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Genetic Transformation of Salvia miltiorrhiza

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Book cover The Salvia miltiorrhiza Genome

Part of the book series: Compendium of Plant Genomes ((CPG))

Abstract

Salvia miltiorrhiza is a valuable traditional Chinese medicinal herb. Due to the great importance of tanshinones and phenolic acids in S. miltiorrhiza, it is necessary to increase their yields to satisfy the rapidly growing demand. Many efforts have been made to elucidate the biosynthetic pathways of tanshinones and phenolic acids. This chapter describes two Agrobacterium-mediated S. miltiorrhiza transformation systems, named Agrobacterium rhizogenes-mediated hairy root transformation, and Agrobacterium tumefaciens-mediated ‘composite’ plant transformation, respectively. These systems provide a solid foundation for genetic engineering of S. miltiorrhiza to enhance these bioactive compounds. The achievements of S. miltiorrhiza metabolic engineering obtained through transformation are summarized. In addition, recent advances on the application of activation tagging mutagenesis (ATM) and CRISPR/Cas9 for mutation of genes in S. miltiorrhiza are discussed.

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References

  • Bai Z, Li W, Jia Y, Yue Z, Jiao J, Huang W, Xia P, Liang Z (2018) The ethylene response factor SmERF6 co-regulates the transcription of SmCPS1 and SmKSL1 and is involved in tanshinone biosynthesis in Salvia miltiorrhiza hairy roots. Planta 248:243–255

    Article  CAS  PubMed  Google Scholar 

  • Barker RF, Idler KB, Thompson DV, Kemp JD (1983) Nucleotide sequence of the T-DNA region from the Agrobacterium tumefaciens octopine Ti plasmid pTi15955. Plant Mol Biol 2(6):335–350

    Article  CAS  PubMed  Google Scholar 

  • Boulter ME, Croy E, Simpson P, Shields R, Shirsat AH (1990) Transformation of Brassica napus L. (oilseed rape) using Agrobacterium tumefaciens and Agrobacterium rhizogenes—a comparison. Plant Sci 70(1):91–99

    Google Scholar 

  • Byrne MC, Koplow J, David C, Tempé J, Chilton MD (1983) Structure of T-DNA in roots transformed by Agrobacterium rhizogenes. J Mol Appl Genet 2(2):201–209

    CAS  PubMed  Google Scholar 

  • Cao W, Wang Y, Shi M, Hao X, Zhao W, Wang Y, Ren J, Kai G (2018) Transcription factor SmWRKY1 positively promotes the biosynthesis of tanshinones in Salvia miltiorrhiza. Front Plant Sci 9:554

    Article  PubMed  PubMed Central  Google Scholar 

  • Chandra S (2012) Natural plant genetic engineer Agrobacterium rhizogenes: role of T-DNA in plant secondary metabolism. Biotechnol Lett 34(3):407–415

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Zhang Y, Qiakefu K, Zhang X, Han L, Hua W, Yan Y, Wang Z (2016) Overexpression of tomato Prosystemin (LePS) enhances pest resistance and the production of tanshinones in Salvia miltiorrhiza Bunge. J Agric Food Chem 64(41):7760–7769

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Chen F, Zhang Y, Song J (1999) Production of lithospermic acid B and rosmarinic acid in hairy root cultures of Salvia miltiorrhiza. J Ind Microbiol Biotechnol 22(3):133–138

    Article  CAS  Google Scholar 

  • Chen H, Yuan J, Chen F, Zhang Y, Song J (1997) Tanshinone production in Ti-transformed Salvia miltiorrhiza cell suspension cultures. J Biotechnol 58(3):147–156

    Article  CAS  PubMed  Google Scholar 

  • Cheng Q, Su P, Hu Y, He Y, Gao W, Huang L (2014) RNA interference-mediated repression of SmCPS (copalyldiphosphate synthase) expression in hairy roots of Salvia miltiorrhiza causes a decrease of tanshinones and sheds light on the functional role of SmCPS. Biotechnol Lett 36(2):363–369

    Article  CAS  PubMed  Google Scholar 

  • Crane C, Wright E, Dixon RA, Wang Z (2006) Transgenic Medicago truncatula plants obtained from Agrobacterium tumefaciens-transformed roots and Agrobacterium rhizogenes-transformed hairy roots. Planta 223(6):1344–1354

