Hairy roots as a potential source for the production of rosmarinic acid from genus Salvia

Authors

DOI:

https://doi.org/10.14719/pst.2541

Keywords:

Salvia, secondary metabolites, rosmarinic acid, hairy root cultures, Agrobacterium rhizogenes, genetic engineering, elicitors

Abstract

The Salvia genus, a member of the Lamiaceae family, exhibits a rich array of secondary metabolites, including di- and triterpenoids, phenols, polyphenols, and essential oil compounds. These constituents contribute to valuable pharmacological activities such as antibacterial, antiviral, anti-inflammatory, and antioxidant properties. Among these metabolites, rosmarinic acid stands out as a particularly promising compound, deriving from the precursors phenylalanine and tyrosine. It belongs to the phenolic compound class and acts as an ester of caffeic acid, showcasing diverse therapeutic potentials like antifungal, antibacterial, antiviral, antioxidant, anticancer, anti-ageing, anti-inflammatory, and anti-diabetic effects. To facilitate the production of such secondary metabolites, plant tissue culture techniques have played a pivotal role, with hairy root cultures being one of the preferred methods. This review provides an extensive examination of the biosynthetic pathway of rosmarinic acid and its successful generation using hairy root cultures. Additionally, the review highlights the utilization of genetic modification tools and various biotic and abiotic elicitors, including yeast extract, methyl jasmonate, and silver ion (Ag+), in hairy root cultures of diverse Salvia species to enhance the production of rosmarinic acid.

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References

Walker JB, Sytsma KJ, Treutlein J, Wink M. Salvia (Lamiaceae) is not monophyletic: implications for the systematics, radiation, and ecological specializations of Salvia and tribe Mentheae. Am J Bot. 2004;91(7):1115–25. https://doi.org/10.3732/ajb.91.7.1115

POWO (2023) Salvia L. | Plants of the World Online | Kew Science [cited 5 May 2023]. Available from: https://powo.science.kew.org/taxon/urn:lsid:ipni.org:names:30000096-2

Raja RR. Medicinally potential plants of labiatae (lamiaceae) family: an overview. Res J of Med Plant. 2012;6(3):203–13. https://doi.org/10.3923/rjmp.2012.203.213

Venkateshappa SM, Sreenath KP. Potential medicinal plants of Lamiaceae. AIJRFANS. 2013;1(3):82–7.

Devecchi M. The use of labiatae of ornamental interest in the design of parks and gardens. Acta Hortic. 2006;(723):51–8. https://doi.org/10.17660/ActaHortic.2006.723.3

Petrovska BB. Historical review of medicinal plants’ usage. Pharmacogn Rev. 2012;6(11):1–5. https://doi.org/10.4103/0973-7847.95849

Tiwari R, Rana CS. Plant secondary metabolites: a review. Int J Eng Res Gen Sci. 2015;3(5):661–70.

Ma X-H, Ma Y, Tang J-F, He Y-L, Liu Y-C, Ma X-J, Shen Y, Cui G-H, Lin H-X, Rong Q-X, Guo J, Huang L-Q. The biosynthetic pathways of tanshinones and phenolic acids in Salvia miltiorrhiza. Molecules. 2015;20(9):16235–54. https://doi.org/10.3390/molecules200916235

Cioffi G, Bader A, Malafronte A, Dal Piaz F, De Tommasi N. Secondary metabolites from the aerial parts of Salvia palaestina Bentham. Phytochem. 2008;69(4):1005–12. https://doi.org/10.1016/j.phytochem.2007.11.002

Koysu P, Genc N, Elmastas M, Aksit H, Erenler R. Isolation, identification of secondary metabolites from Salvia absconditiflora and evaluation of their antioxidative properties. Nat Prod Res. 2019;33(24):3592–5. https://doi.org/10.1080/14786419.2018.1488700

Ghorbanpour M. Major essential oil constituents, total phenolics and flavonoids content and antioxidant activity of Salvia officinalis plant in response to nano-titanium dioxide. Ind J Plant Physiol. 2015;20(3):249–56. https://doi.org/10.1007/s40502-015-0170-7

Llurba-Montesino N, Schmidt TJ. Salvia Species as Sources of natural products with antiprotozoal Activity. Int J Mol Sci. 2018;19(1). https://doi.org/10.3390/ijms19010264

Chen H, Chen F, Zhang YL, Song JY. Production of lithospermic acid B and rosmarinic acid in hairy root cultures of Salvia miltiorrhiza. J Ind Microbiol Biotechnol. 1999;22(3):133–8. https://doi.org/10.1038/sj.jim.2900624

Lu Y, Foo LY. Salvianolic acid L, a potent phenolic antioxidant from Salvia officinalis. Tetrahedron Lett. 2001;42(46):8223–5. https://doi.org/10.1016/S0040-4039(01)01738-5

Lian-Niang L, Rui T, Wei-Ming C. Salvianolic Acid A, a new depside from roots of Salvia miltiorrhiza. Planta Med. 1984;50(3):227–8. https://doi.org/10.1055/s-2007-969684

Scarpati ML. Oriente, G. Isolamento e costituzione dell’acido rosmarinico (dal rosmarinus off.). Ric Sci. 1958; 28: 2329–33.

