Abstract
Rhodiola rosea L. is a worldwide popular plant with adaptogenic activities that have been and currently are exploited in the traditional medicine of many countries, as well as, examined in a number of clinical trials. More than 140 chemical structures have been identified which belong to several natural product classes, including phenylpropanoid glycosides, phenylethanoids, flavonoids and essential oils, and are mainly stored in the rhizomes and the roots of the plant. A number of mechanisms contribute to the adaptogenic activities of R. rosea preparations and its phytochemical constituents. Among them, the intrinsic inducible mammalian stress responses and their effector proteins, such as heat shock protein 70 (Hsp70), are the most prominent. Due to its popular medicinal use, which has led to depletion of its natural habitats, R. rosea is now considered as endangered in most parts of the world. Conservation, cultivation and micropropagation are all implemented as potential preservation strategies. A number of in vitro systems of R. rosea are being developed as sources of pharmaceutically valuable secondary metabolites. These are greatly facilitated by advances in elucidation of the biosynthetic pathways and the enzymes, which catalyse the production of these secondary metabolites in the plant. In addition, biotechnological approaches show promise towards achieving sustainable production of R. rosea secondary metabolites.
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Abbreviations
- 2.4-D:
-
2.4-Dichlorophenoxyacetic acid
- AEs:
-
Adverse events
- BAP:
-
6-Benzylaminopurine
- BAX:
-
Bcl-2-associated X protein
- Bcl-2:
-
B-cell lymphoma-2
- CA:
-
Cinnamyl alcohol
- cAMP:
-
Cyclic adenosine monophosphate
- DW:
-
Dry weight
- eNOS:
-
Endothelial nitric oxide synthase
- GA3 :
-
Gibberellic acid
- GC–MS:
-
Gas chromatography–mass spectroscopy
- GMP:
-
Good manufacturing practices
- HIF1:
-
Hypoxia-inducible factors 1
- HPLC:
-
High performance liquid chromatography
- Hsp70:
-
Heat shock protein 70
- IAA:
-
Indole-3-acetic acid
- IBA:
-
Indole-3-butyric acid
- Kin:
-
Kinetin
- MeJa:
-
Methyl jasmonate
- MS:
-
Murashige and Skoog
- NAA:
-
Naphtaleneacetic acid
- NMR:
-
Nuclear magnetic resonance
- NQO1:
-
NAD(P)H:quinone oxidoreductase 1
- Phe:
-
l-Phenylalanine
- THMP:
-
Traditional herbal medicinal products
- Tyr:
-
l-Tyrosine
- TyrDC:
-
Tyrosine decarboxylase
- UDP:
-
UDP-glucose:tyrosol glucosyltransferase
- Zea:
-
Zeatin
References
Abidov M, Grachev S, Seifulla R et al (2004) Extract of Rhodiola rosea radix reduces the level of C-reactive protein and creatinine kinase in the blood. Bull Exp Biol Med 138:63–64
Akerfelt M, Morimoto R, Sistonen L (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11:545–555
Akgul Y, Ferreira D, Abourashed E et al (2004) Lotaustralin from Rhodiola rosea roots. Fitoterapia 75:612–614
Asea A, Kaur P, Panossian A et al (2013) Evaluation of molecular chaperons Hsp72 and neuropeptide Y as characteristic markers of adaptogenic activity of plant extracts. Phytomedicine 20(14):1323–1329
Aslanyan G, Amroyan E, Gabrielyan E et al (2010) Double-blind, placebo-controlled, randomised study of single dose effects of ADAPT-232 on cognitive functions. Phytomedicine 17:494–499
Avula B, Wang Y, Ali Z et al (2009) RP-HPLC determination of phenylalkanoids and monoterpenoids in Rhodiola rosea and identification by LC-ESI-TOF. Biomed Chromatogr 23(8):865–872
Bai Y, Bi H, Zhuang Y et al (2014) Production of salidroside in metabolically engineered Escherichia coli. Sci Rep. doi:10.1038/srep06640
Booker A, Jalil B, Frommenwiler D et al (2015) The authenticity and quality of Rhodiola rosea products. Phytomedicine. doi:10.1016/j.phymed.2015.10.006
Brown R, Gerbarg P, Ramazanov Z (2002) Rhodiola rosea: a Phytomedicinal overview. HerbalGram 56:40–52
