Panax ginseng genome examination for ginsenoside biosynthesis

GigaScience

Volumn 6, Issue 11, 2017, Pages

  Xu, Jiang ^a   Chu, Yang ^a   Liao, Baosheng ^a   Xiao, Shuiming ^a   Yin, Qinggang ^a   Bai, Rui ^a   Su, He ^a,b   Dong, Linlin ^a   Li, Xiwen ^a   Qian, Jun ^a   Zhang, Jingjing ^a   Zhang, Yujun ^a   Zhang, Xiaoyan ^a   Wu, Mingli ^a   Zhang, Jie ^a   Li, Guozheng ^a   Zhang, Lei ^a   Chang, Zhenzhan ^c   Zhang, Yuebin ^d   Jia, Zhengwei ^e   Liu, Zhixiang ^a   Afreh, Daniel ^f   Nahurira, Ruth ^f   Zhang, Lianjuan ^a   Cheng, Ruiyang ^a   Zhu, Yingjie ^a   Zhu, Guangwei ^a   Rao, Wei ^e   Zhou, Chao ^e   Qiao, Lirui ^e   Huang, Zhihai ^b   Cheng, Yung Chi ^g   Chen, Shilin ^a   more..

^a INSTITUTE OF CHINESE MATERIA MEDICA   (China)

^b GUANGDONG PROVINCIAL HOSPITAL OF CHINESE MEDICINE   (China)

^c PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^d DALIAN INSTITUTE OF CHEMICAL PHYSICS   (China)

^e WATERS CORPORATION   (United States)

^f AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

^g YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Genome; Ginsenosides; Mass spectrometry imaging; Panax ginseng

Indexed keywords

3 HYDROXY 3 METHYLGLUTARYL COENZYME A; GENOMIC DNA; GINSENOSIDE; GLYCOSYLTRANSFERASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; MEVALONIC ACID; SAPONIN; TRANSCRIPTOME;

ARTICLE; BARK; BIOSYNTHESIS; CATALYSIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EXON; FRUIT; GENE CLUSTER; GENE EXPRESSION; GENE IDENTIFICATION; GENOME ANALYSIS; GINSENG; HETEROZYGOSITY; MOLECULAR DOCKING; MULTIGENE FAMILY; NEXT GENERATION SEQUENCING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYTOCHEMISTRY; PLANT DEVELOPMENT; PLANT GENE; PLANT GENOME; PLANT ROOT; PRIORITY JOURNAL; RNA SEQUENCE; SEQUENCE ANALYSIS; TANDEM REPEAT; GENETICS; METABOLISM; MOLECULAR GENETICS; PANAX;

GENOME, PLANT; GINSENOSIDES; GLYCOSYLTRANSFERASES; HYDROXYMETHYLGLUTARYL COA REDUCTASES; MEVALONIC ACID; MOLECULAR SEQUENCE ANNOTATION; PANAX;

EID: 85041189341     PISSN: None     EISSN: 2047217X     Source Type: Journal    
DOI: 10.1093/gigascience/gix093     Document Type: Article

References (99)