Chaprin N, Ellis BE. Microspectrophotometric evaluation of rosmarinic acid accumulation in single cultured plant cells. Can J Bot. 1984;62(11):2278–82. https://doi.org/10.1139/b84-310

Häusler E, Petersen M, Alfermann AW. Isolation of protoplasts and vacuoles from cell suspension cultures of Coleus blumei Benth. Plant Cell Rep. 1993;12(9):510–2. https://doi.org/10.1007/BF00236097

Harborne JB. Notizen: caffeic acid ester distribution in higher plants. Z Naturforsch B. 1966;21(6):604–5. https://doi.org/10.1515/znb-1966-0634

Bohm BA. Phenolic compounds in ferns—III. Phytochem. 1968;7(10):1825–30. https://doi.org/10.1016/S0031-9422(00)86654-6

Petersen M, Abdullah Y, Benner J, Eberle D, Gehlen K, Hücherig S, Janiak V, Kim K-H, Sander M, Weitzel C, Wolters S. Evolution of rosmarinic acid biosynthesis. Phytochem. 2009;70(15–16):1663–79. https://doi.org/10.1016/j.phytochem.2009.05.010

Hansen G, Wright MS. Recent advances in the transformation of plants. Trends Plant Sci. 1999;4(6):226–31. https://doi.org/10.1016/S1360-1385(99)01412-0

Ahmad S, Garg M, Tamboli ET, Abdin MZ, Ansari SH. In vitro production of alkaloids: Factors, approaches, challenges and prospects. Pharmacogn Rev. 2013;7(13):27–33. https://doi.org/10.4103/0973-7847.112837

Karam NS, Jawad FM, Arikat NA, Shibl RA. Growth and rosmarinic acid accumulation in callus, cell suspension, and root cultures of wild Salvia fruticosa. Plant Cell Tiss Org Cult. 2003;73(2):117–21. https://doi.org/10.1023/A:1022806420209

Kittipongpatana N, Hock RS, Porter JR. Production of solasodine by hairy root, callus, and cell suspension cultures of Solanum aviculare Forst. Plant Cell Tiss Org Cult. 1998; 52: 133–43. https://doi.org/10.1023/A:1005974611043

Sharma P, Padh H, Shrivastava N. Hairy root cultures: A suitable biological system for studying secondary metabolic pathways in plants. Eng Life Sci. 2013;13(1):62–75. https://doi.org/10.1002/elsc.201200030

Rekha K, Thiruvengadam M. Secondary metabolite production in transgenic hairy root cultures of cucurbits. Dans: Jha S, directeur. Transgenesis and secondary metabolism. Cham: Springer International Publishing; 2017. (Reference series in phytochemistry). https://doi.org/10.1007/978-3-319-28669-3_6

Yoshikawa T, Furuya T. Saponin production by cultures of Panax ginseng transformed with Agrobacterium rhizogenes. Plant Cell Rep. 1987;6(6):449–53. https://doi.org/10.1007/BF00272780

Yu K-W, Murthy HN, Hahn E-J, Paek K-Y. Ginsenoside production by hairy root cultures of Panax ginseng: influence of temperature and light quality. Biochem Eng J. 2005;23(1):53–6. https://doi.org/10.1016/j.bej.2004.07.001

Lee SY, Xu H, Kim YK, Park SU. Rosmarinic acid production in hairy root cultures of Agastache rugosa Kuntze. World J Microbiol Biotechnol. 2008;24(7):969–72. https://doi.org/10.1007/s11274-007-9560-y

Marchev AS, Yordanova ZP, Georgiev MI. Green (cell) factories for advanced production of plant secondary metabolites. Crit Rev Biotechnol. 2020;40(4):443–58. https://doi.org/10.1080/07388551.2020.1731414

Weremczuk-Je?yna I, Ska?a E, Olszewska MA, Kiss AK, Balcerczak E, Wysoki?ska H, Kicel A. The identification and quantitative determination of rosmarinic acid and salvianolic acid B in hairy root cultures of Dracocephalum forrestii W.W. Smith. Ind Crops Prod. 2016; 91:125–31. https://doi.org/10.1016/j.indcrop.2016.07.002

