Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
권호 표지
DOI QR코드

DOI QR Code

Comprehensive comparative analysis of chloroplast genomes from seven Panax species and development of an authentication system based on species-unique single nucleotide polymorphism markers

  • Nguyen, Van Binh (Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Giang, Vo Ngoc Linh (Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Waminal, Nomar Espinosa (Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Park, Hyun-Seung (Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Kim, Nam-Hoon (Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Jang, Woojong (Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Lee, Junki (Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Yang, Tae-Jin (Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University)
  • Received : 2018.02.20
  • Accepted : 2018.06.15
  • Published : 2020.01.15
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Panax species are important herbal medicinal plants in the Araliaceae family. Recently, we reported the complete chloroplast genomes and 45S nuclear ribosomal DNA sequences from seven Panax species, two (P. quinquefolius and P. trifolius) from North America and five (P. ginseng, P. notoginseng, P. japonicus, P. vietnamensis, and P. stipuleanatus) from Asia. Methods: We conducted phylogenetic analysis of these chloroplast sequences with 12 other Araliaceae species and comprehensive comparative analysis among the seven Panax whole chloroplast genomes. Results: We identified 1,128 single nucleotide polymorphisms (SNP) in coding gene sequences, distributed among 72 of the 79 protein-coding genes in the chloroplast genomes of the seven Panax species. The other seven genes (including psaJ, psbN, rpl23, psbF, psbL, rps18, and rps7) were identical among the Panax species. We also discovered that 12 large chloroplast genome fragments were transferred into the mitochondrial genome based on sharing of more than 90% sequence similarity. The total size of transferred fragments was 60,331 bp, corresponding to approximately 38.6% of chloroplast genome. We developed 18 SNP markers from the chloroplast genic coding sequence regions that were not similar to regions in the mitochondrial genome. These markers included two or three species-specific markers for each species and can be used to authenticate all the seven Panax species from the others. Conclusion: The comparative analysis of chloroplast genomes from seven Panax species elucidated their genetic diversity and evolutionary relationships, and 18 species-specific markers were able to discriminate among these species, thereby furthering efforts to protect the ginseng industry from economically motivated adulteration.

Keywords

References

  1. Radad K, Gille G, Liu L, Rausch WD. Use of ginseng in medicine with emphasis on neurodegenerative disorders. J Pharmacol Sci 2006;100:175-86. https://doi.org/10.1254/jphs.CRJ05010X
  2. Cho IH. Effects of Panax ginseng in neurodegenerative diseases. J Ginseng Res 2012;36:342. https://doi.org/10.5142/jgr.2012.36.4.342
  3. Zheng SD, Wu HJ, Wu DL. Roles and mechanisms of ginseng in protecting heart. Chin J Integr Med 2012;18:548-55. https://doi.org/10.1007/s11655-012-1148-1
  4. Xie JT, Mehendale SR, Li X, Quigg R, Wang X, Wang CZ, Wu JA, Aung HH, ARue P, Bell GI, et al. Anti-diabetic effect of ginsenoside Re in ob/ob mice. Biochim Biophys Acta 2005;1740:319-25. https://doi.org/10.1016/j.bbadis.2004.10.010
  5. Jung HJ, Choi H, Lim HW, Shin D, Kim H, Kwon B, Lee JE, Park EH, Lim CJ. Enhancement of anti-inflammatory and antinociceptive actions of red ginseng extract by fermentation. J Pharm Pharmacol 2012;64:756-62. https://doi.org/10.1111/j.2042-7158.2012.01460.x