Buchwald W, Mordalski R, Kuchrski W et al (2015) Effect of fertilization on roseroot (Rhodiola rosea L.) yield and content of active compounds. Acta Sci Pol Hortorum Cultus 14(2):109–121
Buckley J, Lewis S (2009) The effects of an acute dose of Rhodiola rosea on exercise performance and cognitive function. J Int Soc Sports Nutr 6(1):P14
Cai L, Wang H, Li Q (2008) Salidroside inhibits H2O2-induced apoptosis in PC12 cells by preventing cytochrome c release and inactivating of caspase cascade. Acta Biochim Biophys Sin 40(9):796–802
Chen X, Liu J, Gu X et al (2008) Salidroside attenuates glutamate-induced apoptotic cell death in primary cultured hippocampal neurons of rats. Brain Res 1238:189–198
Chen X, Zhang Q, Cheng Q et al (2009) Protective effect of salidroside against H2O2-induced cell apoptosis in primary culture of rat hippocampal neurons. Mol Cell Biochem 332(1–2):85–93
Chiang H, Chen H, Wu C (2015) Rhodiola plants: chemistry and biological activity. J Food Drug Anal 23:359–369
Committee on Herbal Medicinal Products (2012a) Community herbal monograph on Rhodiola rosea L., rhizoma et radix. EMA/HMPC/232091/2011
Committee on Herbal Medicinal Products (2012b) Assessment report on Rhodiola rosea L., rhizoma et radix. EMA/HMPC/232100/2011
Cuerrier A, Archambault M, Rapinski M et al (2015) Taxonomy of Rhodiola rosea L., with special attention to molecular analyses of Nunavik (Québec) populations. In: Cuerrier A, Ampong-Nyarko K (eds) Rhodiola rosea. Traditional herbal medicines for modern times. CRC Press, Taylor & Francis Group, pp 1–34
Dayalan N, Kostov R, Dinkova-Kostova A (2015) Transcription factors Hsf1 and Nrf2 engage in crosstalk for cytoprotection. Trends Pharmacol Sci 36(1):6–14
Didukh YP (ed) (2009) Red Data Book of Ukraine: Flora. Ukrainian Scientific Publishers, Kyiv, p 900
Dneprovskii I, Kim E, Iumanova T (1975) Seasonal development and growth of Rhodiola rosea L. in relation to introduction [as drug plant]. Biull Gl Bot Sada 98:27–34
Dubichev A, Kurkin V, Zapesochnaya G et al (1991) Chemical composition of the rhizomes of the Rhodiola rosea by the HPLC method. Chem Nat Compd 27(2):161–164
Engler A, Melchior H (1964) Syllabus der Pflanzenfamilien. Gerbuder Borntraeger, Berlin
Evstatieva L, Todorova M, Antonova D (2010) Chemical composition of the essential oils of Rhodiola rosea L. of three different origins. Pharmacogn Mag 6(24):256–258
Fu K, Ohba H (2001) Rhodiola (Crassulaceae). In: Wu Z, Raven P (eds) Flora of China, vol 8. Science Press, Beijing, pp 251–268
Furmanowa M, Oledzka H, Michalska M et al (1995) Rhodiola rosea L. (Roseroot): in vitro regeneration and the biological activity of roots. In: Bajaj YPS (ed) Biotechnology in agriculture and forestry, vol 33. Medicinal and Aromatic Plants VIII. Springer, Berlin, pp 412–426
Furmanowa M, Skopińska-Rozewska E, Rogala E et al (1998) Rhodiola rosea in vitro culture-phytochemical analysis and antioxidant action. Acta Soc Bot Pol 67(1):69–73
Furmanowa M, Hartwich M, Alfermann A et al (1999) Rosavin as a product of glycosylation by Rhodiola rosea (roseroot) cell cultures. Plant Cell Tiss Org 56:105–110
Galambosi B (2006) Demand and availability of Rhodiola rosea L. raw material. In: Bogers R, Cracker L, Lange D (eds) Medicinal and aromatic plants. Springer, The Hague, pp 223–236
Galambosi B (2015) Cultivation of Rhodiola rosea in Europe. In: Cuerrier A, Ampong-Nyarko K (eds) Rhodiola rosea. Traditional herbal medicines for modern times. CRC Press, Taylor & Francis Group, pp 87–124
Georgiev M, Agostini E, Ludwig-Müller J et al (2012) Genetically transformed roots: from plant disease to biotechnological resource. Trends Biotechnol 30(10):528–537
Ghiorghită G, Hârtan M, Maftei D et al (2011) Some considerations regarding the in vitro culture of Rhodiola rosea L. Rom Biotechnol Lett 16(1):5902–5908