Dhakulkar S, Ganapathi TR, Bhargava S, Bapat VA. Induction of hairy roots in Gmelina arborea Roxb. and production of verbascoside in hairy roots. Plant Sci. 2005;169(5):812–8. https://doi.org/10.1016/j.plantsci.2005.05.014

Sudha CG, Obul Reddy B, Ravishankar GA, Seeni S. Production of ajmalicine and ajmaline in hairy root cultures of Rauvolfia micrantha Hook f., a rare and endemic medicinal plant. Biotechnol Lett. 2003;25(8):631–6. https://doi.org/10.1023/A:1023012114628

Gantait S, Mukherjee E. Hairy root culture technology: applications, constraints and prospect. Appl Microbiol Biotechnol. 2021;105(1):35–53. https://doi.org/10.1007/s00253-020-11017-9

Lin H, Kwok KH, Doran PM. Development of Linum flavum hairy root cultures for production of coniferin. Biotechnol Lett. 2003;25(7):521–5. https://doi.org/10.1023/A:1022821600283

Guillon S, Trémouillaux-Guiller J, Kumar Pati P, Gantet P. Hairy roots: a powerful tool for plant biotechnological advances. Dans: Ramawat KG, Merillon JM, directeurs. Bioactive molecules and medicinal plants. Berlin, Heidelberg: Springer Berlin Heidelberg; 2008. https://doi.org/10.1007/978-3-540-74603-4_14

Giri A, Dhingra V, Giri CC, Singh A, Ward OP, Narasu ML. Biotransformations using plant cells, organ cultures and enzyme systems: current trends and future prospects. Biotechnol Adv. 2001;19(3):175–99. https://doi.org/10.1016/S0734-9750(01)00054-4

Nakazawa T, Ohsawa K. Metabolism of rosmarinic acid in rats. J Nat Prod. 1998;61(8):993–6. https://doi.org/10.1021/np980072s

Ticli FK, Hage LIS, Cambraia RS, Pereira PS, Magro AJ, Fontes MRM, et al. Rosmarinic acid, a new snake venom phospholipase A2 inhibitor from Cordia verbenacea (Boraginaceae): antiserum action potentiation and molecular interaction. Toxicon. 2005;46(3):318–27. https://doi.org/10.1016/j.toxicon.2005.04.023

Jayanthy G, Subramanian S. Rosmarinic acid, a polyphenol, ameliorates hyperglycemia by regulating the key enzymes of carbohydrate metabolism in high fat diet – STZ induced experimental diabetes mellitus. Biomed Prev Nutr. 2014;4(3):431–7. https://doi.org/10.1016/j.bionut.2014.03.006

NCBI. [En ligne]. National Center for Biotechnology Information. PubChem Compound Summary for CID 5281792, Rosmarinic acid. [cited 5 May 2023]. Available from: https://pubchem.ncbi.nlm.nih.gov/compound/Rosmarinic-acid

Brewer MS. Natural antioxidants: sources, compounds, mechanisms of action, and potential applications. Comp Rev Food Sci Food Safety. 2011;10(4):221–47. https://doi.org/10.1111/j.1541-4337.2011.00156.x

Swamy MK, Sinniah UR, Ghasemzadeh A. Anticancer potential of rosmarinic acid and its improved production through biotechnological interventions and functional genomics. Appl Microbiol Biotechnol. 2018;102(18):7775–93. https://doi.org/10.1007/s00253-018-9223-y

Lefebvre T, Destandau E, Lesellier E. Sequential extraction of carnosic acid, rosmarinic acid and pigments (carotenoids and chlorophylls) from Rosemary by online supercritical fluid extraction-supercritical fluid chromatography. J Chromatogr A. 2021;1639:461709. https://doi.org/10.1016/j.chroma.2020.461709

Petersen M, Simmonds MSJ. Rosmarinic acid. Phytochem. 2003;62(2):121–5. https://doi.org/10.1016/S0031-9422(02)00513-7

De-Eknamkul W, Ellis BE. Tyrosine aminotransferase: The entrypoint enzyme of the tyrosine-derived pathway in rosmarinic acid biosynthesis. Phytochem. 1987;26(7):1941–6. https://doi.org/10.1016/S0031-9422(00)81734-3

D’Auria JC, Gershenzon J. The secondary metabolism of Arabidopsis thaliana: growing like a weed. Curr Opin Plant Biol. 2005;8(3):308–16. https://doi.org/10.1016/j.pbi.2005.03.012

Razzaque A, Ellis BE. Rosmarinic acid production in Coleus cell cultures. Planta. 1977;137(3):287–91. https://doi.org/10.1007/BF00388164

Petersen M. Cytochrome P450-dependent hydroxylation in the biosynthesis of rosmarinic acid in Coleus. Phytochem. 1997;45(6):1165–72. https://doi.org/10.1016/S0031-9422(97)00135-0

