Abstract
Tyrosine is the starting unit of a wide range of specialized metabolites in plants, including the pharmaceutically important benzylisoquinoline alkaloids (BIAs). Although in vitro cell suspension cultures from some BIA-producing species have been obtained, there are only a few documented cases for the establishment of hairy root cultures, even though this system has been intensively used in other alkaloid-producing plants. Hairy root cultures have been generated from three members of Papaver genus, including P. somniferum, P. orientale, and P. bracteatum. Morphine- and morphinan-type alkaloids have been identified in all of them, suggesting that the biosynthetic capacity is maintained in all cases. Sanguinarine and other benzophenanthridine-type alkaloids were also identified in these cultures, as well as in hairy roots from Eschscholzia californica (Papaveraceae). Only one report of berberine-producing hairy root was found in an extensive literature search, although attempts on probable transformation of recalcitrant species were detected. The use of Beta vulgaris hairy root cultures for the synthesis of betalains, pigments derived from tyrosine, was also included.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adeniyi CBA, Odumosu DO (2008) Phytochemical and in-vitro antimicrobial activity of Zanthoxylum zanthoxyloides (Rutaceae), Terminalia glauscens (Combretaceae) and Pseudocedrela kotschyii (Meliaceae), three Nigerian chewing sticks. Planta Med 74:1027–1027
Akita T, Hina Y, Nishi T (2000) Production of betacyanins by a cell suspension culture of table beet (Beta vulgaris L.) Biosci Biotechnol Biochem 64:1807–1812
Allen RS, Miller JAC, Chitty JA, Fist AJ, Gerlach WL, Larkin PJ (2007) Metabolic engineering of morphinan alkaloids by overexpression and RNAi suppression of salutaridinol 7-O-acetyltransferase in opium poppy. Plant Biotechnol J 6:22–30
Azeredo HMC (2009) Betalains: properties, sources, applications and stability - a review. Int J Food Sci Technol 44:2365–2376
Beaudoin GAW, Facchini PJ (2014) Benzylisoquinoline alkaloid biosynthesis in opium poppy. Planta 240:19–32
Brijwal L, Tamta S (2015) Agrobacterium rhizogenes mediated hairy root induction in endangered Berberis aristata DC. SpingerPlus 4:443. https://doi.org/10.1186/s40064-015-122-1
Cai Y, Sun M, Corke H (1998) Colourant properties and stability of Amaranthus betacyanin pigments. J Agric Food Chem 46:4491–4495
Castellanos-Santiago E, Yahia EM (2008) Identification and quantification of betalains from the fruits of 10 Mexican prickly pear cultivars by high-performance liquid chromatography and electrospray ionization mass spectrometry. J Agric Food Chem 56:5758–5764
Chang XX, Yan HM, Xu Q, Xia MF, Bian H, Zhu TF, Gao X (2012) The effects of berberine on hyperhomocysteinemia and hyperhomocysteinemia and hyperlipidemia in rats fed with a long-term high-fat diet. Lipids Health Dis 11:86
Chen WH, Chan CL, Cai Z, Luo GA, Jiang ZH (2004) Study on noncovalent complexes of cytotoxic protoberberine alkaloids with double-stranded DNA by using electrospray ionization mass spectrometry. Bioorg Med Chem Lett 14:4955–4959
Dvorak Z, Kuban V, Klejdus B, Hlavac J, Vicar J, Ulrichova J, Simanek V (2006) Quaternary benzo [c] phenanthridines sanguinarine and chelerythrine: a review of investigations from chemical and biological studies. Heterocycles 68:2403–2422
