Abstract
Salidroside is a precious phenylethanoid glycoside derived from Rhodiola genus plants, which possesses a broad spectrum of biological properties for application in the cosmetic, medical and food fields. As the supply of salidroside is severely subject to the natural Rhodiola sources, sustainable production of salidroside with more economical and effective approaches has become a research hotspot in recent years. In this review, the biosynthesis pathways and enzymes involved in salidroside production in plants were elucidated in depth. Furthermore, efforts towards enhancement of salidroside production, including cell and tissue culture, enzymatic catalysis, metabolic engineering of micro-organisms were introduced comprehensively. Lastly, the strategies for product development of salidroside are presented with discussions on future prospects for the biosynthesis of salidroside. Given that there is still a certain distance between the current microbial productivity and industrialization requirement, more wisdom is in demand for dynamic regulation of cell growth and product accumulation, specific adsorption of the target compound as well as utilization of more economical carbon sources, so as to boost industrialization of salidroside via microbial fermentation.
Similar content being viewed by others
References
Amsterdam JD, Panossian AG (2016) Rhodiola rosea L. as a putative botanical antidepressant. Phytomedicine 23:770–783. https://doi.org/10.1016/j.phymed.2016.02.009
Bai Y, Bi H, Zhuang Y, Liu C, Cai T, Liu X, Zhang X, Liu T, Ma Y (2014) Production of salidroside in metabolically engineered Escherichia coli. Sci Rep 4:6640. https://doi.org/10.1038/srep06640
Bi Y, Wang Z, Mao Y, Zheng S, Zhang H, Shi H (2012) Ionic liquid effects on the activity of β-Glycosidase for the synthesis of salidroside in co-solvent systems. Chin J Catal 33:1161–1165. https://doi.org/10.1016/s1872-2067(11)60395-1
Bongaerts J, Kramer M, Muller U, Raeven L, Wubbolts M (2001) Metabolic engineering for microbial production of aromatic amino acids and derived compounds. Metab Eng 3:289–300. https://doi.org/10.1006/mben.2001.0196
Chiang HM, Chen HC, Wu CS, Wu PY, Wen KC (2015) Rhodiola plants: chemistry and biological activity. J Food Drug Anal 23:359–369. https://doi.org/10.1016/j.jfda.2015.04.007
Chu YH, Chen CJ, Wu SH, Hsieh JF (2014) Inhibition of xanthine oxidase by Rhodiola crenulata extracts and their phytochemicals. J Food Drug Anal 62:3742–3749. https://doi.org/10.1021/jf5004094
Chung D, Kim SY, Ahn JH (2017) Production of three phenylethanoids, tyrosol, hydroxytyrosol, and salidroside, using plant genes expressing in Escherichia coli. Sci Rep 7:2578. https://doi.org/10.1038/s41598-017-02042-2
Dou X, Ding Q, Lai S, Jiang F, Song Q, Zhao X, Fu A, Moustaidmoussa N, Su D, Li S (2020) Salidroside alleviates lipotoxicity-induced cell death through inhibition of TLR4/MAPKs pathway, and independently of AMPK and autophagy in AML-12 mouse hepatocytes. J Funct Foods 65:103691. https://doi.org/10.1016/j.jff.2019.103691
Fan M, Xu S, Xia S, Zhang X (2007) Effect of different preparation methods on physicochemical properties of salidroside liposomes. J Food Drug Anal 55:3089. https://doi.org/10.1021/jf062935q