Grech-Baran M, Sykłowska-Baranek K, Giebułtowicz J et al (2013) Tyrosol glucosultransferase activity and salidroside production in natural and transformed root cultures of Rhodiola kirilowii (Regel) Regel et Maximowicz. Acta Biol Cracov Ser Bot 55(2):126–133
Grech-Baran M, Sykłowska-Baranek K, Krajewska-Patan A et al (2014) Biotransformation of cinnamyl alcohol to rosavins by non-transformed wild type and hairy root cultures of Rhodiola kirilowii. Biotechnol Lett 36:649–656
Grech-Baran M, Sykłowska-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
Gryszczyńska A, Krajewska-Patan A, Dreger M et al (2012) Proanthocyanidins in Rhodiola kirilowii and Rhodiola rosea callus tissues and transformed roots-determination with UPLC–MS/MS method. Herba Pol 58(4):52–61
Guan S, Feng H, Song B et al (2011a) Salidroside attenuates LPS-induced pro-inflammatory cytokine responses and improves survival in murine endotoxemia. Int Immunopharmacol 11(12):2194–2199
Guan S, Wang W, Lu J (2011b) Salidroside attenuates hydrogen peroxide-induced cell damage through a cAMP-dependent pathway. Molecules 16(4):3371–3379
György Z (2006) Glucoside production by in vitro Rhodiola rosea cultures. Dissertation, Acta Universitatis Ouluensis C Technica 244. Oulu University Press, Oulu
György Z, Hohtola A (2009) Production of cinnamyl glycosides in compact callus aggregate cultures of Rhodiola rosea through biotransformation of cinnamyl alcohol. In: Jain SM, Saxena P (eds) Protocols for in vitro cultures and secondary metabolite analysis of aromatic and medicinal plants. Methods in Molecular Biology, vol 547. Humana Press, New York, pp 305–312
György Z, Tolonen A, Pakonen M et al (2004) Enhancement of the production of cinnamyl glycosides in CCA cultures of Rhodiola rosea through biotransformation of cinnamyl alcohol. Plant Sci 166(1):229–236
György Z, Tolonen A, Neubauer P et al (2005) Enhanced biotransformation capacity of Rhodiola rosea callus cultures for glycosid production. Plant Cell Tiss Org Cult 83:129–135
György Z, Jaakola L, Neubauer P et al (2009) Isolation and genotype-dependent, organ-specific expression analysis of a Rhodiola rosea cDNA encoding tyrosinedecarboxylase. J Plant Physiol 166:1581–1586
Hauser G, Dayao E, Wasserloos K (1996) HSP induction inhibits iNOS mRNA expression and attenuates hypotension in endotoxin-challenged rats. Am J Physiol 271(6 Pt 2):H2529–H2535
Hegi G (ed) (1963) Rhodiola, Rosenwurz. In: Illustrierte Flora von Mitteleuropa. Zweite völlig neubearbeitete Auflage. Band IV/2, Lieferung 2/3. Paul Parey, Hamburg, Berlin, pp 99–102
Hernández-Santana A, Pérez-López V, Zubeldia J (2014) A Rhodiola rosea root extract protects skeletal muscle cells against chemically induced oxidative stress by modulating heat shock protein 70 (HSP70) expression. Phytother Res 28(4):623–628
Héthelyi É, Korány K, Galambosi B et al (2005) Chemical composition of the essential oil from rhizomes of Rhodiola rosea L. grown in Finland. J Essent Oil Res 17(6):628–629
Hooker J, Jackson B (1895–1974) Index Kewensis. Plantarum phanerogamarum nomina et synonima generum et specium. Clarendron Press, Oxford
Hu X, Zhang X, Qiu S (2010) Salidroside induces cell-cycle arrest and apoptosis in human breast cancer cells. Biochem Biophys Res Commun 398(1):62–67
Huang X, Zou L, Yu X (2015) Salidroside attenuates chronic hypoxia-induced pulmonary hypertension via adenosine A2a receptor related mitochondria-dependent apoptosis pathway. J Mol Cell Cardiol 82:153–166
Hung S, Perry R, Ernst E (2011) The effectiveness and efficacy of Rhodiola rosea L.: a systematic review of randomized clinical trials. Phytomedicine 18:235–244