Etsè KD, Aïdam AV, Melin C, Blanc N, Oudin A, Courdavault V, Creche J et al (2014) Optimized genetic transformation of Zanthoxylum zanthoxyloides by Agrobacterium rhizogenes and the production of chelerythrine and skimmiamine in hairy root cultures. Eng Life Sci 14:95–99
Fischer N, Dreiding AS (1972) Biosynthesis of betalaines. In the cleavage of the aromatic ring during the enzymatic transformation of dopa into betalamic acid. Helv Chim Acta 55:649–658
Gandhi SG, Mahajan V, Bedi YS (2015) Changing trends in biotechnology of secondary metabolism in medicinal and aromatic plants. Planta 241:303–317
Gandía-Herrero F, García-Carmona F, Escribano J (2004) Purification and characterization of a latent polyphenol oxidase from beet root (Beta vulgaris L.) J Agric Food Chem 52:609–615
Gandía-Herrero F, Escribano J, García-Carmona F (2012) Purification and antiradical properties of the structural unit betalains. J Nat Prod 75:1030–1036
Gasztonyi MN, Dadood H, Hajos MT, Biacs P (2001) Comparison of red beet (Beta vulgaris var. cibutiva) varieties on the basis of their pigment components. J Sci Food Agric 81:923–933
Georgiev VG, Weber J, Kneschke EM, Denev PN, Bley T, Pavlov AI (2010) Antioxidant activity and phenolic content of betalain extracts from intact plants and hairy root cultures of the red beetroot Beta vulgaris cv. Detroit Dark Red. Plants Foods Hum Nutr 65:105–111
Georgiev MI, Eibl R, Zhong JJ (2013) Hosting the plant cells in vitro: recent trends in bioreactors. Appl Microbiol Biotechnol 97:3787–3800
Godoy-Hernández G, Avilés-Berzunza E, Carrillo-Pech M, Vázquez-Flota F (2008) Agrobacterium-mediated transient transformation of Mexican prickly poppy (Argemone mexicana L.) Electron J Biotechnol 11:1–5
Grycová L, Dostál J, Marek R (2007) Quaternary protoberberine alkaloids. Phytochemistry 68:150–175
Guillon S, Trémouillaux-Guiller J, Pati PK, Rideau M, Gantet P (2006) Harnessing the potential of hairy roots: dawn of a new era. Trends Biotechnol 24:403–409
Guillon S, Gantet P, Thiersault M, Rideau M, Trémouillaux-Guiller J (2008) Hairy roots of Catharanthus roseus: efficient routes to monomeric indole alkaloid production. In: Ramawat KG, Mérillon JM (eds) Bioactive molecules and medicinal plants. Springer, Heidelberg
Hagel JM, Facchini PJ (2013) Benzyl isoquinoline alkaloid metabolism: a century of discovery and brave new world. Plant Cell Physiol 54:647–672
Häkkinen ST, Moyano E, Cusidó RM, Palazón J, Piñol MT, Oksman-Caldentey KM (2005) Enhanced secretion of tropane alkaloids in Nicotiana tabacum hairy roots expressing heterologous hyoscyamine-6-hydroxylase. J Exp Bot 56:2611–2618
Hamill JD, Parr AJ, Robins RJ, Rhodes MJC (1986) Secondary product formation by cultures of Beta vulgaris and Nicotiana rustica transformed with Agrobacterium rhizogenes. Plant Cell Rep 5:111–114
Hashemi SM, Naghavi MR (2016) Production and gene expression of morphinan alkaloids in hairy root culture of Papaver orientale L. using abiotic elicitors. Plant Cell Tiss Org 125:31–41
He M, Jiang L, Ren Z, Wang G, Wang J (2016) Noscapine targets EGFRp-Tyr1068 to suppress the proliferation and invasion of MG63 cells. Sci Rep 6:37062
Kala CP (2002) Indigenous knowledge of Bhotiya tribal community on wool dyeing and its present status in the Garhwal Himalaya, India. Curr Sci 83:814–817
