Enhancement of Phytosterol and Triterpenoid Production in Plant Hairy Root Cultures—Simultaneous Stimulation or Competition?
Abstract
:1. Introduction
2. Hairy Root Cultures
3. Elicitation
4. Competition between General and Specialized Metabolism in Plant Response to Elicitation
5. Biosynthesis of Terpenoids
6. The Problem of the Common Pathway in Triterpenoid Biosynthesis
7. Sterols versus Triterpenoids in Hairy Roots—Competition
8. Sterols and Triterpenoids in Hairy Roots—Parallel Enhancement
9. Discussion
10. Concluding Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Bensaddek, L.; Villarreal, M.L.; Fliniaux, M.A. Induction and growth of hairy roots for the production of medical compounds. Electron. J. Integr. Biosci. 2008, 3, 2–9. [Google Scholar]
- Zhou, L.; Wu, J. Development and application of medicinal plant tissue cultures for production of drugs and herbal medicinal in China. Nat. Prod. Rep. 2006, 23, 789–810. [Google Scholar] [CrossRef]
- Chandra, S.; Chandra, R. Engineering secondary metabolite production in hairy roots. Phytochem. Rev. 2011, 10, 371–375. [Google Scholar] [CrossRef]
- Li, P.; Lou, J.; Mou, Y.; Sun, W.; Shan, T.; Zhou, L. Effects of oligosaccharide elicitors from endophyitc Fusarium oxysporum Dzf17 on diosgenin accumulation in Dioscorea zingiberensis seedling cultures. J. Med. Plants Res. 2012, 6, 5128–5134. [Google Scholar]
- Sivanandhan, G.; Selvaraj, N.; Ganapathi, A.; Manickavasagam, M. Enhanced biosynthesis of withanolides by elicitation and precursor feeding in cell suspension culture of Withania somnifera (L.) Dunal in shake-flask culture and bioreactor. PLoS ONE 2014, 9, e104005. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Muffler, K.; Leipold, D.; Scheller, M.C.; Haas, C.; Steingroewer, J.; Bley, T.; Neuhaus, H.E.; Mirata, M.A.; Schrader, J.; Ulber, R. Biotranformation of triterpenes. Process Biochem. 2011, 46, 1–15. [Google Scholar] [CrossRef]
- Hussain, M.S.; Fareed, S.; Ansari, S.; Rahman, M.A.; Ahmad, I.Z.; Saeed, M. Current approaches toward production of secondary plant metabolites. J. Pharm. Bioallied Sci. 2012, 4, 10–20. [Google Scholar] [CrossRef] [PubMed]
- Isah, T.; Umar, S.; Mujib, A.; Sharma, M.P.; Rajasekharan, P.E.; Zafar, N.; Frukh, A. Secondary metabolism of pharmaceuticals in the plant in vitro cultures: Strategies, approaches, and limitations to achieving higher yield. Plant Cell Tissue Organ Cult. 2018, 132, 239–265. [Google Scholar] [CrossRef]
- Georgiev, M.I.; Pavlov, A.I.; Bley, T. Hairy root type plant in vitro systems as sources of bioactive substances. Appl. Microbiol. Biotechnol. 2007, 74, 1175–1185. [Google Scholar] [CrossRef]
- Ono, N.N.; Tian, L. The multiplicity of hairy root cultures: Prolific possibilities. Plant Sci. 2011, 180, 439–446. [Google Scholar] [CrossRef] [PubMed]
- Mehrotra, S.; Srivastava, V.; Rahman, L.U.; Kukreja, A.K. Hairy root biotechnology—Indicative timeline to understand missing links and future outlook. Protoplasma 2015, 252, 1189–1201. [Google Scholar] [CrossRef]
- Riker, A.J.; Banfield, W.M.; Wright, W.H.; Keitt, G.W.; Sagen, H.E. Studies on infectious hairy root of nursery apple trees. J. Agric. Res. 1930, 41, 507–540. [Google Scholar]