Fan MH, Xu SY, Xia SQ, Zhang XM (2008) Preparation of salidroside nano-liposomes by ethanol injection method and in vitro release study. Eur Food Res Technol 227:167–174. https://doi.org/10.1007/s00217-007-0706-9
Fang DL, Chen Y, Xu B, Ren K, He ZY, He LL, Lei Y, Fan CM, Song XR (2014) Development of lipid-shell and polymer core nanoparticles with water-soluble Salidroside for anti-cancer therapy. J Control Release 15:3373–3388. https://doi.org/10.3390/ijms15033373
Grech-Baran M, Syklowska-Baranek K, Pietrosiuk A (2015) Biotechnological approaches to enhance salidroside, rosin and its derivatives production in selected Rhodiola spp. in vitro cultures. Phytochem Rev 14:657–674. https://doi.org/10.1007/s11101-014-9368-y
Guo W, Huang Q, Liu H, Hou S, Niu S, Jiang Y, Bao X, Shen Y, Fang X (2019) Rational engineering of chorismate-related pathways in Saccharomyces cerevisiae for improving tyrosol production. Front Bioeng Biotech 7:152. https://doi.org/10.3389/fbioe.2019.00152
Guo W, Huang Q, Feng Y, Tan T, Niu S, Hou S, Chen Z, Du Z-Q, Shen Y, Fang X (2020) Rewiring central carbon metabolism for tyrosol and salidroside production in Saccharomyces cerevisiae. Biotechnol Bioeng 117:2410–2419. https://doi.org/10.1002/bit.27370
Gyorgy Z, Tolonen A, Neubauer P, Hohtola A (2005) Enhanced biotransformation capacity of Rhodiola rosea callus cultures for glycosid production. Plant Cell Tiss Organ Cult 83:129–135. https://doi.org/10.1007/s11240-005-4010-8
Gyorgy Z, Jaakola L, Neubauer P, Hohtola A (2009) Isolation and genotype-dependent, organ-specific expression analysis of a Rhodiola rosea cDNA encoding tyrosine decarboxylase. J Plant Physiol 166:1581–1586. https://doi.org/10.1016/j.jplph.2009.03.016
Hu GS, Hur YJ, Jia JM, Lee JH, Chung YS, Yi YB, Yun DJ, Park SK, Kim DH (2011) Effects of 2-aminoindan-2-phosphonic acid treatment on the accumulation of salidroside and four phenylethanoid glycosides in suspension cell culture of Cistanche deserticola. Plant Cell Rep 30:665–674. https://doi.org/10.1007/s00299-010-0997-3
Hu GS, Jia JM, Doh Hoon K (2014) Effects of feeding tyrosine and phenylalanine on the accumulation of phenylethanoid glycosides to Cistanche deserticola cell suspension culture. Chin J Nat Med 12:367–372. https://doi.org/10.1016/S1875-5364(14)60045-5
Jiang J, Yin H, Wang S, Zhuang Y, Liu S, Liu T, Ma Y (2018) Metabolic engineering of Saccharomyces cerevisiae for high-level production of Salidroside from glucose. J Agr Food Chem 66:4431–4438. https://doi.org/10.1021/acs.jafc.8b01272
Ju R, Huang R, Zhou J, Li R, Zhou P, Zhang Z, Xiang F, Xu D, Liu W, Ma X, Zhang Q, Lu W (2011) Separation of injectable salidroside by column chromatography of macroporous resins for treating myocardial ischemia. Sci China Chem 55:1435–1444. https://doi.org/10.1007/s11426-011-4471-z
Kang DY, Sp N, Kim DH, Joung YH, Lee HG, Park YM, Yang YM (2018) Salidroside inhibits migration, invasion and angiogenesis of MDA-MB 231 TNBC cells by regulating EGFR/Jak2/STAT3 signaling via MMP2. Int J Oncol 53:877–885. https://doi.org/10.3892/ijo.2018.4430
Kapoor S, Sharma A, Bhardwaj P, Sood H, Saxena S, Chaurasia OP (2019) Enhanced production of phenolic compounds in compact callus aggregate suspension cultures of Rhodiola imbricata Edgew. Appl Biochem Biotech 187:817–837. https://doi.org/10.1007/s12010-018-2851-y
Kim YJ, Zhang DB, Yang DC (2015) Biosynthesis and biotechnological production of ginsenosides. Biotechnol Adv 33:717–735. https://doi.org/10.1016/j.biotechadv.2015.03.001