    Article  CAS  PubMed  Google Scholar 

  • Cui G, Duan L, Jin B, Qian J, Xue Z, Shen G, Snyder JH, Song J, Chen S, Huang L, Peters RJ, Qi X (2015) Functional divergence of diterpene syntheses in the medicinal plant Salvia miltiorrhiza. Plant Physiol 169(3):1607–1618

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dai S, Zheng P, Marmey P, Zhang S, Tian W, Chen S, Beachy RN, Fauquet C (2001) Comparative analysis of transgenic rice plants obtained by Agrobacterium-mediated transformation and particle bombardment. Mol Breed 7:25–33

    Article  CAS  Google Scholar 

  • Dai Z, Cui G, Zhou S, Zhang X, Huang L (2011) Cloning and characterization of a novel 3-hydroxy-3-methylglutaryl coenzyme A reductase gene from Salvia miltiorrhiza involved in diterpenoid tanshinone accumulation. J Plant Physiol 168(2):148–157

    Article  CAS  PubMed  Google Scholar 

  • de Frammond AJ, Barton KA, Chilton M (1983) Mini-Ti: a new vector strategy for plant genetic engineering. Nat Biotechnol 5:262–269

    Article  Google Scholar 

  • Deng C, Hao X, Shi M, Fu R, Wang Y, Zhang Y, Zhou W, Feng Y, Makunga NP, Kai G (2019) Tanshinone production could be increased by the expression of SmWRKY2 in Salvia miltiorrhiza hairy roots. Plant Sci 284:1–8

    Article  CAS  PubMed  Google Scholar 

  • Ding K, Pei T, Bai Z, Jia Y, Ma P, Liang Z (2017) SmMYB36, a novel R2R3-MYB transcription factor, enhances tanshinone accumulation and decreases phenolic acid content in Salvia miltiorrhiza hairy roots. Sci Rep 7(1):5104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gantet P, Memelink J (2002) Transcription factors: tools to engineer the production of pharmacologically active plant metabolites. Trends Pharmacol Sci 23:563–569

    Article  CAS  PubMed  Google Scholar 

  • Gao W, Sun H, Xiao H, Cui G, Hillwig ML, Jackson A, Wang X, Shen Y, Zhao N, Zhang L, Wang X, Peters RJ, Huang L (2014) Combining metabolomics and transcriptomics to characterize tanshinone biosynthesis in Salvia miltiorrhiza. BMC Genom 15:73

    Article  Google Scholar 

  • Ge Q, Zhang Y, Hua W, Wu Y, Jin X, Song S, Wang Z (2015) Combination of transcriptomic and metabolomic analyses reveals a JAZ repressor in the jasmonate signaling pathway of Salvia miltiorrhiza. Sci Rep 5:14048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ge X, Wu J (2005) Tanshinone production and isoprenoid pathways in Salvia miltiorrhiza hairy roots induced by Ag+ and yeast elicitor. Plant Sci 168(2):487–491

    Article  CAS  Google Scholar 

  • Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67(1):16–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Georgiev MI, Agostini E, Ludwig-Müller J, Xu J (2012) Genetically transformed roots: from plant disease to biotechnological resource. Trends Biotechnol 30(10):528–537

    Article  CAS  PubMed  Google Scholar 

  • Gu X, Chen J, Xiao Y, Di P, Xuan H, Zhou X, Zhang L, Chen W (2012) Overexpression of allene oxide cyclase promoted tanshinone/phenolic acid production in Salvia miltiorrhiza. Plant Cell Rep 31(12):2247–2259

    Article  CAS  PubMed  Google Scholar 

  • Guo J, Ma X, Cai Y, Ma Y, Zhan Z, Zhou YJ, Liu W, Guan M, Yang J, Cui G, Kang L, Yang L, Shen Y, Tang J, Lin H, Ma X, Jin B, Liu Z, Peters RJ, Zhao ZK, Huang L (2016) Cytochrome P450 promiscuity leads to a bifurcating biosynthetic pathway for tanshinones. New Phytol 210(2):525–534