Jeong H, Ryu Y, Park S et al (2009) Neuraminidase inhibitory activities of flavonols isolated from Rhodiola rosea roots and their in vitro anti-influenza viral activities. Bioorg Med Chem 17(19):6816–6823
Joset K, Nyberg N, Van Diermen D et al (2011) Metabolic profiling of Rhodiola rosea rhizomes by 1H NMR spectroscopy. Phytochem Anal 22:158–165
Kenneth N, Rocha S (2008) Regulation of gene expression by hypoxia. Biochem J 414(1):19–29
Khanum F, Bawa A, Singh B (2005) Rhodiola rosea: a versatile adaptogen. Compr Rev Food Sci Food Saf 4:55–62
Kim J, Yenari M, Lee J (2015) Regulation of inflammatory transcription factors by heat shock protein 70 in primary cultured astrocytes exposed to oxygen–glucose deprivation. Neuroscience 286:272–280
Kirschke E, Goswami D, Southworth D (2014) Glucocorticoid receptor function regulated by coordinated action of the Hsp90 and Hsp70 chaperone cycles. Cell 157(7):1685–1697
Kotiranta H, Uotila P, Sulkava S et al (1998) Red data book of East Fennoscandia. Ministry of the environment, Finnish environment institute and botanical museum. Finnish museum of natural history, Helsinki, p 351
Krajewska-Patan A, Dreger M, Łowicka A et al (2007a) Chemical investigations of biotransformed Rhodiola rosea callus tissue. Herba Pol 53(4):77–87
Krajewska-Patan A, Furmanowa M, Dreger M (2007b) Enhancing the biosynthesis of salidroside by biotransformation of p-tyrosol in callus culture of Rhodiola rosea L. Herba Pol 53(1):55–64
Krajewska-Patan A, Dreger M, Łowicka A et al (2008) Preliminary pharmacological investigations of biotransformed roseroot (Rhodiola rosea L.) callus tissue. Herba Pol 53(4):50–58
Kudryavtseva O, Viracheva L (2006) Results of genus Rhodiola (Crassulaceae) species introduction in Polar–Alpine Botanical Garden (Kola Peninsula). Rastit Resur 42(4):28–34
Kurkin V, Zapesochanaya G, Shchavlinskii A (1984) Flavonoids of the rhizomes of Rhodiola rosea III. Chem Nat Compd 20(3):367–368
Kurkin V, Zapesochnaya G, Shchavlinskii A (1985) Flavonoids of the epigeal part of Rhodiola rosea I. Chem Nat Compd 20(5):623–624
Kurkin V, Zapesochnaya G, Gorbunov Y (1986) Chemical investigations on some species of Rhodiola L. and Sedum L. genera and problems of their chemotaxonomy. Rast Res 22(3):310–319
Kurkin V, Zapesochnaya G, Nukhimovsky E et al (1988) Chemical composition of rhizomes of Mongolian Rhodiola rosea population introduced into districts near Moscow. Khim Farm Zh 22(3):324–326
Kurkin V, Zapesochnaya G, Dubichev A (1991) Phenylpropanoids of a callus culture of Rhodiola rosea. Chem Nat Compd 27(4):419–425
Lan X, Chang K, Zheng L et al (2013) Engineering salidroside biosynthetic pathway in hairy root cultures of Rhodiola crenulata based on metabolic characterization of tyrosine decarboxylase. PLoS One 8(10):e75459
Li Q, Wang H, Wang Z (2010) Salidroside attenuates hypoxia-induced abnormal processing of amyloid precursor protein by decreasing BACE1 expression in SH-SY5Y cells. Neurosci Lett 481(3):154–158
Ling-ling S, Li W, Yan-xia Z et al (2007) Approaches to biosynthesis of salidroside and its key metabolic enzymes. For Stud China 9(4):295–299
Linh P, Kim Y, Hong S et al (2000) Quantitative determination of salidroside and tyrosol from the underground part of Rhodiola rosea by high performance liquid chromatography. Arch Pharm Res 23(4):349–352
Linnaeus C (1749) Materia Medica. Liber I. De Plantis. Holmiae-Laurentii Salvii
Lishmanov I, Naumova A, Afanus’ev S (1997) Contribution of the opioid system to realization of inotropic effects of Rhodiola rosea extracts in ischemic and reperfusion heart damage in vitro. Eksp Klin Farmakol 60:34–36
Ma G, Li W, Dou D et al (2006) Rhodiolosides A-E, monoterpene glycosides from Rhodiola rosea. Chem Pharm Bull 54(8):1229–1233
Ma L, Liu B, Gao D et al (2007) Molecular cloning and overexpression of a novel UDP-glucosyltransferase elevating salidroside levels in Rhodiola sachalinensis. Plant Cell Rep 26:989–999