Kolewe ME, Gaurav V, Roberts SC (2008) Pharmaceutically active natural product synthesis and supply via plant cell culture technology. Mol Pharmaceut 5:243–256. https://doi.org/10.1021/mp7001494
Krajewskapatan A, Dreger M, Lowicka A, Gorskapaukszta M, Mscisz A, Mielcarek S, Baraniak M, Buchwald W, Furmanowa M, Mrozikiewicz PM (2007) Chemical investigations of biotransformed Rhodiola rosea callus tissue. Herba Polonica 53(4):77–87
Krajewska-Patan A, Dreger M, Buchwald W, Górska-Paukszta M, Mrozikiewicz PM (2009) Callus tissues of Rhodiola kirilowii (Regel) maxim—dynamic of growth and active compounds production. Herba Polonica 55:222–230
Krivoruchko A, Nielsen J (2015) Production of natural products through metabolic engineering of Saccharomyces cerevisiae. Curr Opin Biotechnol 35:7–15. https://doi.org/10.1016/j.copbio.2014.12.004
Lai M-C, Lin J-G, Pai P-Y, Lai M-H, Lin Y-M, Yeh Y-L, Cheng S-M, Liu Y-f, Huang C-Y, Lee S-D (2014) Protective effect of salidroside on cardiac apoptosis in mice with chronic intermittent hypoxia. Int J Cardiol 174:565–573. https://doi.org/10.1016/j.ijcard.2014.04.132
Lan X, Chang K, Zeng L, Liu X, Qiu F, Zheng W, Quan H, Liao Z, Chen M, Huang W, Liu W, Wang Q (2013) Engineering salidroside biosynthetic pathway in hairy root cultures of Rhodiola crenulata based on metabolic characterization of tyrosine decarboxylase. PLoS ONE 8:e75459. https://doi.org/10.1371/journal.pone.0075459
Li X, Sipple J, Pang Q, Du W (2012) Salidroside stimulates DNA repair enzyme Parp-1 activity in mouse HSC maintenance. Blood 119:4162–4173. https://doi.org/10.1182/blood-2011-10-387332
Li F, Yuan Y, Li H, Zhan Z, Kang L, Li M, Yang B, Huang L (2015) Infrared-assisted extraction of salidroside from the root of Rhodiola crenulata with a novel ionic liquid that dissolves cellulose. Rsc Adv 5:47326–47333. https://doi.org/10.1039/c5ra07969a
Li H, Piao XC, Gao R, Jin MY, Jiang J, Lian ML (2016) Effect of several physicochemical factors on callus biomass and bioactive compound accumulation of R-sachalinensis bioreactor culture. In Vitro Cell Dev Biol Plant 52:241–250. https://doi.org/10.1007/s11627-016-9758-5
Li M, Xu T, Zhou F, Wang M, Song H, Xiao X, Lu B (2018) Neuroprotective effects of four phenylethanoid Glycosides on H2O2-induced apoptosis on PC12 cells via the Nrf2/ARE pathway. Int J Mol Sci 19:1135. https://doi.org/10.3390/ijms19041135
Li T, Zhang W, Kang X, Yang R, Li R, Huang L, Chen J, Yang Q, Sun X (2020) Salidroside protects dopaminergic neurons by regulating the mitochondrial MEF2D-ND6 pathway in the MPTP/MPP(+) -induced model of Parkinson’s disease. J Neurochem 153:276–289. https://doi.org/10.1111/jnc.14868
Liu Z, Li X, Simoneau AR, Jafari M, Zi X (2012) Rhodiola rosea extracts and salidroside decrease the growth of bladder cancer cell lines via inhibition of the mTOR pathway and induction of autophagy. Mol Carcinogen 51:257–267. https://doi.org/10.1002/mc.20780
Liu X, Wen S, Yan F, Liu K, Liu L, Wang L, Zhao S, Ji X (2018a) Salidroside provides neuroprotection by modulating microglial polarization after cerebral ischemia. J Neuroinflamm 15:39. https://doi.org/10.1186/s12974-018-1081-0