    Article  CAS  PubMed  Google Scholar 

  • Guo J, Zhou YJ, Hillwig ML, Shen Y, Yang L, Wang Y, Zhang X, Liu W, Peters RJ, Chen X, Zhao ZK, Huang L (2013) CYP76AH1 catalyzes turnover of miltiradiene in tanshinones biosynthesis and enables heterologous production of ferruginol in yeasts. Proc Natl Acad Sci 110(29):12108–12113

    Article  PubMed  PubMed Central  Google Scholar 

  • Hao G, Jiang X, Feng L, Tao R, Li Y, Huang L (2016) Cloning, molecular characterization and functional analysis of a putative R2R3-MYB transcription factor of the phenolic acid biosynthetic pathway in S. miltiorrhiza Bge. f. alba. Plant Cell Tiss Org Cult 124(1):151–168

    Google Scholar 

  • Hao G, Shi R, Tao R, Fang Q, Jiang X, Ji H, Feng L, Huang L (2013) Cloning, molecular characterization and functional analysis of 1-hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate reductase (HDR) gene for diterpenoid tanshinone biosynthesis in Salvia miltiorrhiza Bge. f. alba. Plant Physiol Biochem 70:21–32

    Article  CAS  PubMed  Google Scholar 

  • Hao X, Shi M, Cui L, Xu C, Zhang Y, Kai G (2015) Effects of methyl jasmonate and salicylic acid on tanshinone production and biosynthetic gene expression in transgenic Salvia miltiorrhiza hairy roots. Biotechnol Appl Biochem 62(1):24–31

    Article  CAS  PubMed  Google Scholar 

  • Hatamoto H, Boulter ME, Shirsat AH, Croy EJ, Ellis JR (1990) Recovery of morphologically normal transgenic tobacco from hairy roots co-transformed with Agrobacterium rhizogenes and a binary vector plasmid. Plant Cell Rep 9:88–92

    Article  CAS  PubMed  Google Scholar 

  • Hayashi H, Czaja I, Lubenow H, Schell J, Walden R (1992) Activation of a plant gene by T-DNA tagging: auxin-independent growth in vitro. Science 258:1350–1353

    Article  CAS  PubMed  Google Scholar 

  • Ho HS, Vishwakarma RK, Chen ECF, Tsay HS (2013) Activation tagging in Salvia miltiorrhiza can cause increased leaf size and accumulation of tanshinone I and IIA in its roots. Bot Stud 54(1):37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoekema A, Hirsh PR, Hooykaas PJJ, Schilperoort RA (1983) A binary plant vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303:179–180

    Article  CAS  Google Scholar 

  • Hood EE, Gelvin SB, Melchers LS, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2(4):208–218

    Article  CAS  Google Scholar 

  • Huang Q, Sun M, Yuan T, Wang Y, Shi M, Lu S, Tang B, Pan J, Wang Y, Kai G (2019) The AP2/ERF transcription factor SmERF1L1 regulates the biosynthesis of tanshinones and phenolic acids in Salvia miltiorrhiza. Food Chem 274:368–375

    Article  CAS  PubMed  Google Scholar 

  • Jia Y, Bai Z, Pei T, Ding K, Liang Z, Gong Y (2017) The protein kinase SmSnRK2.6 positively regulates phenolic acid biosynthesis in Salvia miltiorrhiza by interacting with SmAREB1. Front Plant Sci 8:1384

    Google Scholar 

  • Joos H, Timmerman B, Montagu MV, Schell J (1983) Genetic analysis of transfer and stabilization of Agrobacterium DNA in plant cells. EMBO J 2(12):2151–2160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kai G, Xu H, Zhou C, Liao P, Xiao J, Luo X, You L, Zhang L (2011) Metabolic engineering tanshinone biosynthetic pathway in Salvia miltiorrhiza hairy root cultures. Metab Eng 13(3):319–327

    Article  CAS  PubMed  Google Scholar 

  • Kohli A, Gahakwa D, Vain P, Laurie DA, Christou P (1999) Transgene expression in rice engineered through particle bombardment: molecular factors controlling stable expression and transgene silencing. Planta 208:88–97

    Article  CAS  Google Scholar 

  • Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383–396

    Article  CAS  Google Scholar 

  • Lee CY, Agrawal DC, Wang CS, Yu SM, Chen JJ, Tsay HS (2008) T-DNA activation tagging as a tool to isolate Salvia miltiorrhiza transgenic lines for higher yields of tanshinones. Planta Med 74(07):780–786

