Food Nutr 50(2):168–180

    Article  PubMed  Google Scholar 

  • Dierckxsens N, Mardulyn P, Smits G (2017) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res 45(4):e18

    PubMed  Google Scholar 

  • Ding YQ, Yang F, Jin YL, Hai Z, He KZ (2017) Systematic evolution of lemnoideae determined based on chloroplast genome analysis. Chin J Appl Environ Biol 23(4):622–627

    Google Scholar 

  • Dong WP, Xu C, Li CG, Sun JH, Zuo YJ, Shi S, Cheng T, Guo JJ, Zhou SL (2015) Ycf1, the most promising plastid DNA barcode of land plants. Sci Rep 5:8348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong WL, Wang RN, Zhang NY, Fan WB, Fang MF, Li ZH (2018) Molecular evolution of chloroplast genomes of orchid species: insights into phylogenetic relationship and adaptive evolution. J Mol Sci 19(3):716–736

    Article  CAS  Google Scholar 

  • Doyle JJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Guisinger MM, Chumley TW, Kuehl JV, Boore JL, Jansen RK (2010) Implications of the plastid genome sequence of Typha (Typhaceae, Poales) for understanding genome evolution in Poaceae. J Mol Evol 70(2):149–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He CY, Zhang GY, Zhang JG, Duan AG, Luo HM (2016) Physiological, biochemical, and proteome profiling reveals key pathways underlying the drought stress responses of Hippophae rhamnoides. Proteomics 16(20):2688–2697

    Article  CAS  PubMed  Google Scholar 

  • Hershberg R, Petrov DA (2009) General rules for optimal codon choice. PLoS Genet 5(7):e1000556

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hu SS, Luo H, Wu Q, Yao HP (2016) Analysis of codon bias of chloroplast genome of tartary buckwheat. Mol Plant Breed 14(2):309–317

    CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755

    Article  CAS  PubMed  Google Scholar 

  • Jadhav MS (2014) Identification of gender specific DNA markers in sea buckthorn (Hippophae rhamnoides L.). Ind Res J Genet Biotech 6(3):464–469

    Google Scholar 

  • Jan DV, Sousa FL, Bettina BL, Jürgen S, Gould SB (2015) YCF1: a green TIC? Plant Cell 27(7):1827–1833

    Article  CAS  Google Scholar 

  • Jia DR, Abbott RJ, Liu TL, Mao KS, Bartish IV, Liu JQ (2012) Out of the Qinghai-Tibet Plateau: evidence for the origin and dispersal of Eurasian temperate plants from a phylogeographic study of Hippophae rhamnoides (Elaeagnaceae). New Phytol 194(4):1123–1133

    Article  PubMed  Google Scholar 

  • Kortesniemi M, Sinkkonen J, Yang BR, Kallio H (2017) NMR metabolomics demonstrates phenotypic plasticity of sea buckthorn (Hippophae rhamnoides) berries with respect to growth conditions in Finland and Canada. Food Chem 219:139–147

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li R, Yu YT (2008) Application and prospect of DNA molecular markers in seabuckthorn heredity and breeding. Glob Seabuckthorn Res Dev 6(2):19–25

    Google Scholar 

  • Li FW, Kuo LY, Pryer KM, Rothfels CJ (2016) Genes translocated into the plastid inverted repeat show decelerated substitution rates and elevated GC content. Genome Biol Evol 8(8):2452–2458

    Article  PubMed  PubMed Central  Google Scholar 

  • Li SS, Zeng YF, He CY, Zhang JG (2017) Development of EST-SSR markers based on seabuckthorn transcriptomic sequences. For Res 30(1):69–74

    Google Scholar 

  • Li QL, Yan N, Song Q, Guo JZ (2018) Complete chloroplast genome sequence and characteristics analysis of Morus multicaulis. Chin Bull Bot 53(1):94–103

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Wang MX, Yue WJ, Xing GW, Ge LQ, Nie XJ, Song WN (2017) Analysis of codon usage in the chloroplast genome of broomcorn millet (Panicum miliaceum L.). Plant Sci J 35(3):362–371

    Google Scholar 

  • Liu YP, Su X, Lv T, Liu T (2018) Characterization and phylogenetic analysis of the complete chloroplast genome of Orinus thoroldii (Poaceae). Conserv Genet Resour 10(4):761–764

    Article  Google Scholar 

  • Lütz C, Engel L (2007) Changes in chloroplast ultrastructure in some high-alpine plants: adaptation to metabolic demands and climate? Protoplasma 231(3–4):183–192

    Article  PubMed  Google Scholar 

  • Ma YH, Ye GS, Xiang QS, Gao Y, Yang CJ, Wei GL, Song WX (2014) Phylogenetic relationships of seabuckthorn based on ITS sequences. Chin J Appl Ecol 25(10):2985–2990

    CAS  Google Scholar 

  • Maréchal A, Brisson N (2010) Recombination and the maintenance of plant organelle genome stability. New Phytol 186(2):299–317

    Article  PubMed  CAS  Google Scholar 

  • Meng J, Li XP, Li HT, Yang JB, Wang H, He J (2018) Comparative analysis of the complete chloroplast genomes of four aconitum medicinal species. Molecules 23(5):1015–1030

    Article  PubMed Central  CAS  Google Scholar 

  • Nazareno AG, Carlsen M, Lohmann LG (2015) Complete chloroplast genome of Tanaecium tetragonolobum: the first bignoniaceae plastome. PLoS ONE 10(6):e0129930