Liu X, Li XB, Jiang J, Liu ZN, Qiao B, Li FF, Cheng JS, Sun X, Yuan YJ, Qiao J, Zhao GR (2018b) Convergent engineering of syntrophic Escherichia coli coculture for efficient production of glycosides. Metab Eng 47:243–253. https://doi.org/10.1016/j.ymben.2018.03.016
Liu Y, Tang H, Liu X, Chen H, Feng N, Zhang J, Wang C, Qiu M, Yang J, Zhou X (2019) Frontline Science: reprogramming COX-2, 5-LOX, and CYP4A-mediated arachidonic acid metabolism in macrophages by salidroside alleviates gouty arthritis. J Leukoc Biol 105:11–24. https://doi.org/10.1002/JLB.3HI0518-193R
Liu H, Tian Y, Zhou Y, Kan Y, Wu T, Xiao W, Luo Y (2020) Multi-modular engineering of Saccharomyces cerevisiae for high-titre production of tyrosol and salidroside. Microb Biotechnol. https://doi.org/10.1111/1751-7915.13667
Luo X, Bao N, Chen L, Sun J (2017) Pharmacological activities and progress in structure modification of Salidroside. Med Chem 07(03):818–823. https://doi.org/10.4172/2161-0444.1000434
Lutke-Eversloh T, Stephanopoulos G (2005) Feedback inhibition of chorismate mutase/prephenate dehydrogenase (TyrA) of Escherichia coli: generation and characterization of tyrosine-insensitive mutants. Appl Environ Microb 71:7224–7228. https://doi.org/10.1128/Aem.71.11.7224-7228.2005
Luttik MA, Vuralhan Z, Suir E, Braus GH, Pronk JT, Daran JM (2008) Alleviation of feedback inhibition in Saccharomyces cerevisiae aromatic amino acid biosynthesis: quantification of metabolic impact. Metab Eng 10:141–153. https://doi.org/10.1016/j.ymben.2008.02.002
Ma LQ, Liu BY, Gao DY, Pang XB, Lu SY, Yu HS, Wang H, Yan F, Li ZQ, Li YF, Ye HC (2007) Molecular cloning and overexpression of a novel UDP-glucosyltransferase elevating salidroside levels in Rhodiola sachalinensis. Plant Cell Rep 26:989–999. https://doi.org/10.1007/s00299-007-0317-8
Ma LQ, Gao DY, Wang YN, Wang HH, Zhang JX, Pang XB, Hu TS, Lu SY, Li GF, Ye HC, Li YF, Wang H (2008) Effects of overexpression of endogenous phenylalanine ammonia-lyase (PALrs1) on accumulation of salidroside in Rhodiola sachalinensis. Plant Biol 10:323–333. https://doi.org/10.1111/j.1438-8677.2007.00024.x
Ma C, Tang J, Wang H, Tao G, Gu X, Hu L (2009) Preparative purification of salidroside from Rhodiola rosea by two-step adsorption chromatography on resins. J Sep Sci 32:185–191. https://doi.org/10.1002/jssc.200800438
Mao Y, Li Y, Yao N (2007) Simultaneous determination of salidroside and tyrosol in extracts of Rhodiola L. by microwave assisted extraction and high-performance liquid chromatography. J Pharmaceut Biomed 45:510–515. https://doi.org/10.1016/j.jpba.2007.05.031
Marchev AS, Dinkova-Kostova AT, Gyorgy Z, Mirmazloum I, Aneva IY, Georgiev MI (2016) Rhodiola rosea L.: from golden root to green cell factories. Phytochem Rev 15:515–536. https://doi.org/10.1007/s11101-016-9453-5
McChesney JD, Venkataraman SK, Henri JT (2007) Plant natural products: Back to the future or into extinction? Phytochemistry 68:2015–2022. https://doi.org/10.1016/j.phytochem.2007.04.032
Min Tong A, Ya LuW, He XuJ, Qiang Lin G (2004) Use of apple seed meal as a new source of beta-glucosidase for enzymatic glucosylation of 4-substituted benzyl alcohols and tyrosol in monophasic aqueous-dioxane medium. Bioorg Med Chem Lett 14:2095–20977. https://doi.org/10.1016/j.bmcl.2004.02.042