- Chandra, S. Natural plant genetic engineer Agrobacterium rhizogenes: Role of T-DNA in plant secondary metabolism. Biotechn. Lett. 2012, 34, 407–415. [Google Scholar] [CrossRef]
- Georgiev, M.I.; Agostini, E.; Ludwig-Müller, J.; Xu, J. Genetically transformed roots: From plant disease to biotechnological resource. Trends Biotechnol. 2012, 30, 528–537. [Google Scholar] [CrossRef]
- Gutierrez-Valdes, N.; Häkkinen, S.T.; Lemasson, C.; Guillet, M.; Oksman-Caldentey, K.M.; Ritala, A.; Cardon, F. Hairy rootcultures—A versatile tool with multiple applications. Front. Plant Sci. 2020, 11, 33. [Google Scholar] [CrossRef]
- Mauro, M.L.; Costantino, P.; Bettini, P.P. The neverending story of rol genes: A century after. Plant Cell Tissue Organ Cult. 2017, 131, 201–212. [Google Scholar] [CrossRef]
- Hamill, J.D.; Parr, A.J.; Rhodes, M.J.; Robins, R.J.; Walton, N.J. New routes to plant secondary products. Nat. Biotechnol. 1987, 5, 800–804. [Google Scholar] [CrossRef]
- Giri, A.; Narasu, M.L. Transgenic hairy roots: Recent trends and applications. Biotechnol. Adv. 2000, 18, 1–22. [Google Scholar] [CrossRef]
- Bulgakov, V.P.; Shkryl, Y.N.; Veremeichik, G.N.; Gorpenchenko, T.Y.; Vereshchagina, Y.V. Recent Advances in the Understanding of Agrobacterium rhizogenes—Derived Genes and Their Effects on Stress Resistance and Plant Metabolism. In Biotechnology of Hairy Root Systems. Advances in Biochemical Engineering/Biotechnology; Doran, P., Ed.; Springer: Berlin/Heidelberg, Germany, 2013; Volume 134, pp. 1–22. [Google Scholar]
- Markowski, M.; Długosz, M.; Szakiel, A.; Durli, M.; Poinsignon, S.; Bouguet-Bonnet, S.; Henry, M. Increased synthesis of a new oleanane-type saponin in hairy roots of marigold (Calendula officinalis) after treatment with jasmonic acid. Nat. Prod. Res. 2019, 33, 1218–1222. [Google Scholar] [CrossRef] [PubMed]
- Savitha, B.C.; Thimmaraju, R.; Bhagyalakshmi, N.; Ravishankar, G.A. Different biotic and abiotic elicitors influence betalain production in hairy root cultures of Beta vulgaris in shake-flask and bioreactor. Process Biochem. 2006, 41, 50–60. [Google Scholar] [CrossRef]
- Halder, M.; Roychowdhury, D.; Jha, S. A Critical Review on Biotechnological Interventions for Production and Yield Enhancement of Secondary Metabolites in Hairy Root Cultures. In Hairy Roots; Srivastava, V., Mehrotra, S., Mishra, S., Eds.; Springer: Singapore, 2018; pp. 21–44. [Google Scholar]
- Jozwiak, A.; Ples, M.; Skorupinska-Tudek, K.; Kania, M.; Dydak, M.; Danikiewicz, W.; Swiezewska, E. Sugar availability modulates polyisoprenoid and phytosterol profiles in Arabidopsis thaliana hairy root culture. Biochim. Biophys. Acta Mol. Cell Biol. Lipids. 2013, 1831, 438–447. [Google Scholar] [CrossRef]
- Manuhara, Y.S.W.; Kristanti, A.N.; Utami, E.S.W.; Yachya, A. Effect of sucrose and potassium nitrate on biomass and saponin content of Talinum paniculatum Gaertn. hairy root in balloon-type bubble bioreactor. Asian Pac. J. Trop. Biomed. 2015, 5, 1027–1032. [Google Scholar] [CrossRef]