Ma L, Gao D, Wang Y et al (2008) Effects of overexpression of endogenous phenylalanine ammonia-lyase (PALrs1) on accumulation of salidroside in Rhodiola sachalinensis. Plant Biol 10:323–333
Mao G, Wang Y, Qiu Q et al (2010) Salidroside protects human fibroblast cells from premature senescence induced by H(2)O(2) partly through modulating oxidative status. Mech Ageing Dev 131(11–12):723–731
Mao J, Xie S, Zee J et al (2015) Rhodiola rosea versus ertraline for major depressive disorder: a randomized placebo-controlled trial. Phytomedicine 22:394–399
Marchev A, Haas C, Schulz S et al (2014) Sage in vitro cultures: a promising tool for the production of bioactive terpenes and phenolic substances. Biotechnol Lett 36:211–221
Martin J, Pomahačová B, Dušek J et al (2010) In vitro culture establishment of Schizandra chinensis (Turz.) and Rhodiola rosea L., two adaptogenic compounds producing plants. J Phytol 2(11):80–87
Maslova L, Kondrat’ev B, Maslov L (1994) The cardioprotective and antiadrenergic activity of an extract of Rhodiola rosea in stress. Eksp Klin Farmakol 57(6):61–63
Mell C (1938) Dyes, tannins, perfumes, and medicines from Rhodiola rosea. Text Colorist 60(715):483–484
Mirmazloum I, György Z (2012) Review of the molecular genetics in higher plants towards salidrosid and cinnamyl alcohol glycosides biosynthesis in Rhodiola rosea L. Acta Aliment Hug 41:133–146
Mirmazloum I, Forgács I, Zok A et al (2014) Transgenic callus culture establishment, a tool for metabolic engineering of Rhodiola rosea L. Acta Sci Pol Hortorum Cultus 13(4):95–106
Mirmazloum I, Ladányi M, György Z (2015a) Changes in the content of the glycosides, aglycones and their possible precursors of Rhodiola rosea during the vegetation period. Nat Prod Commun 10(8):1413–1416
Mirmazloum I, Pedryc A, György Z, Komáromi B, Ladányi M (2015b) Glycoside content in Rhodiola rosea L.: dynamics and expression pattern of genes involved in the synthesis of rosavins. Acta Hortic 1098:81–89
Mirmazloum I, Radácsi P, Pedryc A et al (2015c) Hormonal effects of carbenicillin and cefotaxime on Rhodiola rosea callus culture. Planta Med 16(81):PM-243
Morimoto R (2011) The heat shock response: systems biology of proteotoxic stress in aging and disease. Cold Spring Harb Symp Quant Biol 76:91–99
Mossberg B, Stenberg L (2003) Den nya nordiska floran. Stockholm, Wahlström and Widstrand, p 928
Mosser D, Caron A, Bourget L et al (1997) Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol Cell Biol 17(9):5317–5327
Mudge E, Lopes-Lutz D, Brown P (2013) Purification of phenylalkanoids and monoterpene glycosides from Rhodiola rosea L. roots by high-speed counter-current chromatography. Phytochem Anal 24(2):129–134
Olsson E, Schéele B, Panossian A (2009) A randomised, double-blind, placebo-controlled, parallel-group study of the standardised extract SHR-5 of the roots of Rhodiola rosea in the treatment of subjects with stress-related fatigue. Planta Med 75:105–112
Palumbo D, Occhiuto F, Spadaro F (2012) Rhodiola rosea extract protects human cortical neurons against glutamate and hydrogen peroxide-induced cell death through reduction in the accumulation of intracellular calcium. Phytother Res 26(6):878–883
Panossian A (2013) Adaptogens in mental and behavioral disorders. Psychiatr Clin North Am 36(1):49–64
Panossian A, Wagner H (2005) Stimulating effects of adaptogens: an overview of clinical trials of adaptogens with particular reference to their efficacy on single dose administration. Phytother Res 19(10):819–838
Panossian A, Wikman G (2009) Evidence-based efficacy of adaptogens in fatigue, and molecular mechanisms related to their stress-protective activity. Curr Clin Pharmacol 4(3):198–219