Mirmazloum I, Ladanyi M, Beinrohr L, Kiss-Baba E, Kiss A, Gyorgy Z (2019) Identification of a novel UDP-glycosyltransferase gene from Rhodiola rosea and its expression during biotransformation of upstream precursors in callus culture. Int J Biol Macromol 136:847–858. https://doi.org/10.1016/j.ijbiomac.2019.06.086
Moghassemi S, Hadjizadeh A (2014) Nano-niosomes as nanoscale drug delivery systems: An illustrated review. J Control Release 185:22–36. https://doi.org/10.1016/j.jconrel.2014.04.015
Nicolai K, Menezes R, Foito A, da Henriques S, Marcelo D, Braga A, Dekker W, Méndez Sevillano D, Rosado-Ramos R, Jardim C, Oliveira J (2018) Identification and microbial production of the raspberry phenol salidroside that is active against Huntington’s disease. Plant Physiol. https://doi.org/10.1104/pp.18.01074
Nocon J, Steiger M, Mairinger T, Hohlweg J, Rumayer H, Hann S, Gasser B, Mattanovich D (2016) Increasing pentose phosphate pathway flux enhances recombinant protein production in Pichia pastoris. Appl Microbiol Biot 100:5955–5963. https://doi.org/10.1007/s00253-016-7363-5
O’Connor SE (2015) Engineering of secondary metabolism. Annu Rev Genet 49:71–94. https://doi.org/10.1146/annurev-genet-120213-092053
Pandey RP, Parajuli P, Koffas MAG, Sohng JK (2016) Microbial production of natural and non-natural flavonoids: pathway engineering, directed evolution and systems/synthetic biology. Biotechnol Adv 34:634–662. https://doi.org/10.1016/j.biotechadv.2016.02.012
Peng LH, Xu SY, Shan YH, Wei W, Liu S, Zhang CZ, Wu JH, Liang WQ, Gao JQ (2014a) Sequential release of salidroside and paeonol from a nanosphere-hydrogel system inhibits ultraviolet B-induced melanogenesis in guinea pig skin. Int J Nanomed 9:1897–1908. https://doi.org/10.2147/IJN.S59290
Peng LH, Xu SY, Shan YH, Wei W, Shuai L, Zhang CZ, Wu JH, Liang WQ, Gao JQ (2014b) Sequential release of salidroside and paeonol from a nanosphere-hydrogel system inhibits ultraviolet B-induced melanogenesis in guinea pig skin. Int J Nanomed 2014:1897–1908. https://doi.org/10.2147/IJN.S59290
Qian EW, Ge DT, Kong SK (2012) Salidroside protects human erythrocytes against hydrogen peroxide-induced apoptosis. J Nat Prod 75:531–537. https://doi.org/10.1021/np200555s
Qin Y, Liu H, Li M, Zhai D, Tang Y, Yang L, Qiao K, Yang J, Zhong W, Zhang Q (2018) Salidroside improves the hypoxic tumor microenvironment and reverses the drug resistance of platinum drugs via HIF-1α signaling pathway. EBioMedicine 38:25–36. https://doi.org/10.1016/j.ebiom.2018.10.069
Rattan S, Sood A, Kumar P, Kumar A, Kumar D, Warghat AR (2020) Phenylethanoids, phenylpropanoids, and phenolic acids quantification vis-a-vis gene expression profiling in leaf and root derived callus lines of Rhodiola imbricata (Edgew.). Ind Crop Prod 154:112708
Ren M, Xu W, Xu T (2019) Salidroside represses proliferation, migration and invasion of human lung cancer cells through AKT and MEK/ERK signal pathway. Artif Cell Nanomed B 47:1014–1021. https://doi.org/10.1080/21691401.2019.1584566
Satoh Y, Tajima K, Munekata M, Keasling JD, Lee TS (2012) Engineering of a tyrosol-producing pathway, utilizing simple sugar and the central metabolic tyrosine, in Escherichia coli. J Agr Food Chem 60:979–984. https://doi.org/10.1021/jf203256f
Sentheshanmuganathan S, Elsden SR (1958) The mechanism of the formation of tyrosol by Saccharomyces cerevisiae. Biochem J 69:210–218. https://doi.org/10.1042/bj0690210