    Article  CAS  PubMed  Google Scholar 

  • Lemmers M, De Beuckeleer M, Holsters M, Zambryski P, Depicker A, Hernalsteens JP, Van Montagu M, Schell J (1980) Internal organization, boundaries and integration of Ti-plasmid DNA in nopaline crown gall tumours. J Mol Biol 144(3):353–376

    Article  CAS  PubMed  Google Scholar 

  • Li B, Cui G, Shen G, Zhan Z, Huang L, Chen J, Qi X (2017) Targeted mutagenesis in the medicinal plant Salvia miltiorrhiza. Sci Rep 7:43320

    Article  PubMed  PubMed Central  Google Scholar 

  • Li S, Wu Y, Kuang J, Wang H, Du T, Huang Y, Zhang Y, Cao X, Wang Z (2018) SmMYB111 is a key factor to phenolic acid biosynthesis and interacts with both SmTTG1 and SmbHLH51 in Salvia miltiorrhiza. J Agric Food Chem 66(30):8069–8078

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Wu S, Xu J, Sui C, Wei J (2017a) Application of CRISPR/Cas9 in plant biology. Acta Pharm Sin B 7(3):292–302

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Sun G, Zhong Z, Ji L, Zhang Y, Zhou J, Zheng X, Deng K (2017b) Overexpression of AtEDT1 promotes root elongation and affects medicinal secondary metabolite biosynthesis in roots of transgenic Salvia miltiorrhiza. Protoplasma 254(4):1617–1625

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Yang S, Cheng Y, Liu D, Zhang Y, Deng K, Zheng X (2015) Production of herbicide-resistant medicinal plant Salvia miltiorrhiza transformed with the bar gene. Appl Biochem Biotechnol 177(7):1456–1465

    Article  CAS  PubMed  Google Scholar 

  • Lu X, Tang KX, Li P (2016) Plant metabolic engineering strategies for the production of pharmaceutical terpenoids. Front Plant Sci 7:1647

    PubMed  PubMed Central  Google Scholar 

  • Luo H, Zhu Y, Song J, Xu L, Sun C, Zhang X, Xu Y, He L, Sun W, Xu H, Wang B, Li X, Li C, Liu J, Chen S (2014) Transcriptional data mining of Salvia miltiorrhiza in response to methyl jasmonate to examine the mechanism of bioactive compound biosynthesis and regulation. Physiol Plant 152(2):241–255

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Ma X, Meng F, Zhan Z, Guo J, Huang L (2016) RNA interference targeting CYP76AH1 in hairy roots of Salvia miltiorrhiza reveals its key role in the biosynthetic pathway of tanshinones. Biochem Bioph Res Commun 477(2):155–160

    Article  CAS  Google Scholar 

  • Mei XD, Cao YF, Che YY, Li J, Shang ZP, Zhao WJ, Qiao YJ, Zhang JY (2019) Danshen: a phytochemical and pharmacological overview. Chin J Nat Med 17(1):59–80

    Google Scholar 

  • Mugnier J (1988) Establishment of new axenic hairy root lines by inoculation with Agrobacterium rhizogenes. Plant Cell Rep 7:9–12

    Article  CAS  PubMed  Google Scholar 

  • Ngo TM, Tran PT, Hoang LS, Lee JH, Min BS, Kim JA (2019) Diterpenoids isolated from the root of Salvia miltiorrhiza and their anti-inflammatory activity. Nat Prod Res. https://doi.org/10.1080/14786419.2019.1596098

    Article  PubMed  Google Scholar 

  • Rao SR, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20(2):101–153

    Article  CAS  PubMed  Google Scholar 

  • Schell J, Van Montagu M (1977) The Ti-plasmid of Agrobacterium tumefaciens, a natural vector for the introduction of nif genes in plants? In: Hollaender A, Burris RH, Day PR, Hardy RW, Helinski DR, Lamborg MR, Owens L, Valentine RC (eds) Genetic engineering for nitrogen fixation. Basic Life Sci 9(2):159

    Google Scholar 

  • Sharma P, Padh H, Shrivastava N (2013) Hairy root cultures: a suitable biological system for studying secondary metabolic pathways in plants. Eng Life Sci 13(1):62–75