Petersen M, Häusler E, Karwatzki B, Meinhard J. Proposed biosynthetic pathway for rosmarinic acid in cell cultures of Coleus blumei Benth. Planta. 1993;189(1). https://doi.org/10.1007/BF00201337

Karwatzki B, Petersen M, Alfermann A. Transient activity of enzymes involved in the biosynthesis of rosmarinic acid in cell suspension cultures of Coleus blumei. Planta Med. 1989;55(07):663–4. https://doi.org/10.1055/s-2006-962258

Petersen M, Alfermann AW. Two new enzymes of rosmarinic acid biosynthesis from cell cultures of Coleus blumei: Hydroxyphenylpyruvate reductase and rosmarinic acid synthase. Z Naturforsch C. 1988;43(7–8):501–4. https://doi.org/10.1515/znc-1988-7-804

Häusler E, Petersen M, Alfermann AW. Hydroxyphenylpyruvate reductase from cell suspension cultures of Coleus blumei benth. Z Naturforsch C. 1991;46(5–6):371–6. https://doi.org/10.1515/znc-1991-5-607

Petersen MS. Characterization of rosmarinic acid synthase from cell cultures of Coleus blumei. Phytochem. 1991;30(9):2877–81. https://doi.org/10.1016/S0031-9422(00)98217-7

Matsuno M, Nagatsu A, Ogihara Y, Ellis BE, Mizukami H. CYP98A6 from Lithospermum erythrorhizon encodes 4-coumaroyl-4?-hydroxyphenyllactic acid 3-hydroxylase involved in rosmarinic acid biosynthesis. FEBS Lett. 2002;514(2–3):219–24. https://doi.org/10.1016/S0014-5793(02)02368-2

Kelm MA, Nair MG, Strasburg GM, DeWitt DL. Antioxidant and cyclooxygenase inhibitory phenolic compounds from Ocimum sanctum Linn. Phytomed. 2000;7(1):7–13. https://doi.org/10.1016/S0944-7113(00)80015-X

Huang YS, Zhang JT. Antioxidative effect of three water-soluble components isolated from Salvia miltiorrhiza in vitro. Yao Xue Xue Bao. 1992;27(2):96–100.

Kim G-D, Park YS, Jin Y-H, Park C-S. Production and applications of rosmarinic acid and structurally related compounds. Appl Microbiol Biotechnol. 2015;99(5):2083–92. https://doi.org/10.1007/s00253-015-6395-6

Nadeem M, Imran M, Aslam Gondal T, Imran A, Shahbaz M, Muhammad Amir R, Sajid MW, Qaisrani TB, Atif M, Hussain G, Salehi B, Ostrander EA, Martorell M, Rad JS, Cho WC, Martins N. Therapeutic potential of rosmarinic acid: A comprehensive review. NATO Adv Sci Inst Ser E Appl Sci. 2019;9(15):3139. https://doi.org/10.3390/app9153139

Song J, Wang Z. 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. 2011;124(1):183–92. https://doi.org/10.1007/s10265-010-0350-5

Amoah SKS, Sandjo LP, Kratz JM, Biavatti MW. Rosmarinic acid--pharmaceutical and clinical aspects. Planta Med. 2016;82(5):388–406. https://doi.org/10.1055/s-0035-1568274

Vostálová J, Zdarilová A, Svobodová A. Prunella vulgaris extract and rosmarinic acid prevent UVB-induced DNA damage and oxidative stress in HaCaT keratinocytes. Arch Dermatol Res. 2010;302(3):171–81. https://doi.org/10.1007/s00403-009-0999-6

Yang H, Wang H, Andersson U. Targeting inflammation driven by HMGB1. Front Immunol. 2020; 11: 484. https://doi.org/10.3389/fimmu.2020.00484

Chu X, Ci X, He J, Jiang L, Wei M, Cao Q, et al. Effects of a natural prolyl oligopeptidase inhibitor, rosmarinic acid, on lipopolysaccharide-induced acute lung injury in mice. Molecules. 2012;17(3):3586–98. https://doi.org/10.3390/molecules17033586

Wang J, Pan X, Han Y, Guo D, Guo Q, Li R. Rosmarinic acid from eelgrass shows nematicidal and antibacterial activities against pine wood nematode and its carrying bacteria. Mar Drugs. 2012;10(12):2729–40. https://doi.org/10.3390/md10122729

Abedini A, Roumy V, Mahieux S, Biabiany M, Standaert-Vitse A, Rivière C, Sahpaz S, Bailleul F, Neut C, Hennebelle T. Rosmarinic acid and its methyl ester as antimicrobial components of the hydromethanolic extract of Hyptis atrorubens Poit. (Lamiaceae). Evid Based Complement Alternat Med. 2013:604536. https://doi.org/10.1155/2013/604536