Shi LL, Wang CY, Zhou XJ, Zhang YX, Liu YJ, Ma C (2013) Production of salidroside and tyrosol in cell suspension cultures of Rhodiola crenulata. Plant Cell Tiss Org 114:295–303. https://doi.org/10.1007/s11240-013-0325-z
Smetanska I (2008) Production of secondary metabolites using plant cell cultures. Adv Biochem Eng Biot 111:187–228. https://doi.org/10.1007/10_2008_103
Soejima H, Tsuge K, Yoshimura T, Sawada K, Kitagaki H (2012) Breeding of a high tyrosol-producing sake yeast by isolation of an ethanol-resistant mutant from a trp3 mutant. J Inst Brew 118:264–268. https://doi.org/10.1002/jib.46
Song H, Ding MZ, Jia XQ, Ma Q, Yuan YJ (2014) Synthetic microbial consortia: from systematic analysis to construction and applications. Chem Soc Rev 43:6954–6981. https://doi.org/10.1039/c4cs00114a
Sun A, Ju X (2020) Advances in research on anticancer properties of salidroside. Chin J Integr Med. https://doi.org/10.1007/s11655-020-3190-8
Tao K, Wang B, Feng D, Zhang W, Lu F, Lai J, Huang L, Nie T, Yang Q (2016) Salidroside protects against 6-hydroxydopamine-induced cytotoxicity by attenuating ER stress. Neurosci Bull 32:61–69. https://doi.org/10.1007/s12264-015-0001-x
Torrens-Spence MP, Pluskal T, Li FS, Carballo V, Weng JK (2018) Complete pathway elucidation and heterologous reconstitution of rhodiola salidroside biosynthesis. Mol Plant 11:205–217. https://doi.org/10.1016/j.molp.2017.12.007
Vasileva LV, Saracheva KE, Ivanovska MV, Petrova A, Marchev A, Georgiev MI, Murdjeva MA, Getova DP (2018) Antidepressant-like effect of salidroside and curcumin on the immunoreactivity of rats subjected to a chronic mild stress model. Food Chem Toxicol 121:604–611. https://doi.org/10.1016/j.fct.2018.09.065
Wang H, Ding Y, Zhou J, Sun X, Wang S (2009) The in vitro and in vivo antiviral effects of salidroside from Rhodiola rosea L. against coxsackievirus B3. Phytomedicine 16:146–155. https://doi.org/10.1016/j.phymed.2008.07.013
Wang Y, Xu P, Wang Y, Liu H, Zhou Y, Cao X (2013) The protection of Salidroside of the heart against acute exhaustive injury and molecular mechanism in rat. Oxid Med Cell Longev 2013:507832–507832. https://doi.org/10.1155/2013/507832
Wang DP, Wang L, Hou L, Deng XH, Gao Q, Gao NF (2015) Metabolic engineering of Saccharomyces cerevisiae for accumulating pyruvic acid. Ann Microbiol 65:2323–2331. https://doi.org/10.1007/s13213-015-1074-5
Wang H, Li Q, Sun S, Chen S (2020a) Neuroprotective effects of Salidroside in a mouse model of Alzheimer’s disease. Cell Mol Neurobiol 40(7):1133–1142. https://doi.org/10.1007/s10571-020-00801-w
Wang Y, Zhou S, Shen C, Jiang J (2020b) Isolation and identification of four antioxidants from Rhodiola crenulata and evaluation of their UV photoprotection capacity in vitro. J Funct Foods 66:103825. https://doi.org/10.1016/j.jff.2020.103825
Wen ZQ, Minton NP, Zhang Y, Li Q, Liu JL, Jiang Y, Yang S (2017) Enhanced solvent production by metabolic engineering of a twin-clostridial consortium. Metab Eng 39:38–48. https://doi.org/10.1016/j.ymben.2016.10.013
Wu SX, Zu YG, Wu M (2003) High yield production of salidroside in the suspension culture of Rhodiola sachalinensis. J Biotechnol 106:33–43. https://doi.org/10.1016/j.jbiotec.2003.07.009
Xie H, Shen C-Y, Jiang J-G (2020) The sources of salidroside and its targeting for multiple chronic diseases. J Funct Foods 64:103648. https://doi.org/10.1016/j.jff.2019.103648