Panossian A, Wikman G (2010) Effects of adaptogens on the central nervous system and the molecular mechanisms associated with their stress-protective activity. Pharmaceuticals 3:188–224
Panossian A, Wikman G (2015) Evidence-based efficacy and effectiveness of Rhodiola SHR-5 extract in treating stress- and age-associated disorders. In: Cuerrier A, Ampong-Nyarko K (eds) Rhodiola rosea. Traditional herbal medicines for modern times. CRC Press, Taylor & Francis Group, pp 205–224
Panossian A, Wikman G, Kaur P (2009) Adaptogens exert a stress-protective effect by modulation of expression of molecular chaperones. Phytomedicine 16(6–7):617–622
Panossian A, Wikman G, Sarris J (2010) Rosenroot (Rhodiola rosea): traditional use, chemical composition, pharmacology and clinical efficacy. Phytomedicine 17(7):481–493
Panossian A, Wikman G, Kaur P et al (2012) Adaptogens stimulate neuropeptide y and Hsp72 expression and release in neuroglia cells. Front Neurosci 6:6. doi:10.3389/fnins.2012.00006
Panossian A, Hamm R, Wikman G et al (2014) Mechanism of action of Rhodiola, salidroside, tyrosol and triandrin in isolated neuroglial cells: an interactive pathway analysis of the downstream effects using RNA microarray data. Phytomedicine 21(11):1325–1348
Petsalo A, Jalonen J, Tolonen D (2006) Identification of flavonoids of Rhodiola rosea by liquid chromatography-tandem mass spectrometry. J Chromatogr A 1112(1–2):224–231
Platikanov S, Evstatieva L (2008) Introduction of wild golden root (Rhodiola rosea L.) as a potential economic crop in Bulgaria. Econ Bot 62(4):621–627
Punja S, Shamseer L, Olson K et al (2014) Rhodiola rosea for mental and physical fatigue in nursing students: a randomized controlled trial. PLoS One 9(9):e108416
Rohloff J (2002) Volatiles from rhizomes of Rhodiola rosea L. Phytochemistry 59(6):655–661
Ross S (2014) Rhodiola rosea (SHR-5), Part I: a proprietary root extract of Rhodiola rosea is found to be effective in the treatment of stress-related fatigue. Holist Nurs Pract 28(2):149–154
Saratikov A, Krasnov E (2004) Rhodiola rosea (Golden root): a valuable medicinal plant. Tomsk University Press, Tomsk, pp 1–205
Saunders D, Poppleton D, Struchkov A et al (2013) Analysis of five bioactive compounds from naturally occurring Rhodiola rosea in eastern Canada. Can J Plant Sci 94(4):741–748
Schriner S, Avanesian A, Liu Y et al (2009) Protection of human cultured cells against oxidative stress by Rhodiola rosea without activation of antioxidant defenses. Free Radic Biol Med 47(5):577–584
Semenza G (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148(3):399–408
Semple H (2010) Toxicology studies on Rhodiola rosea extract. Pharm Biol 48(S1):25–32
Shanely R, Nieman D, Zwetsloot K et al (2014) Evaluation of Rhodiola rosea supplementation on skeletal muscle damage and inflammation in runners following a competitive marathon. Brain Behav Immun 39:204–210
Shatar S, Adams R, Koenig W (2007) Comparative study of the essential oil of Rhodiola rosea L from Mongolia. J Essent Oil Res 19(3):215–217
Shi T, Feng S, Xing J et al (2012) Neuroprotective effects of salidroside and its analogue tyrosol galactoside against focal cerebral ischemia in vivo and H2O2-induced neurotoxicity in vitro. Neurotox Res 21(4):358–367
Sidjimova B, Valyovska-Popova N, Peev D (2014) Reproductive capacity of four medicinal plants in Nature Park “Rilsky Manastir”–West Bulgaria. J BioSci Biotech 177–180
Simar D, Jacques A, Caillaud C (2012) Heat shock proteins induction reduces stress kinases activation, potentially improving insulin signaling in monocytes from obese subjects. Cell Stress Chaperon 17(5):615–621
Simeonova V, Tasheva K, Kosturkova K et al (2013) A soft computing QSAR adapted model for improvement of golden root in vitro culture growth. Biotechnol Biotechnol Equip 27(3):3877–3884