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Qian XS, Jin JH (2015) Medical research and development of sea-buckthorn. Chin Wild Plant Res 34(6):68–72

    Google Scholar 

  • Ruhfel BR, Gitzendanner MA, Soltis PS, Soltis DE, Burleigh J (2014) From algae to angiosperms-inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. BMC Evol Biol 14(1):23–50

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruhlman TA, Jansen RK (2014) The plastid genomes of flowering plants. In: Maliga P (ed) Chloroplast biotechnology. Humana Press, New York, pp 3–38

    Chapter  Google Scholar 

  • Sato S, Nakamura Y, Kaneko T, Asamizu E, Tabata S (1999) Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res 6(5):283–290

    Article  CAS  PubMed  Google Scholar 

  • Stobdan T, Angchuk D, Singh SB (2008) Seabuckthorn: an emerging storehouse for researchers in India. Curr Sci India 94(94):1236–1237

    Google Scholar 

  • Sugiura M (1992) The chloroplast genome. Springer 19(1):149–168

    CAS  Google Scholar 

  • Suryakumar G, Gupta A (2011) Medicinal and therapeutic potential of sea buckthorn (Hippophae rhamnoides L.). J Ethnopharmacol 138(2):268–278

    Article  PubMed  Google Scholar 

  • Wang L, Dong WP, Zhou SL (2012) Structural mutations and reorganizations in chloroplast genomes of flowering plants. Acta Bot Boreal Occident Sin 32(6):1282–1288

    CAS  Google Scholar 

  • Wang WC, Chen SY, Zhang XZ (2017) Characterization of the complete chloroplast genome of Elaeagnus mollis, a rare and endangered oil plant. Conserv Genet Resour 9:439–442

    Article  Google Scholar 

  • Wang LY, Xing HX, Yuan YC, Wang XL, Saeed M, Tao JC, Feng W, Zhang GH, Song XL, Sun XZ (2018a) Genome-wide analysis of codon usage bias in four sequenced cotton species. PLoS ONE 13(3):e0194372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang PL, Yang LP, Wu HY, Nong YL, Wu SC, Xiao YF, Qin ZH, Wang HY, Liu HL (2018b) Condon preference of chloroplast genome in Camellia oleifera. Guihaia 38(2):135–144

    CAS  Google Scholar 

  • Wicke S, Schneeweiss GM, Depamphilis CW, Muller KF, Quandt D (2011) The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol 76(3–5):273–297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20(17):3252–3255

    Article  CAS  PubMed  Google Scholar 

  • Xu C, Cai XN, Chen QZ, Zhou HX, Cai Y, Ben AL (2011) Factors affecting synonymous codon usage bias in chloroplast genome of oncidium gower ramsey. Evol Bioinform 7:271–278

    Article  CAS  Google Scholar 

  • Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J (2006) KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genom Proteom Bioinform 4(4):259–263

    Article  CAS  Google Scholar 

  • Zhang HY, Li C, Miao HM, Xiong SJ (2013) Insights from the complete chloroplast genome into the evolution of Sesamum indicum L. PLoS ONE 8(11):e80508

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang RT, Wang J, Han K, Ren T, Zeng SY, Biffin E, Liu ZL (2017) Complete chloroplast genome sequence of Pedicularis cheilanthifolia, an alpine plant in China. Conserv Genet Resour 9(W1):1–3

    Google Scholar 

  • Zhao YC, Zheng H, Xu AY, Yan DH, Jiang ZJ, Qi Q, Sun JC (2016) Analysis of codon usage bias of envelope glycoprotein genes in nuclear polyhedrosis virus (NPV) and its relation to evolution. BMC Genom 17(1):677–687

    Article  CAS  Google Scholar 

  • Zhengqiu C, Penaflor C, Kuehl JV, Leebensmack J, Carlson J, Depamphilis CW, Boore JL, Jansen RK (2006) Complete chloroplast genome sequences of Drimys, Liriodendron, and Piper: implications for the phylogeny of magnoliids and the evolution of GC content. Off Sci Tech Inf Tech Rep 6:77

    Google Scholar 

  • Zhou X, Tian L, Zhang JF, Ma L, Li XJ (2017) Rhizospheric fungi and their link with the nitrogen-fixing Frankia harbored in host plant Hippophae rhamnoides L. J Basic Microbiol 57(12):1–10

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. State Key Laboratory of Tree Genetics and Breeding and Key Laboratory of Tree Breeding and Cultivation of the State Forestry and Grassland Administration, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, People’s Republic of China

    Luoyun Wang, Jing Wang, Caiyun He, Jianguo Zhang & Yanfei Zeng

  2. Collaborative Innovation Center of Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, People’s Republic of China

    Jianguo Zhang

Authors
  1. Luoyun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Caiyun He
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jianguo Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yanfei Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jianguo Zhang or Yanfei Zeng.

Additional information

Publisher's Note

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

Project funding: This work was supported by the National Natural Science Foundation of China (31670666) and the Fundamental Research Funds for the Central Non-profit Research Institution of Chinese Academy of Forestry (ZDRIF201706).

The online version is available at http://www.springerlink.com.

Corresponding editor: Yanbo Hu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, L., Wang, J., He, C. et al. Characterization and comparison of chloroplast genomes from two sympatric Hippophae species (Elaeagnaceae). J. For. Res. 32, 307–318 (2021). https://doi.org/10.1007/s11676-019-01079-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11676-019-01079-5

Keywords

Search

Navigation