Xu J, Su Z, Feng P (1998) Regulation of metabolism for improved salidroside production in cell suspension culture of Rhodiola sachalinensis A. Bor. I: The effect of precursor. Nat Prod Res Dev 10:8–14
Xu JF, Liu CB, Han AM, Feng PS, Su ZG (1998) Strategies for the improvement of salidroside production in cell suspension cultures of Rhodiola sachalinensis. Plant Cell Rep 17:288–293. https://doi.org/10.1007/s002990050394
Xu JF, Su ZG, Feng PS (1998) Activity of tyrosol glucosyltransferase and improved salidroside production through biotransformation of tyrosol in Rhodiola sachalinensis cell cultures. J Biotechnol 61:69–73. https://doi.org/10.1016/S0168-1656(98)00011-X
Xu JF, Xie J, Han AM, Feng PS, Su ZG (1998d) Kinetic and technical studies on large-scale culture of Rhodiola sachalinensis compact callus aggregates with air-lift reactors. J Chem Technol Biot 72:227–234. https://doi.org/10.1002/(SICI)1097-4660(199807)72:3%3c227::AID-JCTB898%3e3.0.CO;2-8
Xu JF, Ying PQ, Han AM, Su ZG (1999) Enhanced salidroside production in liquid-cultivated compact callus aggregates of Rhodiola sachalinensis: manipulation of plant growth regulators and sucrose. Plant Cell Tiss Org 55:53–58. https://doi.org/10.1023/A:1026489515174
Xue Y, Chen X, Yang C, Chang J, Shen W, Fan Y (2017) Engineering Eschericha coli for enhanced Tyrosol production. J Agr Food Chem 65:4708–4714. https://doi.org/10.1021/acs.jafc.7b01369
Yan X, Wu S, Wang Y, Shang X, Dai S (2004) Soil nutrient factors related to salidroside production of Rhodiola sachalinensis distributed in Chang Bai mountain. Environ Exp Bot 52:267–276. https://doi.org/10.1016/j.envexpbot.2004.02.005
Yang S, Yu H, Kang D, Ma Z, Qu R, Fu Q, Ma S (2014) Antidepressant-like effects of salidroside on olfactory bulbectomy-induced pro-inflammatory cytokine production and hyperactivity of HPA axis in rats. Pharmacol Biochem Be 124:451–457. https://doi.org/10.1016/j.pbb.2014.07.015
Yang H, Xue Y, Yang C, Shen W, Fan Y, Chen X (2019a) Modular engineering of Tyrosol production in Escherichia coli. J Agr Food Chem 67:3900–3908. https://doi.org/10.1021/acs.jafc.9b00227
Yang L, Yu Y, Zhang Q, Li X, Zhang C, Mao T, Liu S, Tian Z (2019b) Anti-gastric cancer effect of Salidroside through elevating miR-99a expression. Artif Cell Nanomed B 47:3500–3510. https://doi.org/10.1080/21691401.2019.1652626
Yu HL, Xu JH, Lu WY, Lin GQ (2008) Environmentally benign synthesis of natural glycosides using apple seed meal as green and robust biocatalyst. J Biotechnol 133:469–477. https://doi.org/10.1016/j.jbiotec.2007.12.003
Yu HS, Ma LQ, Zhang JX, Shi GL, Hu YH, Wang YN (2011) Characterization of glycosyltransferases responsible for salidroside biosynthesis in Rhodiola sachalinensis. Phytochemistry 72:862–870. https://doi.org/10.1016/j.phytochem.2011.03.020
Yu G, Li N, Zhao Y, Wang W, Feng XL (2018) Salidroside induces apoptosis in human ovarian cancer SKOV3 and A2780 cells through the p53 signaling pathway. Oncol Lett 15:6513–6518. https://doi.org/10.3892/ol.2018.8090
Yu H, He Y, She Y, Wang M, Yan Z, Ren JH, Cao Z, Shao Y, Wang S, Abd El-Aty AM, Hacimuftuoglu A, Wang J (2019) Preparation of molecularly imprinted polymers coupled with high-performance liquid chromatography for the selective extraction of salidroside from Rhodiola crenulata. J Chromatogr B 1118–1119:180–186. https://doi.org/10.1016/j.jchromb.2019.04.004
