Origin and evolution of Korean ginseng revealed by genome sequence

  • Cho, Woohyeon (College of Agriculture & Life Sciences, Seoul National University) ;
  • Shim, Hyeonah (College of Agriculture & Life Sciences, SNU) ;
  • Yang, Tae-Jin (College of Agriculture & Life Sciences, SNU)
  • Received : 2021.01.19
  • Accepted : 2021.02.03
  • Published : 2021.03.15

Abstract

Panax ginseng (Ginseng or Korean ginseng) is one of the most important medicinal herbs in the world. We made a high-quality whole genome sequence of P. ginseng using 'Chunpoong' cultivar, which is the first cultivar registered in Korea Seed and Variety Service (KSVS) with relatively similar genotypes and superior phenotypes, representing approximately 3 Gbp and 60,000 genes. Genome sequence analyses of P. ginseng and related speciesrevealed the origin of Korean ginseng and the ecological adaptation of 18 Panax species around the world. Korean ginseng and American ginseng (P. quinquefolius) are tetraploid species having 24 chromosome pairs, while the other 16 species are diploid species with 12 chromosome pairs. Panax and Aralia are the closest genera belonging to the Araliaceae family that diverged approximately 8 million years ago (MYA). All Panax species evolved as shade plants adapting to cool climates and low light conditions under the canopy of deep forests from Southeast Asia such as Vietnam to Northeast Asia such as Russia approximately 6 MYA. However, through recurrent ice ages and global warming, most diploid Panax species disappeared due to the freezing winter, while tetraploid P. ginseng may have appeared by allotetraploidization, which contributed to the adaptation to cold temperaturesin Northeast Asian countries including the Korea peninsula approximately 2 MYA. American ginseng evolved by the adaptation of P. ginseng in Northeast America after the intercontinental migration 1 MYA. Meanwhile, most of diploid Panax species survived in high-altitude mountains over 1,600 meters in Southeast Asia because they could not endure the hot temperature and freezing cold. The genome sequence provides good basisto unveil the origin and evolution of ginseng and also supports practical gene chips which is useful for breeding and the ginseng industry.

인삼은 세계에서 가장 중요한 약용식물 중 하나이다. 본 연구실에서는 국립종자원에 최초로 등록된 인삼 품종 '천풍'을 이용하여 대략 3Gbp의 완성도 높은 유전체 서열과 60,000여개의 유전자를 동정하여 공개하였다. 인삼속 근연종들과의 비교유전체연구를 통해 종의 분화 시기 등을 추정하였고, 이를 통해 고려인삼의 기원과 두 번의 대륙이동을 통한 인삼속의 진화와 분포모델을 확립하였다. 인삼속 18종 중 2종 (고려인삼, 화기삼)은 24쌍의 염색체를 가지는 사배체 식물이며 나머지 16종은 12쌍의 염색체를 가지는 이배체 식물이다. 인삼속과 두릅나무속은 두릅나무과에 속하는 가장 가까운 식물로서 약 8백만년 전에 분화하였다. 인삼속은 약 6백만년 전 베트남 등의 동남아시아에서 러시아와 같은 동북아시아에 이르는 지역의 깊은 숲 속 서늘한 기후와 숲 속의 음지조건에 적응하며 음지식물로 진화했다. 그 기간은 빙하기와 간빙기가 반복되는 시기로 월동 능력이 없는 이배체 인삼종은 대부분 동북아시아 지역에서 멸종하였고 이 과정에 이배체간 종간 교잡종인 이질사배체가 약 2백만년전 만들어졌으며 한반도를 위시한 동북아시아를 중심으로 월동능력을 가진 고려인삼이 태동되었다고 추정된다. 북미에 분포하는 화기삼은 동북아시아 전역에 분포하던 고려인삼이 약 1백만년전에 빙하의 이동과 더불어 대륙간 이주를 통해 새로운 생태 환경에 적응하면서 분화되었다고 판단된다. 반면 대부분의 이배체 인삼종은 고온을 견디지 못하고 월동능력도 없어 동남아시아 지역에서 1,600미터 이상의 고산 지역으로 쫓겨 올라가 연중 서늘한 기후에서 생존하고 있다. 유전체 해독 정보는 인삼의 기원과 진화기작을 추정하는 학문적 성과 뿐 아니라 인삼산업을 보호하고 우수 인삼을 개발하기 위한 실용적인 분자육종 수단에도 매우 효율적으로 활용될 수 있다.