Daosen G, Guicai D, Li L, Ronggui L. Inhibitory activities of rosmarinic acid against plant pathogenic fungi. Wei Sheng wu xue Tong bao. 2004; 31: 71-76

Paluszczak J, Krajka-Ku?niak V, Baer-Dubowska W. The effect of dietary polyphenols on the epigenetic regulation of gene expression in MCF7 breast cancer cells. Toxicol Lett. 2010;192(2):119–25. https://doi.org/10.1016/j.toxlet.2009.10.010

Moon D-O, Kim M-O, Lee J-D, Choi YH, Kim G-Y. Rosmarinic acid sensitizes cell death through suppression of TNF-alpha-induced NF-kappaB activation and ROS generation in human leukemia U937 cells. Cancer Lett. 2010;288(2):183–91. https://doi.org/10.1016/j.canlet.2009.06.033

Xu Y, Xu G, Liu L, Xu D, Liu J. Anti-invasion effect of rosmarinic acid via the extracellular signal-regulated kinase and oxidation-reduction pathway in Ls174-T cells. J Cell Biochem. 2010;111(2):370–9. https://doi.org/10.1002/jcb.22708

Tai J, Cheung S, Wu M, Hasman D. Antiproliferation effect of Rosemary (Rosmarinus officinalis) on human ovarian cancer cells in vitro. Phytomedicine. 2012;19(5):436–43. https://doi.org/10.1016/j.phymed.2011.12.012

Dubois M, Bailly F, Mbemba G, Mouscadet J-F, Debyser Z, Witvrouw M, Cotelle P. Reaction of rosmarinic acid with nitrite ions in acidic conditions: discovery of nitro- and dinitrorosmarinic acids as new anti-HIV-1 agents. J Med Chem. 2008;51(8):2575–9. https://doi.org/10.1021/jm7011134

Psotová J, Lasovský J, Vicar J. Metal-chelating properties, electrochemical behavior, scavenging and cytoprotective activities of six natural phenolics. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2003;147(2):147–53. https://doi.org/10.5507/bp.2003.020

Osakabe N, Yasuda A, Natsume M, Sanbongi C, Kato Y, Osawa T, Yoshikawa T. Rosmarinic acid, a major polyphenolic component of Perilla frutescens, reduces lipopolysaccharide (LPS)-induced liver injury in D-galactosamine (D-GalN)-sensitized mice. Free Radic Biol Med. 2002;33(6):798–806. https://doi.org/10.1016/S0891-5849(02)00970-X

Kim D-S, Kim H-R, Woo E-R, Hong S-T, Chae H-J, Chae S-W. Inhibitory effects of rosmarinic acid on adriamycin-induced apoptosis in H9c2 cardiac muscle cells by inhibiting reactive oxygen species and the activations of c-Jun N-terminal kinase and extracellular signal-regulated kinase. Biochem Pharmacol. 2005;70(7):1066–78. https://doi.org/10.1016/j.bcp.2005.06.026

Xavier CPR, Lima CF, Fernandes-Ferreira M, Pereira-Wilson C. Salvia fruticosa, Salvia officinalis, and rosmarinic acid induce apoptosis and inhibit proliferation of human colorectal cell lines: the role in MAPK/ERK pathway. Nutr Cancer. 2009;61(4):564–71. https://doi.org/10.1080/01635580802710733

Makino T, Ono T, Muso E, Yoshida H, Honda G, Sasayama S. Inhibitory effects of rosmarinic acid on the proliferation of cultured murine mesangial cells. Nephrol Dial Transplant. 2000;15(8):1140–5. https://doi.org/10.1080/01635580802710733

Braidy N, Matin A, Rossi F, Chinain M, Laurent D, Guillemin GJ. Neuroprotective effects of rosmarinic acid on ciguatoxin in primary human neurons. Neurotox Res. 2014;25(2):226–34. https://doi.org/10.1007/s12640-013-9429-9

Bulgakov VP, Inyushkina YV, Fedoreyev SA. Rosmarinic acid and its derivatives: biotechnology and applications. Crit Rev Biotechnol. 2012;32(3):203–17. https://doi.org/10.1007/s12640-013-9429-9

Choi S-H, Jang G-W, Choi S-I, Jung T-D, Cho B-Y, Sim W-S, Han X, Lee JS, Kim DY, Kim DB, Lee OH. Development and validation of an analytical method for carnosol, carnosic acid and rosmarinic acid in food matrices and evaluation of the antioxidant activity of Rosemary extract as a food additive. Antioxidants (Basel). 2019;8(3). https://doi.org/10.3390/antiox8030076