Yu X, Sun L, Tan L, Wang M, Ren X, Pi J, Jiang M, Li N (2020) Preparation and characterization of PLGA-PEG-PLGA nanoparticles containing Salidroside and Tamoxifen for breast cancer therapy. AAPS PharmSciTech 21:85. https://doi.org/10.1208/s12249-019-1523-8
Yuan Y, Wu X, Zhang X, Hong Y, Yan H (2019) Ameliorative effect of salidroside from Rhodiola Rosea L. on the gut microbiota subject to furan-induced liver injury in a mouse model. Food Chem Toxicol 125:333–340. https://doi.org/10.1016/j.fct.2019.01.007
Zhang HR, Wang XN (2016) Modular co-culture engineering, a new approach for metabolic engineering. Metab Eng 37:114–121. https://doi.org/10.1016/j.ymben.2016.05.007
Zhang C, Yu H, Lu M, Li J, Jin F (2005) Enzymic synthesis of salidroside: purification and characterization of salidrosidase from Aspergillas niger. Process Biochem 40:3143–3147. https://doi.org/10.1016/j.procbio.2005.03.043
Zhang S-q, Bi H-m, Liu C-j (2007) Extraction of bio-active components from Rhodiola sachalinensis under ultrahigh hydrostatic pressure. Sep Purif Technol 57:277–282. https://doi.org/10.1016/j.seppur.2007.04.022
Zhang JX, Ma LQ, Yu HS, Zhang H, Wang HT, Qin YF, Shi GL, Wang YN (2011) A tyrosine decarboxylase catalyzes the initial reaction of the salidroside biosynthesis pathway in Rhodiola sachalinensis. Plant Cell Rep 30:1443–1453. https://doi.org/10.1007/s00299-011-1053-7
Zhang Y, Zhang K, Wu Z, Guo T, Ye B, Lu M, Zhao J, Zhu C, Feng N (2015) Evaluation of transdermal salidroside delivery using niosomes via in vitro cellular uptake. Int J Pharmaceut 478:138–146. https://doi.org/10.1016/j.ijpharm.2014.11.018
Zhao S, Zhu Q, Somerville RL (2000) The sigma(70) transcription factor TyrR has zinc-stimulated phosphatase activity that is inhibited by ATP and tyrosine. J Bacteriol 182:1053–1061. https://doi.org/10.1128/JB.182.4.1053-1061.2000
Zheng T, Yang X, Li W, Wang Q, Chen L, Wu D, Bian F, Xing S, Jin S (2018) Salidroside attenuates high-fat diet-induced nonalcoholic fatty liver disease via AMPK-Dependent TXNIP/NLRP3 Pathway. Oxid Med Cell Longev 2018:8597897. https://doi.org/10.1155/2018/8597897
Zhou XF, Wu YX, Wang XZ, Liu B, Xu HW (2007) Salidroside production by hairy roots of Rhodiola sachalinensis obtained after transformation with Agrobacterium rhizogenes. Biol Pharm Bull 30:439–442. https://doi.org/10.1248/bpb.30.439
Zhou K, Qiao KJ, Edgar S, Stephanopoulos G (2015) Distributing a metabolic pathway among a microbial consortium enhances production of natural products. Nat Biotechnol 33:377-U157. https://doi.org/10.1038/nbt.3095
Acknowledgements
This work was funded by the National Key Research and Development Program of China (2021YFC2100700), National Natural Science Foundation of China (22108097), Natural Science Foundation of Jiangsu Province (BK20200616), China Postdoctoral Science Foundation (2020M671339), and Innovative and Entrepreneurial Doctor of Jiangsu Province (1026010241203190).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interests
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Liu, Y., Wang, J., Wang, L. et al. Biosynthesis and biotechnological production of salidroside from Rhodiola genus plants. Phytochem Rev 21, 1605–1626 (2022). https://doi.org/10.1007/s11101-021-09800-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11101-021-09800-1