Keywords

References

  1. Lee C, Wen J. Phylogeny of Panax using chloroplast trnC-trnD intergenic region and the utility of trnC-trnD in interspecific studies of plants. Mol Phylogenet Evol 2004;31(3):894-903. https://doi.org/10.1016/j.ympev.2003.10.009
  2. Kim NH, Jayakodi M, Lee SC, Choi BS, Jang W, Lee J, Kim HH, Waminal NE, Lakshmanan M, Nguyen VB, et al. Genome and evolution of the shade‐requiring medicinal herb Panax ginseng. PlantBiotechnol J 2018;16(11):1904-17.
  3. Jayakodi M, Choi BS, Lee SC, Kim NH, Park JY, Jang W, Lakshmanan M, Mohan SV, Lee DY, Yang TJ. Ginseng Genome Database: an open-access platformfor genomics of Panax ginseng. BMC Plant Biol 2018;18(1):62. https://doi.org/10.1186/s12870-018-1282-9
  4. Choi HI, Kim NH, Kim JH, Choi BS, Ahn IO, Lee JS, Yang TJ. Development ofreproducible EST-derived SSR markers and assessment of genetic diversity in Panax ginseng cultivars and related species. J Ginseng Res 2011;35(4):399-412. https://doi.org/10.5142/jgr.2011.35.4.399
  5. Kim JH, Jung JY, Choi HI, Kim NH, Park JY, Lee Y, Yang TJ. Diversity and evolution of major Panax species revealed by scanning the entire chloroplast intergenic spacer sequences. Genet Resour Crop Evol 2013;60(2):413-25. https://doi.org/10.1007/s10722-012-9844-4
  6. Choi HI, Kim NH, Lee J, Choi BS, Kim KD, 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(4):1377-87. https://doi.org/10.1007/s10722-012-9926-3
  7. 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(6):e0117159. https://doi.org/10.1371/journal.pone.0117159
  8. 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(30):6298-306. https://doi.org/10.1021/acs.jafc.7b00925
  9. Kim K, Dong J, 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(1):4917. https://doi.org/10.1038/s41598-017-05218-y
  10. Lee J, Waminal NE, Choi HI, Perumal S, Lee SC, Jang W, Kim NH, Gao Lz, Yang TJ. Rapid amplification of four retrotransposon families promoted speciation and genome size expansion in the genus Panax. Sci Rep 2017;7(1):9045. https://doi.org/10.1038/s41598-017-08194-5
  11. Nguyen VB, Giang VNL, Waminal NE, Park HS, Kim NH, Jang W, Lee J, Yang TJ. Comprehensive comparative analysis of chloroplast genomes from seven Panax species and development of an authentication system based on speciesunique single nucleotide polymorphism markers. J Ginseng Res 2020;44(1):135-44. https://doi.org/10.1016/j.jgr.2018.06.003
  12. Choi HI, Waminal NE, Park HM, Kim NH, Choi BS, Park M, Choi D, Lim YP, Kwon SJ, Park BS, et al. Major repeat components covering one‐third of the ginseng (Panax ginseng CA Meyer) genome and evidence for allotetraploidy. Plant J 2014;77(6):906-16. https://doi.org/10.1111/tpj.12441
  13. Jang W, Kim NH, Lee J, Waminal NE, Lee SC, Jayakodi M, Choi HI, Park JY, Lee JE, Yang TJ. A glimpse of Panax ginseng genome structure revealed from ten BAC clone sequences obtained by SMRT sequencing platform. Plant Breed Biotechnol 2017;5(1):25-35. https://doi.org/10.9787/PBB.2017.5.1.25
  14. van Dijk EL, Jaszczyszyn Y, Naquin D, Thermes C. The third revolution in sequencing technology. Trends Genet 2018;34(9):666-81. https://doi.org/10.1016/j.tig.2018.05.008
