Acknowledgement
This work was carried out with the support of "Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ015903)" Rural Development Administration, Republic of Korea. This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. NRF-2021R1A4A1032888 to Y.H.Song and T.J.Yang).
References
- Yang W-z, Hu Y, Wu W-y, Ye M, Guo D-a. Saponins in the genus Panax L.(Araliaceae): a systematic review of their chemical diversity. Phytochemistry 2014;106:7-24. https://doi.org/10.1016/j.phytochem.2014.07.012
- Hou M, Wang R, Zhao S, Wang Z. Ginsenosides in Panax genus and their biosynthesis. Acta Pharmaceutica Sinica B 2021:1813-34.
- Kim NH, Jayakodi M, Lee SC, Choi BS, Jang W, Lee J, Kim HH, Waminal NE, Lakshmanan M, Nguyen Bv, et al. Genome and evolution of the shaderequiring medicinal herb Panax ginseng. Plant Biotechnol J 2018;16(11):1904-17. https://doi.org/10.1111/pbi.12926
- Kim K, Dong J, Wang Y, Park JY, Lee S-C, Yang T-J. Evolution of the Araliaceae family inferred from complete chloroplast genomes and 45S nrDNAs of 10 Panax-related species. Sci Rep 2017;7(1):1-9. https://doi.org/10.1038/s41598-016-0028-x
- Haralampidis K, Trojanowska M, Osbourn AE. Biosynthesis of triterpenoid saponins in plants. History and trends in bioprocessing and biotransformation. Springer; 2002. p. 31-49.
- Tang Q-Y, Chen G, Song W-L, Fan W, Wei K-H, He S-M, Zhang G-H, Tang J-R, Li Y, Lin Y. Transcriptome analysis of Panax zingiberensis identifies genes encoding oleanolic acid glucuronosyltransferase involved in the biosynthesis of oleanane-type ginsenosides. Planta 2019;249.2:393-406. https://doi.org/10.1007/s00425-018-2995-6
- Han JY, Jo H-J, Kwon EK, Choi YE. Cloning and characterization of oxidosqualene cyclases involved in taraxasterol, taraxerol and bauerenol triterpene biosynthesis in taraxacum coreanum. Plant Cell Physiol 2019;60(7):1595-603. https://doi.org/10.1093/pcp/pcz062
- Ladhari A, Chappell J. Unravelling triterpene biosynthesis through functional characterization of an oxidosqualene cyclase (OSC) from Cleome arabica L. Plant Physiology and Biochemistry 2019;144:73-84. https://doi.org/10.1016/j.plaphy.2019.09.035
- Abe I, Rohmer M, Prestwich GD. Enzymatic cyclization of squalene and oxidosqualene to sterols and triterpenes. Chem Rev 1993;93(6):2189-206. https://doi.org/10.1021/cr00022a009
- dela Pena IJI, Kim HJ, Botanas CJ, De La Pena JB, Van Le TH, Nguyen MD, Park JH, Cheong JH. The psychopharmacological activities of Vietnamese ginseng in mice: characterization of its psychomotor, sedative-hypnotic, antistress, anxiolytic, and cognitive effects. J Ginseng Res 2017;41.2:201-8. https://doi.org/10.1016/j.jgr.2016.03.005
- Song SB, Tung NH, Quang TH, Ngan NTT, Kim KE, Kim YH. Inhibition of TNF-α-mediated NF-κB transcriptional activity in HepG2 cells by dammarane-type saponins from Panax ginseng leaves. J Ginseng Res 2012;36(2):146-52. https://doi.org/10.5142/jgr.2012.36.2.146
- Gu C-Z, Lv J-J, Zhang X-X, Yan H, Zhu H-T, Luo H-R, Wang D, Yang C-R, Xu M, Zhang Y-J. Minor dehydrogenated and cleavaged dammarane-type saponins from the steamed roots of Panax notoginseng. Fitoterapia 2015;103:97-105. https://doi.org/10.1016/j.fitote.2015.03.014
- Yoshikawa M, Murakami T, Yashiro K, Yamahara J, Matsuda H, Saijoh R, Tanaka O. Bioactive saponins and glycosides. XI. Structures of new dammarane-type triterpene oligoglycosides, quinquenosides I, II, III, IV, and V, from American ginseng, the roots of Panax quinquefolium L. Chem Pharm Bull 1998;46(4):647-54. https://doi.org/10.1248/cpb.46.647
- Lee YS, Park H-S, Lee D-K, Jayakodi M, Kim N-H, Koo HJ, Lee S-C, Kim YJ, Kwon SW, Yang T-J. Integrated transcriptomic and metabolomic analysis of five Panax ginseng cultivars reveals the dynamics of ginsenoside biosynthesis. Frontiers in Plant Science 2017;8:1048. https://doi.org/10.3389/fpls.2017.01048
- Park H-W, In G, Kim J-H, Cho B-G, Han G-H, Chang I-M. Metabolomic approach for discrimination of processed ginseng genus (Panax ginseng and Panax quinquefolius) using UPLC-QTOF MS. J Ginseng Res 2014;38(1):59-65. https://doi.org/10.1016/j.jgr.2013.11.011