Small E, Catling M (1999) Rhodiola rosea (L.) Scop. Roseroot. In: Cavers P (ed) Canadian medicinal crops. NRC Research Press, Ottawa, pp 134–139
Stancheva S, Mosharrof A (1987) Effect of the extract of Rhodiola rosea L. on the content of the brain biogenic monoamines. Proc Bulg Acad Sci Med 40:85–87
Stough C, Camfield D, Kure C et al (2011) Improving general intelligence with a nutrient-based pharmacological intervention. Intelligence 39:100–107
Talalay P (2000) Chemoprotection against cancer by induction of phase 2 enzymes. BioFactors 12:5–11
Tang Y, Vater C, Jacobi A (2014) Salidroside exerts angiogenic and cytoprotective effects on human bone marrow-derived endothelial progenitor cells via Akt/mTOR/p70S6K and MAPK signaling pathways. Br J Pharmacol 171(9):2440–2456
Tang H, Gao L, Mao J et al (2015) Salidroside protects against bleomycin-induced pulmonary fibrosis: activation of Nrf2-antioxidant signaling, and inhibition of NF-κB and TGF-β1/Smad-2/-3 pathways. Cell Stress Chaperon. doi:10.1007/s12192-015-0654-4
Tasheva K, Kosturkova G (2010) Bulgarian golden root in vitro cultures for micropropagation and reintroduction. Cent Eur J Biol 5(6):853–863
Tasheva K, Kosturkova G (2012a) The role of biotechnology for conservation and biologically active substances production of Rhodiola rosea: endangered medicinal species. Sci World J. doi:10.1100/2012/274942
Tasheva K, Kosturkova G (2012b) Towards Agrobacterium-mediated transformation of the endangered medicinal plant golden root. AgroLife Sci J 1:132–138
Tasheva K, Kosturkova G (2014) The effect of sucrose concentration on in vitro callogenesis of golden root-endangered medicinal plant. Sci Bull Ser F Biotechnol 18:77–82
Taskaev A (1999) Red book of Komi Republic. Rare and endangered species of plants and animals. Design and Cartography, Moscow-Syktyvkar, p 528
Tolonen A, Pakonen M, Hohtola A et al (2003) Phenylpropanoid glycosides form Rhodiola rosea. Chem Pharm Bull 51(4):467–470
Tolonen A, György Z, Jalonen J et al (2004) LC/MS/MS identification of glycosides produced by biotransformation of cinnamyl alcohol in Rhodiola rosea compact callus aggregates. Biomed Chromatogr 18:550–558
Troshchenko A, Kutikova G (1967) Rhodioloside from Rhodiola rosea and Rh. quadrifida. I. Chem Nat Compd 3(4):204–207
Tutin T (1964) Flora europaea. Cambridge University Press, Cambridge, p 363
van Diermen D, Marston A, Bravo J (2009) Monoamine oxidase inhibition by Rhodiola rosea L. roots. J Ethnopharmacol 122(2):397–401
Volkova L, Urmantseva V, Burgutin A et al (2013) Adaptogenic action of the complex of phenylpropanoids on Dioscorea deltoidea cell culture under abiotic stress. Russ J Plant Physiol 60(2):235–243
Wang H, Ding Y, Zhou J (2009) The in vitro and in vivo antiviral effects of salidroside from Rhodiola rosea L. against coxsackievirus B3. Phytomedicine 16(2–3):146–155
Weglarz Z, Przybył J, Geszprych A (2008) Roseroot (Rhodiola rosea L.): effect of internal and external factors on accumulation of biologically active compounds. In: Ramawat K, Mérillon J (eds) Bioactive molecules and medicinal plants. Springer, Berlin Heilderberg, pp 297–315
Wu Y, Lian L, Jiang Y et al (2009) Hepatoprotective effects of salidroside on fulminant hepatic failure induced by d-galactosamine and lipopolysaccharide in mice. J Pharm Pharmacol 61(10):1375–1382
Xin T, Li X, Yao H, Lin Y, Ma X, Cheng R, Song J, Ni L, Fan C, Chen S (2015) Survey of commercial Rhodiola products revealed species diversity and potential safety issues. Sci Rep 9(5):8337
Xing S, Yang X, Li W (2014) Salidroside stimulates mitochondrial biogenesis and protects against H2O2-induced endothelial dysfunction. Oxid Med Cell Longev 2014:904834
Xu J, Su Z, Feng P (1998a) Activity of tyrosol glucosyltransferase and improved salidroside production through biotransformation of tyrosol in Rhodiola sachalinensis cell cultures. J Biotechnol 61:69–73