- Faizal, A.; Sari, A.V. Enhancement of saponin accumulation in adventitious root culture of Javanese ginseng (Talinum paniculatum Gaertn.) through methyl jasmonate and salicylic acid elicitation. Afr. J. Biotechnol. 2019, 18, 130–135. [Google Scholar]
- Długosz, M.; Markowski, M.; Pączkowski, C. Source of nitrogen as a factor limiting saponin production by hairy root and suspension cultures of Calendula officinalis L. Acta Physiol. Plant. 2018, 40, 1–14. [Google Scholar] [CrossRef] [Green Version]
- Hussain, A.; Quarsi, I.A.; Nazir, H.; Ullah, I. Plant tissue culture: Current status and opportunities. In Recent Advances in Plant In Vitro Culture; Leva, A., Rinaldi, L.M.R., Eds.; IntechOpen: Rijeka, Croatia, 2012; pp. 1–29. [Google Scholar]
- Naik, P.M.; Al–Khayri, J.M. Abiotic and Biotic Elicitors—Role in Secondary Metabolites Production Through In Vitro Culture of Medicinal Plants. In Abiotic and Biotic Stress in Plants—Recent Advances and Future Perspectives; Shanker, A.K., Shanker, C., Eds.; InTech: Rijeka, Croatia, 2016; pp. 247–278. [Google Scholar]
- Namdeo, A.G. Plant cell elicitation for production of secondary metabolites: A review. Pharmacogn. Rev. 2007, 1, 69–79. [Google Scholar]
- Patel, H.; Krishnamurthy, R. Elicitors in plant tissue culture. J. Pharmacogn. Phytochem. 2013, 2, 60–65. [Google Scholar]
- Thakur, M.; Sohal, B.S. Role of elicitors in inducing resistance in plants against pathogen infection: A review. ISRN Biochem. 2013, 2013, 762412. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, J.; Davis, L.C.; Verpoorte, R. Elicitor signal transduction leading to production of plant secondary metabolites. Biotech. Adv. 2005, 23, 283–333. [Google Scholar] [CrossRef] [PubMed]
- Zhang, B.; Zheng, L.P.; Wang, J.W. Nitric oxide elicitation for secondary metabolite production in cultured plant cells. Appl. Microbiol. Biotechnol. 2012, 93, 455–466. [Google Scholar] [CrossRef] [PubMed]
- Ramirez-Estrada, K.; Vidal-Limon, H.; Hidalgo, D.; Moyano, E.; Goleniowski, M.; Cusidó, R.M.; Palazon, J. Elicitation, an effective strategy for the biotechnological production of bioactive high-added value compounds in plant cell factories. Molecules 2016, 21, 182. [Google Scholar] [CrossRef]
- Yang, L.; Wen, K.S.; Ruan, X.; Zhao, Y.X.; Wei, F.; Wang, Q. Response of plant secondary metabolites to environmental factors. Molecules 2018, 23, 762. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Takken, W.; Dicke, M. Chemical Ecology—A Multidisciplinary Approach. In Chemical Ecology: From Gene to Ecosystem; Springer Science & Business Media: Berlin, Germany, 2006; Volume 16, pp. 1–8. [Google Scholar]
- Neilson, E.H.; Goodger, J.Q.D.; Woodrow, I.E.; Möller, B.L. Plant chemical defense: At what cost? Trends Plant Sci. 2013, 18, 250–258. [Google Scholar] [CrossRef] [PubMed]
- Fiorucci, A.S. To grow or defend? More on the plant Cornelian dilemma. Plant Physiol. 2020, 183, 437–438. [Google Scholar] [CrossRef] [PubMed]
- Garagounis, C.; Delkis, N.; Papadopoulou, K.K. Unraveling the roles of plant specialized metabolites using synthetic biology to design molecular biosensors. New Phytol. 2012, 231, 1338–1352. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Wang, H.; Ye, H.C.; Li, G.F. Advances in the plant isoprenoid biosynthesis pathway and its metabolic engineering. J. Integr. Plant Biol. 2005, 47, 769–782. [Google Scholar] [CrossRef]