- Lu C, Zhao S, Wei G, Zhao H, Qu Q. biochemistry. Functional regulation of ginsenoside biosynthesis by RNA interferences of a UDP-glycosyltransferase gene in Panax ginseng and Panax quinquefolius. Plant Physiol Biochem 2017;111:67-76. https://doi.org/10.1016/j.plaphy.2016.11.017
- Zhao M, Lin Y, Wang Y, Li X, Han Y, Wang K, Sun C, Wang Y, Zhang M. Transcriptome analysis identifies strong candidate genes for ginsenoside biosynthesis and reveals its underlying molecular mechanism in Panax ginseng CA Meyer. Sci Rep 2019;9(1):1-10. https://doi.org/10.1038/s41598-018-37186-2
- Wei G, Yang F, Wei F, Zhang L, Gao Y, Qian J, Chen Z, Jia Z, Wang Y, Su HJ. Metabolomes and transcriptomes revealed the saponin distribution in root tissues of Panax quinquefolius and Panax notoginseng. J Ginseng Res 2020;44(6):757-69. https://doi.org/10.1016/j.jgr.2019.05.009
- Liu M-H, Yang B-R, Cheung W-F, Yang KY, Zhou H-F, Kwok JS-L, Liu G-C, Li X-F, Zhong S, Lee SM-Y, et al. Transcriptome analysis of leaves, roots and flowers of Panax notoginseng identifies genes involved in ginsenoside and alkaloid biosynthesis. BMC Genom 2015;16(1):1-12. https://doi.org/10.1186/1471-2164-16-1
- Zhang G-H, Ma C-H, Zhang J-J, Chen J-W, Tang Q-Y, He M-H, Xu X-Z, Jiang N-H, Yang S-C. Transcriptome analysis of Panax vietnamensis var. fuscidicus discovers putative ocotillol-type ginsenosides biosynthesis genes and genetic markers. BMC Genomics 2015;16(1):1-20. https://doi.org/10.1186/1471-2164-16-1
- Jayakodi M, Lee S-C, Park H-S, Jang W, Lee YS, Choi B-S, Nah GJ, Kim D-S, Natesan S, Sun CJ, et al. Transcriptome profiling and comparative analysis of Panax ginseng adventitious roots. J Ginseng Res 2014;38(4):278-88. https://doi.org/10.1016/j.jgr.2014.05.008
- Lee YS, Park H-S, Lee D-K, Jayakodi M, Kim N-H, Lee S-C, Kundu A, Lee D-Y, Kim YC, In JG, et al. Comparative analysis of the transcriptomes and primary metabolite profiles of adventitious roots of five Panax ginseng cultivars. J Ginseng Res 2017;41(1):60-8. https://doi.org/10.1016/j.jgr.2015.12.012
- Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014;30(15):2114-20. https://doi.org/10.1093/bioinformatics/btu170
- Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nature Biotechnology 2011;29(7):644-52. https://doi.org/10.1038/nbt.1883
- Fu L, Niu B, Zhu Z, Wu S, Li W, Cd-Hit. Accelerated for clustering the next-generation sequencing data. Bioinformatics 2012;28(23):3150-2. https://doi.org/10.1093/bioinformatics/bts565
- Katoh K, Misawa K, Kuma Ki, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acid Res 2002;30(14):3059-66. https://doi.org/10.1093/nar/gkf436
- Tamura K, Dudley J, Nei M, Kumar S. evolution. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007;24(8):1596-9. https://doi.org/10.1093/molbev/msm092
- Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Method 2012;9(4):357-9. https://doi.org/10.1038/nmeth.1923
- Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf 2011;12(1):1-16. https://doi.org/10.1186/1471-2105-12-1
- Chung M, Bruno VM, Rasko DA, Cuomo CA, Munoz JF, Livny J, Shetty AC, Mahurkar A, Hotopp JCD. Best practices on the differential expression analysis of multi-species RNA-seq. Genom Biol 2021;22(1):1-23. https://doi.org/10.1186/s13059-020-02207-9
- Fukushima K, Pollock DD. Amalgamated cross-species transcriptomes reveal organ-specific propensity in gene expression evolution. Nat Commun 2020;11(1):1-14. https://doi.org/10.1038/s41467-019-13993-7
- Kalamakis G, Brune D, Ravichandran S, Bolz J, Fan W, Ziebell F, Stiehl T, Martinez FC-, Kupke J, Zhao S, et al. Quiescence modulates stem cell maintenance and regenerative capacity in the aging brain. Cell 2019;176(6):1407-19. https://doi.org/10.1016/j.cell.2019.01.040
- Tsai C-C, Wu K-M, Chiang T-Y, Huang C-Y, Chou C-H, Li S-J, Chiang Y-C. Comparative transcriptome analysis of Gastrodia elata (Orchidaceae) in response to fungus symbiosis to identify gastrodin biosynthesis-related genes. BMC Genom 2016;17(1):1-16. https://doi.org/10.1186/s12864-016-2508-6
- Faraway JJ. Practical regression and ANOVA using R, vol. 168. Bath: University of Bath; 2002.