    Article  CAS  Google Scholar 

  • Shi M, Luo X, Ju G, Li L, Huang S, Zhang T, Wang H, Kai G (2016a) Enhanced diterpene tanshinone accumulation and bioactivity of transgenic Salvia miltiorrhiza hairy roots by pathway engineering. J Agric Food Chem 64(12):2523–2530

    Article  CAS  PubMed  Google Scholar 

  • Shi M, Luo X, Ju G, Yu X, Hao X, Huang Q, Xiao J, Cui L, Kai G (2014) Increased accumulation of the cardio-cerebrovascular disease treatment drug tanshinone in Salvia miltiorrhiza hairy roots by the enzymes 3-hydroxy-3-methylglutaryl CoA reductase and 1-deoxy-D-xylulose 5-phosphate reductoisomerase. Funct Integr Genomic 14(3):603–615

    Article  CAS  Google Scholar 

  • Shi M, Zhou W, Zhang J, Huang S, Wang H, Kai G (2016b) Methyl jasmonate induction of tanshinone biosynthesis in Salvia miltiorrhiza hairy roots is mediated by jasmonate zim-domain repressor proteins. Sci Rep 6:20919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimomura K, Kitazawa T, Okamura N, Yagi A (1991) Tanshinone production in adventitious roots and regenerates of Salvia miltiorrhiza. J Nat Prod 54:1583

    Article  CAS  Google Scholar 

  • Song J, Wang Z (2011) RNAi-mediated suppression of the phenylalanine ammonia-lyase gene in Salvia miltiorrhiza causes abnormal phenotypes and a reduction in rosmarinic acid biosynthesis. J Plant Res 124:183

    Article  CAS  PubMed  Google Scholar 

  • Song J, Zhang Y, Qi J, Lu G (1997) Selection of a high tanshinone–producing crown gall strain and production of tanshinone in the strain. Chin J Biotechnol 13(3):207–210

    CAS  PubMed  Google Scholar 

  • Su C, Ming Q, Rahman K, Han T, Qin L (2015) Salvia miltiorrhiza: Traditional medicinal uses, chemistry, and pharmacology. Chin J Nat Med 13(3):163–182

    CAS  PubMed  Google Scholar 

  • Sun M, Shi M, Wang Y, Huang Q, Yuan T, Wang Q, Wang C, Zhou W, Kai G (2018) The biosynthesis of phenolic acids is positively regulated by the JA-responsive transcription factor ERF115 in Salvia miltiorrhiza. J Exp Bot 70(1):243–254

    Article  Google Scholar 

  • Suzuki K, Hattori Y, Uraji M, Ohta N, Iwata K, Murata K, Kato A, Yoshida K (2000) Complete nucleotide sequence of a plant tumor-inducing Ti plasmid. Gene 242:331–336

    Article  CAS  PubMed  Google Scholar 

  • Suzuki Y, Uemura S, Saito Y, Murofushi N, Schmitz G, Theres K, Yamaguchi I (2001) A novel transposon tagging element for obtaining gain-of-function mutants based on a self-stabilizing Ac derivative. Plant Mol Biol 45:123–131

    Article  CAS  PubMed  Google Scholar 

  • Tan Y, Wang KY, Wang N, Li G, Liu D (2014) Ectopic expression of human acidic fibroblast growth factor 1 in the medicinal plant, Salvia miltiorrhiza, accelerates the healing of burn wounds. BMC Biotechnol 14:74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tao W, Deng K, Zhang Q, Gao Y, Liu Y, Yang M, Zhang L, Zheng X, Wang C, Liu Z, Chen C, Zhang Y (2017) Modulating AtDREB1C expression improves drought tolerance in Salvia miltiorrhiza. Front Plant Sci 8:52

    Google Scholar 

  • Tepfer D (1990) Genetic transformation using Agrobacterium rhizogenes. Physiol Plant 79:140–146

    Article  CAS  Google Scholar 

  • Tsutomu N, Hitoshi M, Masao N, Hideko H, Kaisuke Y (1983) Production of cryptotanshinone and ferruginol in cultured cells of Salvia miltiorrhiza. Phytochem 22(3):721–722