  6. Wong AS, Che CM, Leung KW. Recent advances in ginseng as cancer therapeutics: a functional and mechanistic overview. Nat Prod Rep 2015;32:256-72. https://doi.org/10.1039/C4NP00080C
  7. Nguyen VB, Park HS, Lee SC, Lee J, Park JY, Yang TJ. Authentication markers for five major Panax species developed via comparative analysis of complete chloroplast genome sequences. J Agric Food Chem 2017;65:6298-306. https://doi.org/10.1021/acs.jafc.7b00925
  8. Chan T, But P, Cheng S, Kwok I, Lau F, Xu H. Differentiation and authentication of Panax ginseng, Panax quinquefolius, and ginseng products by using HPLC/MS. Anal Chem 2000;72:1281-7. https://doi.org/10.1021/ac990819z
  9. Yuk J, McIntyre KL, Fischer C, Hicks J, Colson KL, Lui E, Brown D, Arnason JT. Distinguishing Ontario ginseng landraces and ginseng species using NMRbased metabolomics. Anal Bioanal Chem 2013;405:4499-509. https://doi.org/10.1007/s00216-012-6582-6
  10. Wang X, Sakuma T, Asafu-Adjaye E, Shiu GK. Determination of ginsenosides in plant extracts from Panax ginseng and Panax quinquefolius L. by LC/MS/MS. Anal Chem 1999;71:1579-84. https://doi.org/10.1021/ac980890p
  11. Yang W, Qiao X, Li K, Fan J, Bo T, Guo DA, Ye M. Identification and differentiation of Panax ginseng, Panax quinquefolium, and Panax notoginseng by monitoring multiple diagnostic chemical markers. Acta Pharm Sin B 2016;6:568-75. https://doi.org/10.1016/j.apsb.2016.05.005
  12. Shi W, Wang Y, Li J, Zhang H, Ding L. Investigation of ginsenosides in different parts and ages of Panax ginseng. Food Chem 2007;102:664-8. https://doi.org/10.1016/j.foodchem.2006.05.053
  13. Oh JY, Kim YJ, Jang MG, Joo SC, Kwon WS, Kim SY, Jung SK, Yang DC. Investigation of ginsenosides in different tissues after elicitor treatment in Panax ginseng. J Ginseng Res 2014;38:270-7. https://doi.org/10.1016/j.jgr.2014.04.004
  14. Lee YS, Park HS, Lee DK, Jayakodi M, Kim NH, Koo HJ, Lee SC, Kim YJ, Kwon SW, Yang TJ. Integrated transcriptomic and metabolomic analysis of five Panax ginseng cultivars reveals the dynamics of ginsenoside biosynthesis. Front Plant Sci 2017;8:1048. https://doi.org/10.3389/fpls.2017.01048
  15. Xiao D, Yue H, Xiu Y, Sun X, Wang Y, Liu S. Accumulation characteristics and correlation analysis of five ginsenosides with different cultivation ages from different regions. J Ginseng Res 2015;39:338-44. https://doi.org/10.1016/j.jgr.2015.03.004
  16. Kim YJ, Jeon JN, Jang MG, Oh JY, Kwon WS, Jung SK, Yang DC. Ginsenoside profiles and related gene expression during foliation in Panax ginseng Meyer. J Ginseng Res 2014;38:66-72. https://doi.org/10.1016/j.jgr.2013.11.001
  17. Jiang M, Liu J, Quan X, Quan L, Wu S. Different chilling stresses stimulated the accumulation of different types of ginsenosides in Panax ginseng cells. Acta Physiol Plant 2016;38:210. https://doi.org/10.1007/s11738-016-2210-y
  18. Leebens-Mack J, Raubeson LA, Cui L, Kuehl JV, Fourcade MH, Chumley TW, Boore JL, Jansen RK, Depamphilis CW. Identifying the basal angiosperm node in chloroplast genome phylogenies: sampling one's way out of the Felsenstein zone. Mol Biol Evol 2005;22:1948-63. https://doi.org/10.1093/molbev/msi191
  19. Kim K, Nguyen VB, Dong JZ, Wang Y, Park JY, Lee SC, Yang TJ. Evolution of the Araliaceae family inferred from complete chloroplast genomes and 45S nrDNAs of 10 Panax-related species. Sci Rep 2017;7:4917. https://doi.org/10.1038/s41598-017-05218-y
  20. Artyukova E, Kozyrenko M, Reunova G, Muzarok T, Zhuravlev YN. RAPD analysis of genome variability of planted ginseng, Panax ginseng. Mol Biol 2000;34:297-302. https://doi.org/10.1007/bf02759655
  21. Ma KH, Dixit A, Kim YC, Lee DY, Kim TS, Cho EG, Park YJ. Development and characterization of new microsatellite markers for ginseng (Panax ginseng CA Meyer). Conserv Genet 2007;8:1507-9. https://doi.org/10.1007/s10592-007-9284-4