- Moses, T.; Pollier, J.; Thevelein, J.M.; Goossens, A. Bioengineering of plant triterpenoids: From metabolic engineering of plants to synthetic biology in vivo and in vitro. New Phytol. 2013, 200, 27–43. [Google Scholar] [CrossRef]
- Mahato, S.B.; Nandy, A.K.; Roy, G. Triterpenoids. Phytochemistry 1992, 31, 2199–2249. [Google Scholar] [CrossRef]
- Hemmerlin, A.; Harwood, J.L.; Bach, T.J. A raison d’être for two distinct pathways in the early steps of plant isoprenoid biosynthesis? Prog. Lipid Res. 2012, 51, 95–148. [Google Scholar] [CrossRef]
- Kumari, S.; Priya, P.; Misra, G.; Yadav, G. Structural and biochemical perspectives in plant isoprenoid biosynthesis. Phytochem. Rev. 2013, 12, 255–291. [Google Scholar] [CrossRef]
- Jozwiak, A.; Lipko, A.; Kania, M.; Danikiewicz, W.; Surmacz, L.; Witek, A.; Wojcik, J.; Zdanowski, K.; Pączkowski, C.; Chojnacki, T.; et al. Modelling of dolichol mass spectra isotopic envelopes as a tool to monitor isoprenoid biosynthesis. Plant Physiol. 2017, 174, 857–874. [Google Scholar] [CrossRef]
- Phillips, M.A.; D’Auria, J.C.; Gershenzon, J.; Pichersky, E. The Arabidopsis thaliana type I isopentenyl diphosphate isomerases are targeted to multiple subcellular compartments and have overlapping functions in isoprenoid biosynthesis. Plant Cell 2008, 20, 677–696. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Naraki, S.; Kakihara, M.; Kato, S.; Saga, Y.; Mannen, K.; Takase, S.; Takano, A.; Shinpo, S.; Hosouchi, T.; Nakane, T.; et al. Two triterpene synthases from Imperata cylindrica catalyzing the formation of as pair of diastereoisomers through boat or chair cyclization. ChemBioChem 2021, 22, 1992–2001. [Google Scholar] [CrossRef] [PubMed]
- Biswas, T.; Dwivedi, U.N. Plant triterpenoid saponins: Biosynthesis, in vitro production, and pharmacological relevance. Protoplasma 2019, 256, 1462–1486. [Google Scholar] [CrossRef] [PubMed]
- Ghosh, S. Biosynthesis of structurally diverse triterpenes in plants: The role of oxidosqualene cyclases. Proc. Indian Natl. Sci. Acad. 2016, 82, 1189–1210. [Google Scholar] [CrossRef]
- Gao, W.; Dong, X.; Wei, T.; Xing, W. The chemical structure and bioactivity of cycloartane-type compounds. Curr. Org. Chem. 2019, 23, 25. [Google Scholar] [CrossRef]
- Moreau, R.A.; Whitaker, B.D.; Hicks, K.B. Phytosterols, phytostanols, and their conjugates in foods: Structural diversity, quantitative analysis, and health-promoting uses. Prog. Lipid Res. 2002, 41, 457–500. [Google Scholar] [CrossRef]
- Rogowska, A.; Szakiel, A. The role of sterols in plant response to abiotic stress. Phyt. Rev. 2020, 19, 1525–1538. [Google Scholar] [CrossRef]
- Kamisako, W.; Morimoto, K.; Makino, I.; Isoi, K. Changes in triterpenoid content during the growth cycle of cultured plant cells. Plant Cell Physiol. 1984, 25, 1571–1574. [Google Scholar] [CrossRef]
- Flores-Sánchez, I.J.; Ortega-López, J.; del Carmen Montes-Horcasitas, M.; Ramos-Valdivia, A.C. Biosynthesis of sterols and triterpenesin cell suspension cultures of Uncaria tomentosa. Plant Cell Physiol. 2002, 43, 1502–1509. [Google Scholar] [CrossRef] [Green Version]