- Kang KB, Jayakodi M, Lee YS, Park H-S, Koo HJ, Choi IY, Kim DH, Chung YJ, Ryu B, Lee DY, et al. Identification of candidate UDP-glycosyltransferases involved in protopanaxadiol-type ginsenoside biosynthesis in Panax ginseng. Sci Rep 2018;8(1):1-10. https://doi.org/10.1038/s41598-018-30262-7
- Tsugawa H, Cajka T, Kind T, Ma Y, Higgins B, Ikeda K, Kanazawa M, VanderGheynst J, Fiehn O, Arita Ms-Dial M. data-independent MS/MS deconvolution for comprehensive metabolome analysis. Nat Method 2015;12(6):523-6. https://doi.org/10.1038/nmeth.3393
- Yang W-z, Ye M, Qiao X, Liu C-f, Miao W-j, Bo T, Tao H-y, Guo D-a. A strategy for efficient discovery of new natural compounds by integrating orthogonal column chromatography and liquid chromatography/mass spectrometry analysis: its application in Panax ginseng, Panax quinquefolium and Panax notoginseng to characterize 437 potential new ginsenosides. Anal Chim Acta 2012;739:56-66. https://doi.org/10.1016/j.aca.2012.06.017
- Mao Q, Bai M, Xu J-D, Kong M, Zhu L-Y, Zhu H, Wang Q, Li S-L. Discrimination of leaves of Panax ginseng and P. quinquefolius by ultra high performance liquid chromatography quadrupole/time-of-flight mass spectrometry based metabolomics approach. J Pharma Biomed Analysis 2014;97:129-40. https://doi.org/10.1016/j.jpba.2014.04.032
- Chu C, Xu S, Li X, Yan J, Liu LJ. Profiling the ginsenosides of three ginseng products by Lc-Q-Tof/Ms. J Food Sci 2013;78(5):C653-9. https://doi.org/10.1111/1750-3841.12102
- Wang H-P, Zhang Y-B, Yang X-W, Yang X-B, Xu W, Xu F, Cai S-Q, Wang Y-P, Xu Y-H, Zhang L-X. High-performance liquid chromatography with diode array detector and electrospray ionization ion trap time-of-flight tandem mass spectrometry to evaluate ginseng roots and rhizomes from different regions. Molecules 2016;21(5):603. https://doi.org/10.3390/molecules21050603
- Zhang L, Wu S, Chang X, Wang X, Zhao Y, Xia Y, Trigiano RN, Jiao Y, Chen F. The ancient wave of polyploidization events in flowering plants and their facilitated adaptation to environmental stress. Plant, Cell Environ 2020;43(12):2847-56. https://doi.org/10.1111/pce.13898
- Sumner LW, Amberg A, Barrett D, Beale MH, Beger R, Daykin CA, Fan TW-M, Fiehn O, Goodacre R, Griffin JL, et al. Proposed minimum reporting standards for chemical analysis. Metabolomics 2007;3(3):211-21. https://doi.org/10.1007/s11306-007-0082-2
- Darnet S, Rahier A. Plant sterol biosynthesis: identification of two distinct families of sterol 4alpha-methyl oxidases. Biochem J 2004;378(3):889-98. https://doi.org/10.1042/BJ20031572
- Sadre R, Kuo P, Chen J, Yang Y, Banerjee A, Benning C, Hamberger B. Cytosolic lipid droplets as engineered organelles for production and accumulation of terpenoid biomaterials in leaves. Nat Commun 2019;10(1):1-12. https://doi.org/10.1038/s41467-018-07882-8
- Boutte Y, Grebe M. Cellular processes relying on sterol function in plants. Curr Opin Plant Biol 2009;12(6):705-13. https://doi.org/10.1016/j.pbi.2009.09.013
- Augustin JM, Kuzina V, Andersen SB, Bak S. Molecular activities, biosynthesis and evolution of triterpenoid saponins. Phytochemistry 2011;72(6):435-57. https://doi.org/10.1016/j.phytochem.2011.01.015