  22. Kim NH, Choi HI, Ahn IO, Yang TJ. EST-SSR marker sets for practical authentication of all nine registered ginseng cultivars in Korea. J Ginseng Res 2012;36:298. https://doi.org/10.5142/jgr.2012.36.3.298
  23. Choi HI, Kim NH, Kim JH, Choi BS, Ahn IO, Lee JS, Yang TJ. Development of reproducible EST-derived SSR markers and assessment of genetic diversity in Panax ginseng cultivars and related species. J Ginseng Res 2011;35:399. https://doi.org/10.5142/jgr.2011.35.4.399
  24. Li X, Yang Y, Henry RJ, Rossetto M, Wang Y, Chen S. Plant DNA barcoding: from gene to genome. Biol Rev 2015;90:157-66. https://doi.org/10.1111/brv.12104
  25. Kim K, Lee SC, Lee J, Lee HO, Joh HJ, Kim NH, Park HS, Yang TJ. Comprehensive survey of genetic diversity in chloroplast genomes and 45S nrDNAs within Panax ginseng species. PloS One 2015;10. e0117159. https://doi.org/10.1371/journal.pone.0117159
  26. Jung J, Kim KH, Yang K, Bang KH, Yang TJ. Practical application of DNA markers for high-throughput authentication of Panax ginseng and Panax quinquefolius from commercial ginseng products. J Ginseng Res 2014;38:123-9. https://doi.org/10.1016/j.jgr.2013.11.017
  27. Chen X, Liao B, Song J, Pang X, Han J, Chen S. A fast SNP identification and analysis of intraspecific variation in the medicinal Panax species based on DNA barcoding. Gene 2013;530:39-43. https://doi.org/10.1016/j.gene.2013.07.097
  28. Kim NH, Jayakodi M, Lee SC, Choi BS, Jang W, Lee J, Kim HH, Waminal NE, Lakshmana M, Binh NV, et al. Genome and evolution of the shade-requiring medicinal herb Panax ginseng. Plant Biotechnol J, 2018. https://doi.org/10.1111/pbi.12926.
  29. Kim K, Lee SC, Lee J, Yu Y, Yang K, Choi BS, Koh HJ, Waminal NE, Choi HI, Kim NH, et al. Complete chloroplast and ribosomal sequences for 30 accessions elucidate evolution of Oryza AA genome species. Sci Rep 2015;5:15655. https://doi.org/10.1038/srep15655
  30. Allen G, Flores-Vergara M, Krasynanski S, Kumar S, Thompson W. A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide. Nat Protoc 2006;1:2320-5. https://doi.org/10.1038/nprot.2006.384
  31. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013;30:2725-9. https://doi.org/10.1093/molbev/mst197
  32. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B. Artemis: sequence visualization and annotation. Bioinformatics 2000;16:944-5. https://doi.org/10.1093/bioinformatics/16.10.944
  33. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. Circos: an information aesthetic for comparative genomics. Genome Res 2009;19:1639-45. https://doi.org/10.1101/gr.092759.109
  34. Cui Y, Qin S, Jiang P. Chloroplast transformation of Platymonas (Tetraselmis) subcordiformis with the bar gene as selectable marker. PloS One 2014;9:e98607. https://doi.org/10.1371/journal.pone.0098607
  35. Dong W, Liu H, Xu C, Zuo Y, Chen Z, Zhou S. A chloroplast genomic strategy for designing taxon specific DNA mini-barcodes: a case study on ginsengs. BMC Genetics 2014;15:138. https://doi.org/10.1186/s12863-014-0138-z
  36. Li R, Ma PF, Wen J, Yi TS. Complete sequencing of five Araliaceae chloroplast genomes and the phylogenetic implications. PloS One 2013;8:e78568. https://doi.org/10.1371/journal.pone.0078568
  37. Huang H, Shi C, Liu Y, Mao SY, Gao LZ. Thirteen Camellia chloroplast genome sequences determined by high-throughput sequencing: genome structure and phylogenetic relationships. BMC Evol Biol 2014;14:151. https://doi.org/10.1186/1471-2148-14-151
  38. Cho KS, Yun BK, Yoon YH, Hong SY, Mekapogu M, Kim KH, Yang TJ. Complete chloroplast genome sequence of Tartary Buckwheat (Fagopyrum tataricum) and comparative analysis with Common Buckwheat (F. esculentum). PloS One 2015;10. e0125332. https://doi.org/10.1371/journal.pone.0125332