- Van der Heijden, R.; Threlfall, D.R.; Verpoorte, R.; Whitehead, I.M. Regulation and enzymology of pentacyclic triterpenoid phytoalexin biosynthesis in cell suspension cultures of Tabernaemontana divaricata. Phytochemistry 1989, 28, 2981–2988. [Google Scholar] [CrossRef]
- Ayabe, S.; Takano, H.; Fujito, T.; Furuya, T.; Hitota, H.; Takamashi, T. Triterpenoid biosynthesis in tissue cultures of Glycyrrhiza glabra var. glandulifera. Plant Cell Rep. 1990, 9, 181–184. [Google Scholar] [CrossRef]
- Liang, Y.; Zhao, S. Progress in understanding of ginsenoside biosynthesis. Plant Biol. 2008, 10, 415–421. [Google Scholar] [CrossRef]
- Liang, Y.; Zhao, S.; Zhang, X. Antisense suppression of cycloartenol synthase results in elevated ginsenoside levels in Panax ginseng hairy roots. Plant Mol. Biol. Rep. 2009, 27, 298–304. [Google Scholar] [CrossRef]
- Kim, Y.S.; Cho, J.H.; Park, S.; Han, J.Y.; Back, K.; Choi, Y.E. Gene regulation patterns in triterpene biosynthetic pathway driven by overexpression of squalene synthase and methyl jasmonate elicitation in Bupleurum falcatum. Planta 2011, 233, 343–355. [Google Scholar] [CrossRef]
- Kim, O.T.; Kim, S.H.; Ohyama, K.; Muranaka, T.; Choi, Y.E.; Lee, H.Y.; Kim, M.Y.; Hwang, B. Upregulation of phytosterol and triterpene biosynthesis in Centiella asiatica hairy roots overexpressed ginseng farnesyl diphosphate synthase. Plant Cell Rep. 2010, 29, 403–411. [Google Scholar] [CrossRef]
- Alsoufi, A.S.M.; Pączkowski, C.; Szakiel, A.; Długosz, M. Effect of jasmonic acid and chitosan on triterpenoid production in Calendula officinalis hairy root cultures. Phytochem. Lett. 2019, 31, 5–11. [Google Scholar] [CrossRef]
- Alsoufi, A.S.M.; Staśkiewicz, K.; Markowski, M. Alterations in oleanolic acid and sterol content in marigold (Calendula officinalis) hairy root cultures in response to stimulation by selected phytohormones. Acta Physiol. Plant. 2021, 43, 44. [Google Scholar] [CrossRef]
- Lee, M.H.; Jeong, J.H.; Seo, J.W.; Shin, C.G.; Kim, Y.C.; In, Y.G.; Yang, D.C.; Yi, J.S.; Choi, Y.E. Enhanced triterpene and phytosterol biosynthesis in Panax ginseng overexpressing squalene synthase gene. Plant Cell Physiol. 2004, 45, 976–984. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, Y.K.; Kim, Y.B.; Uddin, M.R.; Lee, S.; Kim, S.U.; Park, S.U. Enhanced triterpene accumulation in Panax ginseng hairy roots overexpressing mevalonate-5-pyrophosphate decarboxylase and farnesyl pyrophosphate synthase. ACS Synth. Biol. 2014, 3, 773–779. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.K.; Kim, J.K.; Kim, Y.B.; Sanghyun, L.; Kim, S.U.; Park, S.U. Enhanced accumulation of phytosterol and triterpene in hairy root cultures of Platycodon grandifolium by overexpression of Panax ginseng 3-hydroxyl-3-methylglutaryl-coenzym A reductase. J. Agric. Food Chem. 2013, 61, 1928–1934. [Google Scholar] [CrossRef] [PubMed]
- Alsoufi, A.S.M.; Pączkowski, C.; Długosz, M.; Szakiel, A. Influence of selected abiotic factors on triterpenoid biosynthesis and saponin secretion in marigold (Calendula officinalis L.) in vitro hairy root cultures. Molecules 2019, 24, 2907. [Google Scholar] [CrossRef] [Green Version]