Kassem MA, Jacquin A (2001) Somatic embryogenesis, rhizogenesis, and morphinan alkaloids production in two species of opium poppy. J Biomed Biotechnol 1(2):70–78
Lan X, Chang K, Zeng L, Liu X, Qiu F, Zheng W, Quan H et al (2013) Engineering salidroside biosynthetic pathway in hairy root cultures of Rhodiola crenulata based on metabolic characterization of tyrosine decarboxylase. PLoS One 8:e75459
Lan J, Zhao Y, Dong F, Yan Z, Zheng W, Fan J, Sun G (2015) Meta-analysis of the effect and safety of berberine in the treatment of type 2 diabetes mellitus, hyperlipemia and hypertension. J Ethnopharmacol 161:69–81
Larkin PJ, Miller JAC, Allen RS, Chitty JA, Gerlach WL, Frick S, Kutchan TM et al (2007) Increasing morphinan alkaloid production by over-expressing codeinone reductase in transgenic Papaver somniferum. Plant Biotechnol J 5:26–37
Laurain-Matter D, Gillet-Manceau F, Buchon L, Nabha S, Fliniaux MA, Jacquin-Dubreuil A (1999) Somatic embryogenesis and rhizogenesis of tissue cultures of two genotypes of Papaver somniferum: relationships to alkaloid production. Planta Med 65:167–170
Le Flem-Bonhomme V, Laurain-Mattar D, Fliniaux MA (2004) Hairy root induction of Papaver somniferum var. album, a difficult-to-transform plant, by A. rhizogenes LBA 9402. Planta 218:890–893
Leathers RR, Davin C, Zryd JP (1992) Betalain producing cell cultures of Beta vulgaris L. var. Bikores monogerm (red beet). In Vitro Cell Dev Biol 28:39–45
Liscombe DK, MacLeod BP, Lokanina N, Nandi OI, Facchini PJ (2005) Evidence for the monophyletic evolution of benzylisoquinoline alkaloid biosynthesis in angiosperms. Phytochemistry 66:1374–1393
Liu JK, Couldwell WT (2005) Intra-arterial papaverine infusions for the treatment of cerebral vasospasm induced by aneurysmal subarachnoid hemorrhage. Neurocrit Care 2:124–132
Loyola-Vargas VM, Miranda-Ham ML (1995) Root culture as a source of secondary metabolites of economic importance. In: Arnason JT, Mata R, Romeo JT (eds) Advances in phytochemistry: phytochemistry of medicinal plants. Plenum, New York
Lu X, Wang Y, Zhang Z (2009) Radioprotective activity of betalains from red beets in mice exposed to gamma radiation. Eur J Pharmacol 615:223–227
MacLeod BP, Facchini PJ (2006) Methods for regeneration and transformation in Eschscholzia californica. In: Loyola-Vargas VM, Vázquez-Flota F (eds) Methods in molecular biology, Plant cell culture protocols, vol 318, 2nd edn. Humana, Totowa
Magnotta M, Murata J, Chen J, De Luca V (2007) Expression of deacetylvindoline-4-O-acetyltransferase in Catharanthus roseus hairy roots. Phytochemistry 68:1922–1931
Moyano E, Fornalé S, Palazón J, Cusidó RM, Bagni N, Piñol MT (2002) Alkaloid production in Duboisia hybrid hairy root cultures overexpressing the pmt gene. Phytochemistry 59:689–670
Mundokan U, Bhide V, Singh G, Curtis WR (1998) pH mediated release of betalains from transformed root cultures of Beta vulgaris. Appl Microbiol Biotechnol 50:241–245
Nessler CL (1990) Poppy. In: Ammirato PV, Evans DA, Sharp WR, Bajaj YPS (eds) Handbook of plant cell culture. McGraw-Hill, New York
Oni O (1993) Conservation and vegetative propagation of the genetic resources of some endangered medicinal woody plants of Nigeria. Acta Hortic 331:269–274