    Article  Google Scholar 

  • Van Larebeke N, Engler G, Holsters M, Van den Elsacker S, Zaenen J, Schilperoort RA, Schell J (1974) Large plasmid in Agrobacterium tumefaciens essential for crown gall-inducing ability. Nature 252:169–170

    Article  PubMed  Google Scholar 

  • Wang B, Niu J, Li B, Huang Y, Han L, Liu Y, Zhou W, Hu S, Li L, Wang D, Wang S, Cao X, Wang Z (2018a) Molecular characterization and overexpression of SmJMT increases the production of phenolic acids in Salvia miltiorrhiza. Int J Mol Sci 19(12):3788

    Article  CAS  PubMed Central  Google Scholar 

  • Wang D, Song Y, Chen Y, Yao W, Li Z, Liu W, Yue S, Wang Z (2013) Metabolic pools of phenolic acids in Salvia miltiorrhiza are enhanced by co-expression of Antirrhinum majus Delila and Rosea1 transcription factors. Biochem Eng J 74(Complete):115–120

    Google Scholar 

  • Wang D, Yao W, Song Y, Liu W, Wang Z (2012a) Molecular characterization and expression of three galactinol synthase genes that confer stress tolerance in Salvia miltiorrhiza. J Plant Physiol 169(18):1838–1848

    Article  CAS  PubMed  Google Scholar 

  • Wang G, Chen J, Yi B, Tan H, Zhang L, Chen W (2017a) HPPR encodes the hydroxyphenylpyruvate reductase required for the biosynthesis of hydrophilic phenolic acids in Salvia miltiorrhiza. Chin J Nat Med 15(12):0917–0927

    Google Scholar 

  • Wang H, Wei T, Wang X, Zhang L, Yang M, Chen L, Song W, Wang C, Chen C (2018b) Transcriptome analyses from mutant Salvia miltiorrhiza reveals important roles for SmGASA4 during plant development. Int J Mol Sci 19(7):2088

    Article  CAS  PubMed Central  Google Scholar 

  • Wang Z, Cui L, Chen C, Liu X, Yan Y, Wang Z (2012b) Downregulation of cinnamoyl CoA reductase affects lignin and phenolic acids biosynthesis in Salvia miltiorrhiza Bunge. Plant Mol Biol Rep 30:1229

    Article  CAS  Google Scholar 

  • Wang Z, Ge Q, Chen C, Jin X, Cao X, Wang Z (2017b) Function analysis of caffeoyl-COA O-methyltransferase for biosynthesis of lignin and phenolic acid in Salvia miltiorrhiza. Appl Biochem Biotechnol 181(2):562–572

    Article  CAS  PubMed  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webb KJ, Robbins MP, Mizen S (1994) Expression of GUS in primary transformants and segregation patterns of GUS, TL- and TR-DNA in the T1 generation of hairy root transformants of Lotus corniculatus. Transgenic Res 3:232–240

    Article  CAS  Google Scholar 

  • Wei T, Deng K, Gao Y, Liu Y, Yang M, Zhang L, Zheng X, Wang C, Song W, Chen C, Zhang Y (2016a) Arabidopsis DREB1B in transgenic Salvia miltiorrhiza increased tolerance to drought stress without stunting growth. Plant Physiol Biochem 104:17–28

    Article  CAS  PubMed  Google Scholar 

  • Wei T, Deng K, Liu D, Gao Y, Liu Y, Yang M, Zhang L, Zheng X, Wang C, Song W, Chen C, Zhang Y (2016b) Ectopic expression of DREB transcription factor, AtDREB1A, confers tolerance to drought in transgenic Salvia miltiorrhiza. Plant Cell Physiol 57(8):1593–1609

    Article  CAS  PubMed  Google Scholar 

  • Wei WJ, Zhou PP, Lin CJ, Wang WF, Li Y, Gao K (2017) Diterpenoids from Salvia miltiorrhiza and their immune-modulating activity. J Agric Food Chem 65(29):5985–5993

    CAS  PubMed  Google Scholar 

  • White FF, Nester EW (1980) Relationship of plasmids responsible for hairy root and crown gall tumorigenicity. J Bacteriol 144:710–720

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu C, Karioti A, Rohr D, Bilia AR, Efferth T (2016) Production of rosmarinic acid and salvianolic acid B from callus culture of Salvia miltiorrhiza with cytotoxicity towards acute lymphoblastic leukemia cells. Food Chem 201:292–297