- Yang, J.L.; Hu, Z.F.; Zhang, T.T.; Gu, A.D.; Gong, T.; Zhu, P. Progress on the studies of the key enzymes of ginsenoside biosynthesis. Molecules 2018, 23, 589. [Google Scholar] [CrossRef] [Green Version]
- Ayora-Talavera, T.; Chappell, J.; Lozoya-Gloria, E.; Loyola-Vargas, V.M. Overexpression in Catharanthus roseus hairy roots of a truncated hamster 3-hydroxy-3-methylglutaryl-CoS reductase gene. Appl. Biochem. Biotechnol. 2002, 97, 135–144. [Google Scholar] [CrossRef]
- Yendo, A.C.A.; de Costa, F.; Gosmann, G.; Fett-Neto, A.G. Production of plant bioactive triterpenoid saponins: Elicitation strategies and target genes to improve yield. Mol. Biotechnol. 2010, 46, 94–104. [Google Scholar] [CrossRef]
- Zhou, M.L.; Zhu, X.M.; Shao, J.R.; Tang, Y.X.; Wu, Y.M. Production and metabolic engineering of bioactive substances in plant hairy root culture. Appl. Microbiol. Biotechnol. 2011, 90, 1229–1239. [Google Scholar] [CrossRef] [PubMed]
- Miraz-Moreno, B.; Sabater-Jara, A.B.; Pedreño, M.A.; Almagro, L. Bioactivity of phytosterols and their production in plant in vitro cultures. J. Agric. Food Chem. 2016, 64, 7049–7058. [Google Scholar] [CrossRef] [PubMed]
- Zolfaghari, F.; Rashidi-Monfared, S.; Moieni, A.; Abedini, D.; Ebrahimi, A. Improving diosgenin production and its biosynthesis in Trigonella foenum-graecum L. hairy root cultures. Ind. Crops Prod. 2020, 145, 112075. [Google Scholar] [CrossRef]
- Kohsari, S.; Rezayian, M.; Niknam, V.; Mirmasoumi, M. Antioxidative enzymes activities and accumulation of steroids in hairy roots of Trigonella. Physiol. Mol. Biol. Plants 2020, 26, 281–288. [Google Scholar] [CrossRef] [PubMed]
- Zhang, B.; Chen, L.; Huo, Y.; Feng, J.; Ma, Z.; Zhang, X.; Zhu, C. Enhanced production of celastrol in Tripterygium wilfordii hairy root culture by overexpression of TwSQS2. Biochem. Eng. J. 2020, 161, 107681. [Google Scholar] [CrossRef]
- Park, Y.J.; Thwe, A.A.; Li, X.; Kim, Y.J.; Kim, J.K.; Arasu, M.V.; Al-Dhabi, N.A.; Park, S.U. Triterpene and flavonoid biosynthesis and metabolic profiling of hairy roots, adventitious roots, and seedling roots of Astragalus membranaceus. J. Agric. Food Chem. 2015, 63, 8862–8869. [Google Scholar] [CrossRef]
- Mirjalili, M.H.; Moyano, E.; Bonfill, M.; Cusido, R.M.; Palazón, J. Overexpression of the Arabidopsis thaliana squalene synthase gene in Withania coagulans hairy root culture. Biol. Plant. 2011, 55, 357–360. [Google Scholar] [CrossRef]
- Dhar, N.; Razdan, S.; Rana, S.; Bhat, W.W.; Vishwarkarma, R.; Lattoo, S.K. A decade of molecular understanding of withanolide biosynthesis and in vitro studies in Withania somnifera (L.) Dunal: Prospects and perspectives for pathways engineering. Front. Plant. Sci. 2015, 6, 1031. [Google Scholar] [CrossRef] [Green Version]
- Sharam, A.; Rana, S.; Rather, G.A.; Misra, P.; Dhar, M.K.; Lattoo, S.K. Characterization and overexpression of sterol Δ22-saturase, a key enzyme modulates the biosyntheses of stigmasterol and withanolides in Withania somnifera (L.) Dunal. Plant Sci. 2020, 301, 110642. [Google Scholar] [CrossRef]