1. Hemmerly TE. A ginseng farm in Lawrence County, Tennessee. Econ Bot 1977;31(2):160-2.
2. Leung KW. Pharmacology of Ginsenosides. In: Ramawat KG, Ḿ erillon J-M, eds. Natural Products. Springer: Berlin Heidelberg; 2013:3497-514.
3. Leung K, Wong A. Pharmacology of ginsenosides: a literature review. Chin Med 2010;5(1):20.
4. Yun TK. Brief Introduction of Panax ginseng C.A. Meyer. J Korean Med Sci 2001;16(Suppl):S3-5.
5. Zhang Y, Li G, Jiang C, et al. Tissue-specific distribution of ginsenosides in different aged ginseng and antioxidant activity of ginseng leaf. Molecules 2014;19(11):17381-99.
6. Fukuda N, Shan S, Tanaka H, et al. New staining methodology: eastern blotting for glycosides in the field of Kampo medicines. J Nat Med 2006;60(1):21-7.
7. Yokota S, Onohara Y, Shoyama Y. Immunofluorescence and immunoelectron microscopic localization of medicinal substance, Rb1, in several plant parts of Panax ginseng. CDDT 2011;8(1):51-9.
8. Christensen LP, Jensen M, Kidmose U. Simultaneous determination of ginsenosides and polyacetylenes in American ginseng root (Panax quinquefolium L.) by high-performance liquid chromatography. J Agric Food Chem 2006;54(24):8995-9003.
9. Tani T, Kubo M, Katsuki T, et al. Histochemistry II. Ginsenosides in ginseng (Panax ginseng, root). J Nat Prod 1981;44(4):401-7.
10. Augustin JM, Kuzina V, Andersen SB, et al. Molecular activities, biosynthesis and evolution of triterpenoid saponins. Cheminform 2011;72(28):435-57.
11. Haralampidis K, Trojanowska M, Osbourn AE. Biosynthesis of triterpenoid saponins in plants. Adv Biochem Eng Biotechnol 2002;75(75):31-49.
12. Thimmappa R, Geisler K, Louveau T, et al. Triterpene biosynthesis in plants. Annu Rev Plant Biol 2014;65(1):225-57.
13. Lee M, Jeong J, Seo J, et al. Enhanced triterpene and phytosterol biosynthesis in Panax ginseng overexpressing squalene synthase gene. Plant Cell Physiol 2004;45(8):976-84.
14. Han J, In J, Kwon Y, et al. Regulation of ginsenoside and phytosterol biosynthesis by RNA interferences of squalene epoxidase gene in Panax ginseng. Phytochemistry 2010;71(1):36-46.
15. Phillips DR, Rasbery JM, Bartel B, et al. Biosynthetic diversity in plant triterpene cyclization. Curr Opin Plant Biol 2006;9(3):305-14.
16. Han J, Kim H, Kwon Y, et al. The Cyt P450 enzyme CYP716A47 catalyzes the formation of protopanaxadiol from dammarenediol-II during ginsenoside biosynthesis in Panax ginseng. Plant Cell Physiol 2011;52(12):2062-73.
17. Han J-Y, Kim M-J, Ban Y-W, et al. The involvement of -amyrin 28-oxidase (CYP716A52v2) in oleanane-type ginsenoside biosynthesis in Panax ginseng. Plant Cell Physiol 2013;54(12):2034-46.
18. JennerH, Townsend B, Osbourn A. Unravelling triterpene glycoside synthesis in plants: phytochemistry and functional genomics join forces. Planta 2005;220(4):503-6.
19. Li C, Zhu Y, Guo X, et al. Transcriptome analysis reveals ginsenosides biosynthetic genes, microRNAs and simple sequence repeats in Panax ginseng C. A. Meyer. BMC Genomics 2013;14(1):245.
20. Achnine L, Huhman DV, Farag MA, et al. Genomics-based selection and functional characterization of triterpene glycosyltransferases from the model legume Medicago truncatula. Plant J 2005;41(6):875-87.
21. Meesapyodsuk D, Balsevich J, Reed DWet al. Saponin biosynthesis in Saponaria vaccaria. cDNAs encoding beta-amyrin synthase and a triterpene carboxylic acid glucosyltransferase. Plant Physiol 2007;143(2):959-69.
22. Augustin JM, Drok S, Shinoda T, et al. UDPglycosyltransferases from the UGT73C subfamily in Barbarea vulgaris catalyze sapogenin 3-O-glucosylation in saponinmediated insect resistance. Plant Physiol 2012;160(4):1881-95.
23. Shibuya M, Nishimura K, Yasuyama N, et al. Identification and characterization of glycosyltransferases involved in the biosynthesis of soyasaponin I in Glycine max. FEBS Lett 2010;584(11):2258-64.
24. Wang P, Wei Y, Fan Y, et al. Production of bioactive ginsenosides Rh2 and Rg3 by metabolically engineered yeasts. Metab Eng 2015;29:97-105.
25. Jung S, Kim W, Park SC, et al. Two ginseng UDPglycosyltransferases synthesize ginsenoside Rg3 and Rd. Plant Cell Physiol 2014;55(12):2177-88.
26. Yan X, Fan Y, Wei W, et al. Production of bioactive ginsenoside compound K in metabolically engineered yeast. Cell Res 2014;24(6):770-3.
27. Wei W, Wang P, Wei Y, et al. Characterization of Panax ginseng UDP-glycosyltransferases catalyzing protopanaxatriol and biosyntheses of bioactive ginsenosides F1 and Rh1 in metabolically engineered yeasts. Mol Plant 2015;8(9):1412-24.