  39. Court WE. Ginseng: the genus Panax. Taylor & Francis E-Library; 2006. p. 15.
  40. Freeling M, Thomas BC. Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 2006;16:805-14. https://doi.org/10.1101/gr.3681406
  41. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, Wall PK, Soltis PS. Polyploidy and angiosperm diversification. Am J Bot 2009;96:336-48. https://doi.org/10.3732/ajb.0800079
  42. Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH. The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci 2009;106:13875-9. https://doi.org/10.1073/pnas.0811575106
  43. Kim NH, Choi HI, Kim KH, Jang W, Yang TJ. Evidence of genome duplication revealed by sequence analysis of multi-loci expressed sequence tagesimple sequence repeat bands in Panax ginseng Meyer. J Ginseng Res 2014;38:130-5. https://doi.org/10.1016/j.jgr.2013.12.005
  44. Choi HI, Kim NH, Lee J, Choi BS, Do Kim K, Park JY, Lee SC, Yang TJ. Evolutionary relationship of Panax ginseng and P. quinquefolius inferred from sequencing and comparative analysis of expressed sequence tags. Genet Resour Crop Evol 2013;60:1377-87. https://doi.org/10.1007/s10722-012-9926-3
  45. Shi FX, Li MR, Li YL, Jiang P, Zhang C, Pan YZ, Liu B, Xiao HX, Li LF. The impacts of polyploidy, geographic and ecological isolations on the diversification of Panax (Araliaceae). BMC Plant Biol 2015;15:297. https://doi.org/10.1186/s12870-015-0669-0
  46. Timmis JN, Ayliffe MA, Huang CY, Martin W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 2004;5:123. https://doi.org/10.1038/nrg1271
  47. Kleine T, Maier UG, Leister D. DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol 2009;60:115-38. https://doi.org/10.1146/annurev.arplant.043008.092119
  48. Park S, Ruhlman TA, Sabir JS, Mutwakil MH, Baeshen MN, Sabir MJ, Baeshen NA, Jansen RK. Complete sequences of organelle genomes from the medicinal plant Rhazya stricta (Apocynaceae) and contrasting patterns of mitochondrial genome evolution across asterids. BMC Genomics 2014;15:405. https://doi.org/10.1186/1471-2164-15-405
  49. Hazkani-Covo E, Zeller RM, Martin W. Molecular poltergeists: mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genet 2010;6. e1000834. https://doi.org/10.1371/journal.pgen.1000834
  50. Smith DR, Crosby K, Lee RW. Correlation between nuclear plastid DNA abundance and plastid number supports the limited transfer window hypothesis. Genome Biol Evol 2011;3:365-71. https://doi.org/10.1093/gbe/evr001
  51. Gui S, Wu Z, Zhang H, Zheng Y, Zhu Z, Liang D, Ding Y. The mitochondrial genome map of Nelumbo nucifera reveals ancient evolutionary features. Sci Rep 2016;6:30158. https://doi.org/10.1038/srep30158
  52. Zuo Y, Chen Z, Kondo K, Funamoto T, Wen J, Zhou S. DNA barcoding of Panax species. Planta Med 2011;77:182. https://doi.org/10.1055/s-0030-1250166
  53. Ngan F, Shaw P, But P, Wang J. Molecular authentication of Panax species. Phytochem 1999;50:787-91. https://doi.org/10.1016/S0031-9422(98)00606-2

Cited by

  1. The complete chloroplast genome sequence of an invasive plant Lonicera Maackii (Caprifoliaceae) vol.4, pp.1, 2020, https://doi.org/10.1080/23802359.2018.1524722