- Garagounis, C.; Beritza, K.; Georgopulou, M.E.; Sonawane, P.; Haralampidis, K.; Goosens, A.; Aharoni, A.; Papadopoulou, K.K. A hairy-root transformation protocol for Trigonella foenum-graecum L. as a tool for metabolic engineering and specialized metabolite pathway elucidation. Plant Physiol. Biochem. 2020, 154, 451–462. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.B.; Reed, D.W.; Covello, P.S. Production of triterpenoid sapogenins in hairy root cultures of Silene vulgaris. Nat. Prod. Com. 2015, 10, 1919–1922. [Google Scholar]
- Kamińska, M. Role and activity of jasmonates in plants under in vitro conditions. Plant Cell Tissue Org. Cult. 2021, 146, 425–447. [Google Scholar] [CrossRef]
- Su, L.; Li, S.; Qiu, H.; Wang, H.; Wang, C.; He, C.; Xu, M.; Zhang, Z. Full-length transcriptome analyses of genes involved in triterpenoid saponin biosynthesis of Psammosilene tunicoides hairy root cultures with exogenous salicylic acid. Front. Genet. 2021, 12, 657060. [Google Scholar] [CrossRef] [PubMed]
- Park, Y.J.; Kim, J.K.; Park, S.U. Yeast extract improved biosynthesis of astragalosides in hairy root cultures of Astragalus membranaceus. Prep. Biochem. Biotech. 2021, 51, 467–474. [Google Scholar] [CrossRef]
- Kochan, E.; Szymczyk, P.; Kuźma, Ł.; Szymańska, G.; Wajs-Bonikowska, A.; Bonikowski, R.; Sienkiewicz, M. The increase of triterpene saponin production induced by trans-anethole in hairy root culture of Panax quinquefolium. Molecules 2018, 23, 2674. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Srivastava, M.; Singh, G.; Sharma, S.; Shukla, S.; Misra, P. Elicitation enhanced the yield of glycyrrhizin and antioxidant activities in hairy root cultures of Glycyrrhiza glabra L. J. Plant Growth Reg. 2019, 38, 373–384. [Google Scholar] [CrossRef]
- Hajati, R.J.; Payamnoor, V.; Chashmi, N.A. Effect of biotic and abiotic elicitors on production of betulin and betulinic acid in the hairy root culture of Betula pendula Roth. Prep. Biochem. Biotechnol. 2019, 49, 1010–1019. [Google Scholar] [CrossRef] [PubMed]
- Baek, S.; Ho, T.T.; Lee, H.; Jung, G.; Kim, Y.E.; Jeong, C.S.; Park, S.Y. Enhanced biosynthesis of triterpenoids in Centiella asiatica hairy root culture by precursor feeding and elicitation. Plant Biotech. Rep. 2020, 14, 45–53. [Google Scholar] [CrossRef]
- Sharma, P.; Padh, H.; Shrivastava, N. Hairy root cultures: A suitable biological system for studying metabolic pathways in plants. Eng. Life Sci. 2013, 13, 62–75. [Google Scholar] [CrossRef]
- Da Silva Magedans, Y.V.; Philips, M.A. Production of plant bioactive triterpenoid saponins: From metabolites to genes and back. Phyt. Rev. 2020, 20, 461–482. [Google Scholar] [CrossRef]
Plant Species/ Experimental Model | Compounds (Triterpenoid Saponins/Sterols) | Strategy Applied to Enhance Saponin Productivity | Effect | Reference |
---|---|---|---|---|
Panax ginseng adventitious or hairy roots | ginsenosides (dammarane- and oleanane-type)/ campesterol, sitosterol, stigmasterol | antisense suppression of cycloartenol synthase | ginsenoside content increased by 50–100%, sterol content decreased by 50% in obtained antisense transgenic lines | [58] |