28. Xu J, Chu Y, Xiao S. Ginseng genome examination for ginsenoside biosynthesis. GigaScience Database. 2017. http://dx.doi.org/10.5524/100348.
29. Grabherr MG, Haas BJ, Yassour M, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011;29(7):644-52.
30. Simao FA, Waterhouse RM, Ioannidis P, et al. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 2015;31(19): 3210-2.
31. Choi H, Waminal NE, Park HM, et al. Major repeat components covering one-third of the ginseng (Panax ginseng C.A. Meyer) genome and evidence for allotetraploidy. Plant J 2014;77(6):906-16.
32. http://www.uniprot.org/taxonomy/4054.
33. Ruhfel BR, Gitzendanner MA, Soltis PS, et al. From algae to angiosperms-inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. BMC Evol Biol 2014;14 1:23.
34. Liang Y, Zhao S. Progress in understanding of ginsenoside biosynthesis. Plant Biol 2008;10(4):415-21.
35. Wang K, Jiang S, Sun C, et al. The spatial and temporal transcriptomic landscapes of ginseng, Panax ginseng C. A. Meyer. Sci Rep 2016;5 1:18283.
36. Chen S, Song J, Sun C, et al. Herbal genomics: examining the biology of traditional medicines. Science 2015;347(6219):S27-9.
37. Zhihai H, Jiang X, Shuiming X, et al. Comparative optical genome analysis of two pangolin species: Manis pentadactyla and Manis javanica. Gigascience 2016;5(1):1-5.
38. Guan R, Zhao Y, Zhang H, et al. Draft genome of the living fossil Ginkgo biloba. Gigascience 2016;5(1):49.
39. Cai J, Liu X, Vanneste K, et al. Corrigendum: the genome sequence of the orchid Phalaenopsis equestris. Nat Genet 2015;47(2):186.
40. Paterson AH, Bowers JE, Bruggmann R, et al. The Sorghum bicolor genome and the diversification of grasses. Nature 2009;457(7229):551-6.
41. Mach J. Mass spectrometry imaging with single-cell resolution: spatial distribution of lipids in cotton seeds. Plant Cell Online 2012;24(2):371.
42. Li B, Hansen SH, Janfelt C. Direct imaging of plant metabolites in leaves and petals by desorption electrospray ionization mass spectrometry. Int J Mass Spectrom 2013;348(2):15-22.
43. Schramek N, Huber C, Schmidt S, et al. Biosynthesis of ginsenosides in field-grown Panax ginseng. JSM Biotechnol Biomed Eng 2014;2(1):1033.
44. Kim Y, Zhang D, Yang D. Biosynthesis and biotechnological production of ginsenosides. Biotechnol Adv 2015;33(6):717-35.
45. Kim T, Han J, Huh GH, et al. Expression and functional characterization of three squalene synthase genes associated with saponin biosynthesis in Panax ginseng. Plant Cell Physiol 2011;52(1):125-37.
46. Kim Y-J, Lee OR, Oh JY, et al. Functional analysis of 3-hydroxy-3-methylglutaryl coenzyme a reductase encoding genes in triterpene saponin-producing ginseng. Plant Physiol 2014;165(1):373-87.
47. Yang W, Zhang Y, Wu W, et al. Approaches to establish Q-markers for the quality standards of traditional Chinese medicines. Acta Pharmaceutica Sinica B 2017;7(4):439-46.
48. Jiang H, Lei R, Ding S, et al. Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics 2014;15(1):182.
49. Luo R, Liu B, Xie Y, et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 2012;1(1):18.
50. Chikhi R, Medvedev P. Informed and automated k-mer size selection for genome assembly. Bioinformatics 2014;30(1):31-7.
51. Boetzer M, Henkel CV, Jansen HJ, et al. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011;27(4):578-9.
52. Li R, Zhu H, Ruan J, et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 2010;20(2):265-72.
53. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009;25(14):1754-60.
54. Zdobnov EM, Tegenfeldt F, Kuznetsov D, et al. OrthoDB v9.1: cataloging evolutionary and functional annotations for animal, fungal, plant, archaeal, bacterial and viral orthologs. Nucleic Acids Res 2017;45(D1):D744-9.
55. Altschul SF, Gish W, Miller W, et al. Basic local alignment search tool. J Mol Biol 1990;215(3):403-10.
56. http://tophat.cbcb.umd.edu/.
57. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012;9(4):357-9.
58. http://cufflinks.cbcb.umd.edu/.
59. Trapnell C, Hendrickson DG, Sauvageau M, et al. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 2013;31(1):46-53.
60. https://github.com/tanghaibao/Goatools.
61. http://kobas.cbi.pku.edu.cn/home.do.
62. Xie C, Mao X, Huang J, et al. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 2011;39(suppl?2):W316-22.