- Sawai S, Saito K. Triterpenoid biosynthesis and engineering in plants. Front Plant Sci 2011;2:25. https://doi.org/10.3389/fpls.2011.00025
- Basyuni M, Oku H, Tsujimoto E, Kinjo K, Baba S, Takara K. Triterpene synthases from the Okinawan mangrove tribe, Rhizophoraceae. FEBS J 2007;274(19):5028-42. https://doi.org/10.1111/j.1742-4658.2007.06025.x
- Bennett RN, Wallsgrove RM. Secondary metabolites in plant defence mechanisms. New Phytol 1994;127(4):617-33. https://doi.org/10.1111/j.1469-8137.1994.tb02968.x
- Pozo D, Carlos J, Parra ER. Whole genome duplications in plants: an overview from Arabidopsis. Journal of Experimental Botany. J Exp Botany 2015;66(22):6991-7003. https://doi.org/10.1093/jxb/erv432
- Madani H, Escrich A, Hosseini B, Sanchez-Munoz R, Khojasteh A, Palazon J. ~ Effect of polyploidy induction on natural metabolite production in medicinal plants. Biomolecules 2021;11(6):899. https://doi.org/10.3390/biom11060899
- Parida BP, Misra BB. Is a plant's ploidy status reflected in its metabolome? J Postdoc Res 2015;1:11. https://doi.org/10.14304/SURYA.JPR.V3N4.1
- Kaensaksiri T, Soontornchainaksaeng P, Soonthornchareonnon N, Prathanturarug S. In vitro induction of polyploidy in Centella asiatica (L.) Urban. Plant Cell. Tissue Organ Cult (PCTOC) 2011;107(2):187-94. https://doi.org/10.1007/s11240-011-9969-8
- Gaynor ML, Lim-Hing S, Mason CM. Impact of genome duplication on secondary metabolite composition in non-cultivated species: a systematic meta-analysis. Annals of Botany 2020;126(3):363-76. https://doi.org/10.1093/aob/mcaa107
- Lee S-Y, Jeong J-J, Le THV, Eun S-H, Nguyen MD, Park JH, Ocotillol D-HKim. A majonoside R2 metabolite, ameliorates 2, 4, 6-trinitrobenzenesulfonic acid-induced colitis in mice by restoring the balance of Th17/Treg cells. J Agric Food Chem 2015;63(31):7024-31. https://doi.org/10.1021/acs.jafc.5b02183
- Van Le TH, Lee SY, Kim TR, Kim JY, Kwon SW, Nguyen NK, Park JH, Nguyen MD. Processed Vietnamese ginseng: preliminary results in chemistry and biological activity. J Ginseng Res 2014;38(2):154-9. https://doi.org/10.1016/j.jgr.2013.11.015
- Liu J, Xu Y, Yang J, Wang W, Zhang J, Zhang R, Meng QJ. Discovery, semisynthesis, biological activities, and metabolism of ocotillol-type saponins. J Ginseng Res 2017;41(3):373-8. https://doi.org/10.1016/j.jgr.2017.01.001
- Li Z, Wu CF, Pei G, Guo YY, Li X. Behavior. Antagonistic effect of pseudoginsenoside-F11 on the behavioral actions of morphine in mice. Pharmacol Biochem Behav 2000;66(3):595-601. https://doi.org/10.1016/S0091-3057(00)00260-4
- Vlahakis C, Hazebroek J. Phytosterol accumulation in canola, sunflower, and soybean oils: effects of genetics, planting location, and temperature. J Am Oil Chem Soc 2000;77(1):49-53. https://doi.org/10.1007/s11746-000-0008-6
- Geiser C, Mandakova T, Arrigo N, Lysak MA, Parisod C. Repeated whole-genome duplication, karyotype reshuffling, and biased retention of stress-responding genes in Buckler mustard. Plant Cell 2016;28(1):17-27. https://doi.org/10.1105/tpc.15.00791