Guitard R, Paul J-F, Nardello-Rataj V, Aubry J-M. Myricetin, rosmarinic and carnosic acids as superior natural antioxidant alternatives to ?-tocopherol for the preservation of omega-3 oils. Food Chem. 2016; 213: 284–95. https://doi.org/10.3390/antiox8030076

Klisurova D, Petrova I, Ognyanov M, Georgiev Y, Kratchanova M, Denev P. Co-pigmentation of black chokeberry (Aronia melanocarpa) anthocyanins with phenolic co-pigments and herbal extracts. Food Chem. 2019; 279: 162–70. https://doi.org/10.3390/antiox8030076

Mesnier X, Gregory C, Fanca-Berthon P, Boukobza F, Bily A. Heat and light colour stability of beverages coloured with a natural carotene emulsion: Effect of synthetic versus natural water soluble antioxidants. Food Res Int. 2014; 65:149–55. https://doi.org/10.1016/j.foodres.2014.06.025

Isah T, Umar S, Mujib A, Sharma MP, Rajasekharan PE, Zafar N, Frukh A. Secondary metabolism of pharmaceuticals in the plant in vitro cultures: strategies, approaches, and limitations to achieving higher yield. Plant Cell Tiss Org Cult. 2017;132(2):1–27. https://doi.org/10.1007/s11240-017-1332-2

Murthy HN, Lee E-J, Paek K-Y. Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation. Plant Cell Tiss Organ Cult. 2014;118(1):1–16. https://doi.org/10.1007/s11240-014-0467-7

Grzegorczyk I, Królicka A, Wysoki?ska H. Establishment of Salvia officinalis L. hairy root cultures for the production of rosmarinic acid. Z Naturforsch, C, J Biosci. 2006;61(5–6):351–6. https://doi.org/10.1515/znc-2006-5-609

Grzegorczyk I, Wysoki?ska H. Antioxidant compounds in Salvia officinalis L. shoot and hairy root cultures in the nutrient sprinkle bioreactor. Acta Soc Bot Pol. 2011;79(1):7–10. https://doi.org/10.5586/asbp.2010.001

Ruffoni B, Bertoli A, Pistelli L, Pistelli L. Micropropagation of Salvia wagneriana Polak and hairy root cultures with rosmarinic acid production. Nat Prod Res. 2016;30(22):2538–44. https://doi.org/10.1080/14786419.2015.1120725

Grzegorczyk-Karolak I, Ku?ma ?, Ska?a E, Kiss AK. Hairy root cultures of Salvia viridis L. for production of polyphenolic compounds. Ind Crops Prod. 2018; 117: 235–44. https://doi.org/10.1016/j.indcrop.2018.03.014

Wojciechowska M, Owczarek A, Kiss AK, Gr?bkowska R, Olszewska MA, Grzegorczyk-Karolak I. Establishment of hairy root cultures of Salvia bulleyana Diels for production of polyphenolic compounds. J Biotechnol. 2020; 318: 10–9. https://doi.org/10.1016/j.jbiotec.2020.05.002

Brockman IM, Prather KLJ. Dynamic metabolic engineering: New strategies for developing responsive cell factories. Biotechnol J. 2015;10(9):1360–9. https://doi.org/10.1002/biot.201400422

Hain R, Grimmig B. Modification of plant secondary metabolism by genetic engineering. Dans: Verpoorte R, Alfermann AW, directeurs. Metabolic Engineering of Plant Secondary Metabolism. Dordrecht: Springer Netherlands; 2000. p. 217–31. https://doi.org/10.1007/978-94-015-9423-3_11

Ma P, Liu J, Zhang C, Liang Z. Regulation of water-soluble phenolic acid biosynthesis in Salvia miltiorrhiza Bunge. Appl Biochem Biotechnol. 2013;170(6):1253–62. https://doi.org/10.1007/s12010-013-0265-4

Xiao Y, Zhang L, Gao S, Saechao S, Di P, Chen J, Chen W. The c4h, tat, hppr and hppd genes prompted engineering of rosmarinic acid biosynthetic pathway in Salvia miltiorrhiza hairy root cultures. PLoS ONE. 2011;6(12):e29713. https://doi.org/10.1371/journal.pone.0029713

Butelli E, Titta L, Giorgio M, Mock H-P, Matros A, Peterek S, Schijlen EGWM, Hall RD, Bovy AG, Luo J, Martin C. Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol. 2008;26(11):1301–8. https://doi.org/10.1038/nbt.1506

Wang D, Song Y, Chen Y, Yao W, Li Z, Liu W, Yue S, Wang Z. Metabolic pools of phenolic acids in Salvia miltiorrhiza are enhanced by co-expression of Antirrhinum majus Delila and Rosea1 transcription factors. Biochem Eng J. 2013;74:115–20. https://doi.org/10.1016/j.bej.2013.02.014