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Zhang Y, Li L, Guo X, Wang B, Cao X, Wang Z (2018) AtPAP1 interacts with and activates SmbHLH51, a positive regulator to phenolic acids biosynthesis in Salvia miltiorrhiza. Front Plant Sci 9:1687

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiao Y, Gao S, Di P, Chen J, Chen W, Zhang L (2009) Methyl jasmonate dramatically enhances the accumulation of phenolic acids in Salvia miltiorrhiza hairy root cultures. Physiol Plant 137(1):1–9

    Article  CAS  PubMed  Google Scholar 

  • Xiao Y, Gao S, Di P, Chen J, Chen W, Zhang L (2010) Lithospermic acid B is more responsive to silver ions (Ag+) than rosmarinic acid in Salvia miltiorrhiza hairy root cultures. Biosci Rep 30(1):33–40

    Article  CAS  Google Scholar 

  • Xiao Y, Zhang L, Gao S, Saechao S, Di P, Chen J, Chen W (2011) The c4 h, tat, hppr and hppd genes prompted engineering of rosmarinic acid biosynthetic pathway in Salvia miltiorrhiza hairy root cultures. PLoS One 6(12):e29713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xing B, Liang L, Liu L, Hou Z, Yang D, Yan K, Zhang X, Liang Z (2018a) Overexpression of SmbHLH148 induced biosynthesis of tanshinones as well as phenolic acids in Salvia miltiorrhiza hairy roots. Plant Cell Rep 37(12):1681–1692

    CAS  PubMed  Google Scholar 

  • Xing B, Yang D, Yu H, Zhang B, Yan K, Zhang X, Han R, Liang Z (2018b) Overexpression of SmbHLH10 enhances tanshinones biosynthesis in Salvia miltiorrhiza hairy roots. Plant Sci 276:229–238

    Article  CAS  PubMed  Google Scholar 

  • Xu H, Song J, Luo H, Zhang Y, Li Q, Zhu Y, Xu J, Li Y, Song C, Wang B, Sun W, Shen G, Zhang X, Qian J, Ji A, Xu Z, Luo X, He L, Li C, Sun C, Yan H, Cui G, Li X, Li X, Wei J, Liu J, Wang Y, Hayward A, Nelson D, Ning Z, Peters RJ, Qi X, Chen S (2016) Analysis of the genome sequence of the medicinal plant Salvia miltiorrhiza. Mol Plant 9:949–952

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Peters RJ, Weirather J, Luo H, Liao B, Zhang X, Zhu Y, Ji A, Zhang B, Hu S, Au K, Song J, Chen S (2015) Full-length transcriptome sequences and splice variants obtained by a combination of sequencing platforms applied to different root tissues of Salvia miltiorrhiza and tanshinone biosynthesis. Plant J 82(6):951–961

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Song J (2017) The 2-oxoglutarate-dependent dioxygenase superfamily participates in tanshinone production in Salvia miltiorrhiza. J Exp Bot 68(9):2299–2308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan Y, Wang Z (2007) Genetic transformation of the medicinal plant Salvia miltiorrhiza by Agrobacterium tumefaciens-mediated method. Plant Cell Tiss Org Cult 88(2):175–184

    Article  CAS  Google Scholar 

  • Yang N, Zhou W, Su J, Wang X, Li L, Wang L, Cao X, Wang Z (2017) Overexpression of SmMYC2 increases the production of phenolic acids in Salvia miltiorrhiza. Front Plant Sci 8:1804

    Article  PubMed  PubMed Central  Google Scholar 

  • Zambryski P, Holsters M, Kruger K, Depicker A, Schell J, Van Montagu M, Goodman HM (1980) Tumor DNA structure in plant cells transformed by A. tumefaciens. Science 209:1385–1391

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Yan Q, Cheuk WK, Wu J (2004) Enhancement of tanshinone production in Salvia miltiorrhiza hairy root culture by Ag+ elicitation and nutrient feeding. Planta Med 70(02):147–151

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Liu X, Xie D, Chen R, Tao X, Zou J, Dai J (2013a) Two new diterpenoids from cell cultures of Salvia miltiorrhiza. Chem Pharm Bull 61(5):576–580