Xu J, Liu C, Han A et al (1998b) Strategies for the improvement of salidroside production in cell suspension cultures of Rhodiola sachalinensis. Plant Cell Rep 17(4):288–293
Xu M, Gong Y, Su M et al (2011) Absence of the adenosine A2A receptor confers pulmonary arterial hypertension and increased pulmonary vascular remodeling in mice. J Vasc Res 48(2):171–183
Xu M, Shi H, Wang H et al (2013) Salidroside protects against hydrogen peroxide-induced injury in HUVECs via the regulation of REDD1 and mTOR activation. Mol Med Rep 8(1):147–153
Yaglom J, Gabai V, Meriin A et al (1999) The function of HSP72 in suppression of c-Jun N-terminal kinase activation can be dissociated from its role in prevention of protein damage. J Biol Chem 274(29):20223–20228
Yousef G, Grace M, Cheng D (2006) Comparative phytochemical characterization of three Rhodiola species. Phytochemistry 67(21):2380–2391
Yu H, Ma L, Zhang J et al (2011) Characterization of glycosyltransferases responsible for salidroside biosynthesis in Rhodiola sachalinensis. Phytochemistry 72:862–870
Zapesochnaya G, Kurkin V (1982) Glycosides of cinnamyl alcohol from the rhizomes of Rhodiola rosea. Chem Nat Compd 18(6):685–688
Zapesochnaya G, Kurkin V (1983) The flavonoids of the rhizomes of Rhodiola rosea II A flavonolignan and glycosides of herbacetin. Chem Nat Compd 19(1):21–29
Zhang L, Yu H, Sun Y et al (2007) Protective effects of salidroside on hydrogen peroxide-induced apoptosis in SH-SY5Y human neuroblastoma cells. Eur J Pharmacol 564(1–3):18–25
Zhang J, Liu A, Hou R et al (2009) Salidroside protects cardiomyocyte against hypoxia-induced death: a HIF-1alpha-activated and VEGF-mediated pathway. Eur J Pharmacol 607(1–3):6–14
Zhang J, Ma L, Yu H et al (2011) A tyrosine decarboxylase catalyzes the initial reaction of the salidroside biosynthesis pathway in Rhodiola sachalinensis. Plant Cell Rep 30:1443–1453
Zhang H, Shen W, Gao C et al (2012) Protective effects of salidroside on epirubicin-induced early left ventricular regional systolic dysfunction in patients with breast cancer. Drugs R&D 12(2):101–106
Zhao X, Jin L, Shen N et al (2013) Salidroside inhibits endogenous hydrogen peroxide induced cytotoxicity of endothelial cells. Biol Pharm Bull 36(11):1773–1778
Zheng K, Zhang Z, Guo A et al (2012) Salidroside stimulates the accumulation of HIF-1α protein resulted in the induction of EPO expression: a signalling via blocking the degradation pathway in kidney and liver cells. Eur J Pharmacol 679(1–3):34–39
Zheng K, Sheng Z, Li Y et al (2014) Salidroside inhibits oxygen glucose deprivation (OGD)/re-oxygenation-induced H9c2 cell necrosis through activating of Akt-Nrf2 signalling. Biochem Biophys Res Commun 451(1):79–85
Zhong X, Lin R, Li Z et al (2014) Effects of salidroside on cobalt chloride-induced hypoxia damage and mTOR signaling repression in PC12 cells. Biol Pharm Bull 37(7):1199–1206
Zhou X, Wu Y, Wang X (2007) Salidroside production by hairy roots of Rhodiola sachalinensis obtained after transformation with Agrobacterium rhizogenes. Biol Pharm Bull 30(3):439–442
Zhu J, Wan X, Zhu Y et al (2010) Evaluation of salidroside in vitro and in vivo genotoxicity. Drug Chem Toxicol 33(2):220–226
Zhu Y, Shi Y, Wu D et al (2011) Salidroside protects against hydrogen peroxide-induced injury in cardiac H9c2 cells via PI3K-Akt dependent pathway. DNA Cell Biol 30(10):809–819
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Marchev, A.S., Dinkova-Kostova, A.T., György, Z. et al. Rhodiola rosea L.: from golden root to green cell factories. Phytochem Rev 15, 515–536 (2016). https://doi.org/10.1007/s11101-016-9453-5
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DOI: https://doi.org/10.1007/s11101-016-9453-5