Bielecka M, Zielinska S, Pencakowski B, Stafiniak M, Slusarczyk S, Prescha A, Matkowski A. Age-related variation of polyphenol content and expression of phenylpropanoid biosynthetic genes in Agastache rugosa. Ind Crops Prod. 2019;141:111743. https://doi.org/10.1016/j.indcrop.2019.111743

Veliky IA, Martin SM. A fermenter for plant cell suspension cultures. Can J Microbiol. 1970; 16(4): 223-226. https://doi.org/10.1139/m70-041

Zhang S, Li H, Liang X, Yan Y, Xia P, Jia Y, Liang Z. 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. 2015;103(103):185–92. https://doi.org/10.1016/j.bej.2015.07.019

Fu R, Shi M, Deng C, Zhang Y, Zhang X, Wang Y, Jai G. Improved phenolic acid content and bioactivities of Salvia miltiorrhiza hairy roots by genetic manipulation of RAS and CYP98A14. Food Chem. 2020;331:127365. https://doi.org/10.1016/j.foodchem.2020.127365

Deng C, Wang Y, Huang F, Lu S, Zhao L, Ma X, et al. SmMYB2 promotes salvianolic acid biosynthesis in the medicinal herb Salvia miltiorrhiza. J Integr Plant Biol. 2020;62(11):1688–702. https://doi.org/10.1111/jipb.12943

Hao X, Pu Z, Cao G, You D, Zhou Y, Deng C, Shi M, Nile SH, Wang Y, Zhou W, Kai G. Tanshinone and salvianolic acid biosynthesis are regulated by SmMYB98 in Salvia miltiorrhiza hairy roots. J Advert Res. 2020;23:1–12. https://doi.org/10.1016/j.jare.2020.01.012

Xiao Y, Gao S, Di P, Chen J, Chen W, Zhang L. Methyl jasmonate dramatically enhances the accumulation of phenolic acids in Salvia miltiorrhiza hairy root cultures. Physiol Plant. 2009;137(1):1–9. https://doi.org/10.1111/j.1399-3054.2009.01257.x

Gu X-C, Chen J-F, Xiao Y, Di P, Xuan H-J, Zhou X, Zhang L, Chen WS. Overexpression of allene oxide cyclase promoted tanshinone/phenolic acid production in Salvia miltiorrhiza. Plant Cell Rep. 2012;31(12):2247–59. https://doi.org/10.1007/s00299-012-1334-9

Ziegler J, Stenzel I, Hause B, Maucher H, Hamberg M, Grimm R, Ganal M, Wasternack C. Molecular cloning of allene oxide cyclase. The enzyme establishing the stereochemistry of octadecanoids and jasmonates. J Biol Chem. 2000;275(25):19132–8. https://doi.org/10.1074/jbc.M002133200

Yang N, Zhou W, Su J, Wang X, Li L, Wang L, Cao X, Wang Z. Overexpression of SmMYC2 increases the production of phenolic acids in Salvia miltiorrhiza. Front Plant Sci. 2017;8. https://doi.org/10.3389/fpls.2017.01804

Yang C-Q, Fang X, Wu X-M, Mao Y-B, Wang L-J, Chen X-Y. Transcriptional regulation of plant secondary metabolism. J Integr Plant Biol. 2012;54(10):703–12. https://doi.org/10.1111/j.1744-7909.2012.01161.x

Xing B, Liang L, Liu L, Hou Z, Yang D, Yan K, Zhang X, Liang Z. Overexpression of SmbHLH148 induced biosynthesis of tanshinones as well as phenolic acids in Salvia miltiorrhiza hairy roots. Plant Cell Rep. 2018;37(12):1681–92. https://doi.org/10.1007/s00299-018-2339-9

Halder M, Sarkar S, Jha S. Elicitation: A biotechnological tool for enhanced production of secondary metabolites in hairy root cultures. Eng Life Sci. 2019;19(12):880–95. https://doi.org/10.1002/elsc.201900058

Vasconsuelo A, Boland R. Molecular aspects of the early stages of elicitation of secondary metabolites in plants. Plant Sci. 2007;172(5):861–75. https://doi.org/10.1016/j.plantsci.2007.01.006

Chen H, Chen F. Induction of phytoalexin formation in crown gall and hairy root culture of Salvia miltiorrhiza by methyl viologen. Biotechnol Lett. 2000; 22: 715-720. https://doi.org/10.1023/A:1005696022081

Chen H, Chena F, Chiu FC, Lo CM. The effect of yeast elicitor on the growth and secondary metabolism of hairy root cultures of Salvia miltiorrhiza. Enzyme Microb Technol. 2001;28(1):100–5. https://doi.org/10.1016/S0141-0229(00)00284-2