    Article  CAS  Google Scholar 

  • Zhang G, Tian Y, Zhang J, Shu L, Yang S, Wang W, Sheng J, Dong Y, Chen W (2015a) Hybrid de novo genome assembly of the Chinese herbal plant danshen (Salvia miltiorrhiza Bunge). GigaScience 4:62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Zhou L, Zheng X, Zhang J, Yang L, Tan R, Zhao S (2017) Overexpression of SmMYB9b enhances tanshinone concentration in Salvia miltiorrhiza hairy roots. Plant Cell Rep 36(8):1297–1309

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Li H, Liang X, Yan Y, Xia P, Jia Y, Liang Z (2015b) Enhanced production of phenolic acids in Salvia miltiorrhiza hairy root cultures by combing the RNAi-mediated silencing of chalcone synthase gene with salicylic acid treatment. Biochem Eng J 103:185–192

    Article  CAS  Google Scholar 

  • Zhang S, Ma P, Yang D, Li W, Liang Z, Liu Y, Liu F (2013b) Cloning and characterization of a putative R2R3 MYB transcriptional repressor of the rosmarinic acid biosynthetic pathway from Salvia miltiorrhiza. PLoS ONE 8(9):e73259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Guan H, Dai Z, Guo J, Shen Y, Cui G, Gao W, Huang L (2015c) Functional analysis of the isopentenyl diphosphate isomerase of Salvia miltiorrhiza via color complementation and RNA interference. Molecules 20(11):20206–20218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Yan Y, Wang Z (2010) The Arabidopsis PAP1 transcription factor plays an important role in the enrichment of phenolic acids in Salvia miltiorrhiza. J Agr Food Chem 58(23):12168–12175

    Article  CAS  Google Scholar 

  • Zhang Y, Yan Y, Wu Y, Hua W, Chen C, Ge Q, Wang Z (2014) Pathway engineering for phenolic acid accumulations in Salvia miltiorrhiza by combinational genetic manipulation. Metab Eng 21:71–80

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Zhou L, Wu J (2010) Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Appl Microbiol Biotechnol 87(1):137–144

    Article  CAS  PubMed  Google Scholar 

  • Zhao S, Zhang J, Tan R, Yang L, Zheng X (2015) Enhancing diterpenoid concentration in Salvia miltiorrhiza hairy roots through pathway engineering with maize C1 transcription factor. J Exp Bot 66(22):7211

    Article  CAS  PubMed  Google Scholar 

  • Zhi B, Alfermann AW (1993) Diterpenoid production in hairy root cultures of Salvia miltiorrhiza. Phytochemistry 32(3):699–703

    Article  Google Scholar 

  • Zhou L, Zuo Z, Chow MS (2005) Danshen: an overview of its chemistry, pharmacology, pharmacokinetics, and clinical use. J Clin Pharmacol 45(12):1345–1359

    Article  CAS  PubMed  Google Scholar 

  • Zhou W, Huang F, Li S, Wang Y, Zhou C, Shi M, Wang J, Chen Y, Wang Y, Wang H, Kai G (2016a) Molecular cloning and characterization of two 1-deoxy-d-xylulose-5-phosphate synthase genes involved in tanshinone biosynthesis in Salvia miltiorrhiza. Mol Breed 36(9):124

    Article  CAS  Google Scholar 

  • Zhou Y, Sun W, Chen J, Tan H, Xiao Y, Li Q, Ji Q, Gao S, Chen L, Chen S, Zhang L, Chen W (2016b) SmMYC2a and SmMYC2b played similar but irreplaceable roles in regulating the biosynthesis of tanshinones and phenolic acids in Salvia miltiorrhiza. Sci Rep 6:22852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Z, Tan H, Li Q, Chen J, Gao S, Wang Y, Chen W, Zhang L (2018) CRISPR/Cas9-mediated efficient targeted mutagenesis of RAS in Salvia miltiorrhiza. Phytochemistry 148:63–70

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (81872964, 81773836) and the CAMS Innovation Fund for Medical Sciences (CIFMS) (2016-I2M-3-016).

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Correspondence to Shanfa Lu .

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Wang, M., Lu, S. (2019). Genetic Transformation of Salvia miltiorrhiza. In: Lu, S. (eds) The Salvia miltiorrhiza Genome. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-030-24716-4_13

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