  2. Two complete chloroplast genome sequences and intra-species diversity for Rehmannia glutinosa (Orobanchaceae) vol.4, pp.1, 2020, https://doi.org/10.1080/23802359.2018.1545529
  3. Dynamic Chloroplast Genome Rearrangement and DNA Barcoding for Three Apiaceae Species Known as the Medicinal Herb “Bang-Poong” vol.20, pp.9, 2020, https://doi.org/10.3390/ijms20092196
  4. Comparative Analysis of two Sugarcane Ancestors Saccharum officinarum and S. spontaneum based on Complete Chloroplast Genome Sequences and Photosynthetic Ability in Cold Stress vol.20, pp.15, 2020, https://doi.org/10.3390/ijms20153828
  5. Development of novel Quercus rubra chloroplast genome CAPS markers for haplotype identification vol.69, pp.1, 2020, https://doi.org/10.2478/sg-2020-0011
  6. Characterization of Chloroplast Genomes From Two Salvia Medicinal Plants and Gene Transfer Among Their Mitochondrial and Chloroplast Genomes vol.11, 2020, https://doi.org/10.3389/fgene.2020.574962
  7. Comparative analyses of chloroplast genomes of Theobroma cacao and Theobroma grandiflorum vol.75, pp.5, 2020, https://doi.org/10.2478/s11756-019-00388-8
  8. Comparative Survey of Morphological Variations and Plastid Genome Sequencing Reveals Phylogenetic Divergence between Four Endemic Ilex Species vol.11, pp.9, 2020, https://doi.org/10.3390/f11090964
  9. Complete Mitochondrial Genome and a Set of 10 Novel Kompetitive Allele-Specific PCR Markers in Ginseng (Panax ginseng C. A. Mey.) vol.10, pp.12, 2020, https://doi.org/10.3390/agronomy10121868
  10. Comparative analysis of the complete plastid genomes of Mangifera species and gene transfer between plastid and mitochondrial genomes vol.9, 2020, https://doi.org/10.7717/peerj.10774
  11. Foliose Ulva Species Show Considerable Inter‐Specific Genetic Diversity, Low Intra‐Specific Genetic Variation, and the Rare Occurrence of Inter‐Specific Hybrids in the Wild vol.57, pp.1, 2020, https://doi.org/10.1111/jpy.13079
  12. Generation of Chloroplast Molecular Markers to Differentiate Sophora toromiro and Its Hybrids as a First Approach to Its Reintroduction in Rapa Nui (Easter Island) vol.10, pp.2, 2020, https://doi.org/10.3390/plants10020342
  13. Characterization of the complete chloroplast genome of China Viburnum burejaeticum Regel et Herd and intra-species diversity vol.6, pp.4, 2020, https://doi.org/10.1080/23802359.2021.1907810
  14. Diversity and authentication of Rubus accessions revealed by complete plastid genome and rDNA sequences vol.6, pp.4, 2020, https://doi.org/10.1080/23802359.2021.1911712
  15. Comparative plastome analysis of Blumea , with implications for genome evolution and phylogeny of Asteroideae vol.11, pp.12, 2020, https://doi.org/10.1002/ece3.7614
  16. DNA barcoding: a modern age tool for detection of adulteration in food vol.41, pp.5, 2021, https://doi.org/10.1080/07388551.2021.1874279
  17. Development of Hydrolysis Probe-Based qPCR Assays for Panax ginseng and Panax quinquefolius for Detection of Adulteration in Ginseng Herbal Products vol.10, pp.11, 2021, https://doi.org/10.3390/foods10112705
  18. Phylogenetic analysis and development of molecular markers for five medicinal Alpinia species based on complete plastome sequences vol.21, pp.1, 2021, https://doi.org/10.1186/s12870-021-03204-1