  15. Soltis DE, Albert VA, Leebens‐Mack J, Bell CD, Paterson AH, ZhengC, Sankoff D, de Pamphilis CW, Wall PK, Soltis PS. Polyploidy and angiosperm diversification. Am J Bot 2009;96(1):336-48. https://doi.org/10.3732/ajb.0800079
  16. U N. Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn J Bot 1935;7(7):389-452.
  17. Chalhoub B, Denoeud F, Liu S, Parkin IA, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, et al. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 2014;345(6199):950-3. https://doi.org/10.1126/science.1253435
  18. Yang TJ, Kim JS, Kwon SJ, Lim KB, Choi BS, Kim JA, Jin M, Park JY, Lim MH, Kim HI, et al. Sequence-level analysis of the diploidization process in the triplicated FLOWERING LOCUS C region of Brassica rapa. Plant Cell 2006;18(6):1339-47. https://doi.org/10.1105/tpc.105.040535
  19. Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F. The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 2011;43(10):1035-9. https://doi.org/10.1038/ng.919
  20. Kim NH. Molecular characterization of whole genome duplication in Panax ginseng [dissertation]. Seoul: Seoul National University; 2015.
  21. Birky CW. Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 1995;92(25):11331-8. https://doi.org/10.1073/pnas.92.25.11331
  22. Palmer JD, Stein DB. Conservation of chloroplast genome structure among vascular plants. Curr Genet 1986;10(11):823-33. https://doi.org/10.1007/BF00418529
  23. 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(1):1-13.
  24. Wostemeyer J, Kreibich A. Repetitive DNA elements in fungi (Mycota): impact on genomic architecture and evolution. Curr Genet 2002;41(4):189-98. https://doi.org/10.1007/s00294-002-0306-y
  25. 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(1):1-11. https://doi.org/10.1186/s12870-014-0410-4
  26. Xia P, Li J, Wang R, Zhang Y, Guo H, Yan X, Liu Y, Liang Z. Comparative study on volatile oils of four Panax genus species in Southeast Asia by gas chromatography-mass spectrometry. Ind Crops Prod 2015;74:478-84. https://doi.org/10.1016/j.indcrop.2015.05.059
  27. Jayakodi M. Adaptive evolution of polyploid ginseng (Panax ginseng) revealed by genome annotation and comparative transcriptomes [dissertation]. Seoul: Seoul National University; 2018.
  28. Hollister JD. Polyploidy: adaptation to the genomic environment. New Phytol 2015;205(3):1034-9. https://doi.org/10.1111/nph.12939
  29. 인삼. http://www.seed.go.kr/seed/109/subview.do (검색일: 2021년 1월 8일)
  30. 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(3):298-307. https://doi.org/10.5142/jgr.2012.36.3.298
  31. Joh HJ, Kim NH, Jayakodi M, Jang W, Park JY, Kim YC, In JG, Yang TJ. Authentication of golden-berry P. ginseng cultivar 'Gumpoong' from a landrace 'Hwangsook' based on pooling method using chloroplast-derived markers. Plant Breed Biotechnol 2017;5(1):16-24. https://doi.org/10.9787/PBB.2017.5.1.16
  32. Jang W, Jang Y, Kim NH, Waminal NE, Kim YC, Lee JW, Yang TJ. Genetic diversity among cultivated and wild Panax ginseng populations revealed by high-resolution microsatellite markers. J Ginseng Res 2020;44(4):637-43. https://doi.org/10.1016/j.jgr.2019.05.008
  33. 장우종, 조우현, 양태진. 인삼 분자표지 개발 현황 및 활용. 종자과학과 산업: 한국종자연구회지 2020;16(1):9-21.