63. Langfelder P, Horvath S.WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 2008;9 1:559.
64. Edgar RC, Myers EW. PILER: identification and classification of genomic repeats. Bioinformatics 2005;21(Suppl 1):i152-8.
65. http://www.repeatmasker.org.
66. Xu Z, Wang H. LTR FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res 2007;35(Web Server):W265-8.
67. Campbell MS, Law M, Holt C, et al. MAKER-P: a tool kit for the rapid creation, management, and quality control of plant genome annotations. Plant Physiol 2014;164(2): 513-24.
68. Johnson AD, Handsaker RE, Pulit SL, et al. SNAP: a web-based tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics 2008;24(24):2938-9.
69. Deng Y, Li J, Wu S, et al. Integrated nr database in protein annotation system and its localization. Comput Engineer 2006;32(5):71-2.
70. Koonin EV, Fedorova ND, Jackson JD, et al. A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes. Genome Biol 2004;5(2):R7.
71. Apweiler R, Bairoch A, Wu CH, et al. UniProt: the universal protein knowledgebase. Nucleic Acids Res 2004;32(90001):D115-9.
72. Ashburner M, Ball CA, Blake JA, et al. Gene ontology: tool for the unification of biology. Nat Genet 2000;25(1):25-9.
73. Moriya Y, Itoh M, Okuda S, et al. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 2007;35:W182-5. http://www.genome.jp/tools/kaas/.
74. Kanehisa M, Goto S, Kawashima S, et al. The KEGG resource for deciphering the genome. Nucleic Acids Res 2003;32(suppl 1):D277-80.
75. Li L. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003;13(9):2178-89.
76. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32(5):1792-7.
77. Talavera G, Castresana J, Kjer K, et al. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007;56(4):564-77.
78. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014;30(9):1312-3.
79. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Bioinformatics 1997;13(5): 555-6.
80. Huang C, Sun R, Hu Y, et al. Resolution of Brassicaceae phylogeny using nuclear genes uncovers nested radiations and supports convergent morphological evolution. Mol Biol Evol 2016;33(2):394-412.
81. Barreda VD, Palazzesi L, Telleŕia MC, et al. Early evolution of the angiosperm clade Asteraceae in the Cretaceous of Antarctica. Proc Natl Acad Sci U S A 2015;112(35): 10989-94.
82. Jeanmougin F, Thompson JD, Gouy M, et al. Multiple sequence alignment with Clustal X. Trends Biochem Sci 1998;23(10):403-5.
83. Tamura K, Dudley J, Nei M, et al. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007;24(8):1596-9.
84. https://www.mn-am.com/onlinedemos/corinademointeractive.
85. http://swissmodel.expasy.org.
86. Schwede T. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 2003;31(13): 3381-5.
87. http://bioinfo3D.cs.tau.ac.il/Patchdock.
88. Duhovny D, Nussinov R, Wolfson HJ. Efficient unbound docking of rigid molecules. Lect Notes Comput Sci 2002;2452:185-200.
89. Schneidman-Duhovny D, Inbar Y, Nussinov R, et al. Patch-Dock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res 2005;33(Web Server):W363-7.
90. Seeliger D, de Groot BL, Ligand docking and binding site analysis with PyMOL and Autodock/Vina. J Comput Aided Mol Des 2010;24(5):417-22.
91. Taira S, Ikeda R, Yokota N, et al. Mass spectrometric imaging of ginsenosides localization in Panax ginseng root. Am J Chin Med 2010;38(03):485-93.
92. Osbourn A, Goss RJM, Field RA. The saponins -polar isoprenoids with important and diverse biological activities. Nat Prod Rep 2011;28(7):1261-8.
93. Sawai S, Saito K. Triterpenoid biosynthesis and engineering in plants. Front Plant Sci 2011;2(25):25.
94. Han J, Hwang H, Choi S, et al. Cytochrome P450 CYP716A53v2 catalyzes the formation of protopanaxatriol from protopanaxadiol during ginsenoside biosynthesis in Panax ginseng. Plant Cell Physiol 2012;53(9):1535-45.
95. Chen S, Song J. Herbgenomics. China J Chin Materia Medica. 2016;41(21):3881-9.
96. Chen S, Xu J, Liu C, et al. Genome sequence of the model medicinal mushroom Ganoderma lucidum. Nat Commun 2012;3(2):913.
97. International Rice Genome Sequencing Project. The map-based sequence of the rice genome. Nature 2005;436(7052):793-800.
98. Jaillon O, Aury J-M, Noel B, et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007;449(7161):463-7.
99. Massoni J, Couvreur TL, Sauquet H. Five major shifts of diversification through the long evolutionary history of Magnoliidae (angiosperms). BMC Evol Biol 2015;15:49.