overexpression of squalene synthase | 1.6-3-fold increase of ginsenoside content, 2-fold increase of sterol content | [63] | ||
overexpression of mevalonate-5-pyro- phosphate decarboxylase and farnesyl pyrophosphate synthase | 2.4-fold and 4.6-fold increase of ginsenoside and sterol content, respectively, in lines overexpressing farnesyl pyrophosphate synthase; 4.4-fold increase of sterol content (ginsenoside content not changed) in lines overexpressing mevalonate-5-pyrophosphate decarboxylase | [64] | ||
Bupleurum falcatum adventitious roots | saikosaponins (oleanane-type)/ campesterol, sitosterol, stigmasterol | elicitation with methyl jasmonate, overexpression of squalene synthase, | elicitation increased saikosaponin content and decreased sterol content in wild-type roots; overexpression of squalene synthase in sense orientation enhanced the level of both saikosaponins and sterols | [59] |
Centella asiatica hairy roots | centellasaponins, asiaticosides, madecassosides/ campesterol, cholesterol, sitosterol, stigmasterol | overexpression of ginseng farnesyl diphosphate synthase, elicitation with methyl jasmonate | 3-fold increase of sterol content (saponin content not affected in transgenic roots, 1.15-fold increase obtained after elicitation with methyl jasmonate | [60] |
Platycodon grandifolium hairy roots | platycodins (oleanane-type)/ α-spinasterol | overexpression of ginseng 3-hydroxyl-3-methylglutaryl-coenzym A reductase. | up to 2.5-fold and 1.6-fold increase in saponin and sterol content, respectively | [65] |
Calendula officinalis hairy roots | calendula saponins (oleanane-type)/ cholesterol, campesterol, isofucosterol, sitosterol, stigmasterol | elicitation with jasmonic acid and 6-aminopurine | up to 113-fold increase in saponin release to the medium, 60% decrease in sterol content after elicitation with jasmonic acid; 10-fold increase in saponin release accompanied by 17% decrease in sterol content after elicitation with 6-aminopurine | [61,62] |
elicitation with chitosan | up to 3-fold increase in saponin release to medium, 18% increase in sterol content | [62] | ||
elicitation with auxins, cytokinins, abiotic elicitors (cadmium and silver ions, UV-irradiation, ultrasound) | up to 12-fold increase in saponin release to the medium, up to 17% increase in sterol content, often accompanied by alterations in sterol profile | [62,66] |
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Rogowska, A.; Szakiel, A. Enhancement of Phytosterol and Triterpenoid Production in Plant Hairy Root Cultures—Simultaneous Stimulation or Competition? Plants 2021, 10, 2028. https://doi.org/10.3390/plants10102028
Rogowska A, Szakiel A. Enhancement of Phytosterol and Triterpenoid Production in Plant Hairy Root Cultures—Simultaneous Stimulation or Competition? Plants. 2021; 10(10):2028. https://doi.org/10.3390/plants10102028
Chicago/Turabian StyleRogowska, Agata, and Anna Szakiel. 2021. "Enhancement of Phytosterol and Triterpenoid Production in Plant Hairy Root Cultures—Simultaneous Stimulation or Competition?" Plants 10, no. 10: 2028. https://doi.org/10.3390/plants10102028