Yan Q, Shi M, Ng J, Wu JY. Elicitor-induced rosmarinic acid accumulation and secondary metabolism enzyme activities in Salvia miltiorrhiza hairy roots. Plant Sci. 2006;170(4):853–8. https://doi.org/10.1016/j.plantsci.2005.12.004

Zhang S, Yan Y, Wang B, Liang Z, Liu Y, Liu F, Qi Z. Selective responses of enzymes in the two parallel pathways of rosmarinic acid biosynthetic pathway to elicitors in Salvia miltiorrhiza hairy root cultures. J Biosci Bioeng. 2014;117(5):645–51. https://doi.org/10.1016/j.jbiosc.2013.10.013

Yan Y, Zhang S, Zhang J, Ma P, Duan J, Liang Z. Effect and mechanism of endophytic bacteria on growth and secondary metabolite synthesis in Salvia miltiorrhiza hairy roots. Acta Physiol Plant. 2014;36(5):1095–105. https://doi.org/10.1007/s11738-014-1484-1

Attaran Dowom S, Abrishamchi P, Radjabian T, Salami SA. Elicitor-induced phenolic acids accumulation in Salvia virgata Jacq. hairy root cultures. Plant Cell Tissue Organ Cult. 2022;148(1):107–17. https://doi.org/10.1007/s11240-021-02170-8

Krzemi?ska M, Owczarek A, Gonciarz W, Chmiela M, Olszewska MA, Grzegorczyk-Karolak I. The antioxidant, cytotoxic and antimicrobial potential of phenolic acids-enriched extract of elicited hairy roots of Salvia bulleyana. Molecules. 2022;27(3). https://doi.org/10.3390/molecules27030992

Liang Z, Ma Y, Xu T, Cui B, Liu Y, Guo Z, Yang D. Effects of abscisic acid, gibberellin, ethylene and their interactions on production of phenolic acids in Salvia miltiorrhiza bunge hairy roots. PLoS ONE. 2013;8(9):e72806. https://doi.org/10.1371/journal.pone.0072806

Hong LokeKah [Hong LKM, Bhatt A, NingShu P, ChanLai K. Detection of elicitation effect on Hyoscyamus niger L. root cultures for the root growth and production of tropane alkaloids. Roman Biotechnol Lett. 2012; 17(3): 7340-51.

Xing B, Yang D, Liu L, Han R, Sun Y, Liang Z. Phenolic acid production is more effectively enhanced than tanshinone production by methyl jasmonate in Salvia miltiorrhiza hairy roots. Plant Cell Tissue Organ Cult. 2018;134(1):119–29. https://doi.org/10.1007/s11240-018-1405-x

Li J, Li B, Luo L, Cao F, Yang B, Gao J, et al. Increased phenolic acid and tanshinone production and transcriptional responses of biosynthetic genes in hairy root cultures of Salvia przewalskii Maxim. treated with methyl jasmonate and salicylic acid. Mol Biol Rep. 2020;47(11):8565–78. https://doi.org/10.1007/s11033-020-05899-1

Grzegorczyk-Karolak I, Krzemi?ska M, Kiss AK, Olszewska MA, Owczarek A. Phytochemical profile and antioxidant activity of aerial and underground parts of Salvia bulleyana Diels. Plants. Metabolites. 2020;10(12). https://doi.org/10.3390/metabo10120497

Liu L, Yang D, Liang T, Zhang H, He Z, Liang Z. Phosphate starvation promoted the accumulation of phenolic acids by inducing the key enzyme genes in Salvia miltiorrhiza hairy roots. Plant Cell Rep. 2016;35(9):1933–42. https://doi.org/10.1007/s00299-016-2007-x

Zhou J, Xu Z, Ran Z, Fang L, Guo L. Effects of smoke-water and smoke-derived butenolide on accumulation of phenolic acids in cultured hairy roots of Salvia miltiorrhiza Bung. Bangladesh J Bot. 2018;47(3):479–85. https://doi.org/10.3329/bjb.v47i3.38715

Mishra BN, Ranjan R. Growth of hairy-root cultures in various bioreactors for the production of secondary metabolites. Biotechnol Appl Biochem. 2008;49(1):1–10. https://doi.org/10.1042/BA20070103?

Published

23-11-2023 — Updated on 21-12-2023

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Shriti S, Kuldeep Prasad A, Narasimha Sudheer W, Praveen N. Hairy roots as a potential source for the production of rosmarinic acid from genus Salvia . Plant Sci. Today [Internet]. 2023 Dec. 21 [cited 2024 Dec. 22];10(sp2). Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/2541

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Special issue on Mini Reviews