Pandey SS, Singh S, Babu CSV, Shanker K, Srivastava NK, Kalra A (2016) Endophytes of opium poppy differentially modulate host plant productivity and genes for the biosynthetic pathway of benzylisoquinoline alkaloids. Planta 160:1–8
Park SU, Facchini PJ (2000a) Agrobacterium rhizogenes-mediated transformation of opium poppy, Papaver somniferum L., and California poppy, Eschscholzia californica Cham., root cultures. J Exp Bot 51:1005–1016
Park SU, Facchini PJ (2000b) Agrobacterium-mediated genetic transformation of California poppy, Eschscholzia californica Cham., via somatic embryogenesis. Plant Cell Rep 19:1006–1012
Patel M, Dewey RE, Qu R (2013) Enhancing Agrobacterium tumefaciens-mediated transformation efficiency of perennial ryegrass and rice using heat and high maltose treatments during bacterial infection. Plant Cell Tiss Org 114:19–29
Pavlov A, Bley T (2006) Betalains biosynthesis by Beta vulgaris L. hairy root culture in a temporary immersion cultivation system. Process Biochem 41:848–852
Pavlov A, Kovatcheva P, Georgiev V, Koleva I, Ilieva M (2002) Biosynthesis and radical scavenging activity of betalains during the cultivation of red beet (Beta vulgaris) hairy root cultures. Z Naturforsch 57c:640–644
Pavlov A, Georgiev V, Kovatcheva P (2003) Relationship between type and age of the inoculum cultures and betalains biosynthesis by Beta vulgaris hairy root cultures. Biotechnol Lett 25:307–309
Pavlov A, Georgiev M, Bley T (2007) Batch and fed-batch production of betalains by red beet (Beta vulgaris) hairy roots in a bubble column reactor. Z Naturforsch 62c:439–446
Ramakrishnan D, Curtis WR (2004) Trickle-bed root culture bioreactor design and scale-up: growth, fluid-dynamics and oxygen mass transfer. Biotechnol Bioeng 88:248–260
Rizvi NF, Weaver JD, Cram EJ, Lee-Parsons CWT (2016) Silencing the transcriptional repressor, ZCT1, illustrates the tight regulation of terpenoid indole alkaloid biosynthesis in Catharanthus roseus hairy roots. PLoS One 11:e0159712
Robbins RC, Artuso-Ponte VC, Moeser AJ, Morrow WEM, Spears JW, Gebreyes WA (2013) Effects of quaternary benzo(c)phenanthridine alkaloids on growth performance, shedding of organisms, and gastrointestinal tract integrity in pigs inoculated with multidrug-resistant Salmonella spp. Am J Vet Res 74:1530–1535
Roberts MF, Wink M (1998) Introduction. In: Robert MF, Wink M (eds) Alkaloid. Biochemistry, ecology, and medicinal applications. Plenum, New York, pp 1–7
Roberts MF, Strack D, Wink M (2010) Biosynthesis of alkaloids and betalains. In: Wink M (ed) Biochemistry of plant secondary metabolism, Annual plant review, vol 40, 2nd edn. Wiley, Oxford, pp 20–91
Rostampour S, Hashemi S, Jourabchi E, Ansari E (2009) Influence of Agrobacterium rhizogenes on induction of hairy roots and benzylisoquinoline alkaloids production in Persian poppy (Papaver bracteatum Lindl.): preliminary report. World J Microb Biot 25:1807–1814
Rubio-Piña J, Vázquez-Flota F (2013) Pharmaceutical applications of the benzylisoquinoline alkaloids from Argemone mexicana L. Curr Top Med Chem 13:2200–2207
Schaefer HM, Schaefer V, Levey DJ (2004) How plant-animal interactions signal new insights in communication. Trends Ecol Evol 19:577–584
Schmeller T, Wink M (1998) Utilization of alkaloids in modern medicine. In: Robert MF, Wink M (eds) Alkaloid. Biochemistry, ecology and medicinal applications. Plenum, New York
Seddigh M, Jolliff GD, Calhoun W, Crane JM (1982) Papaver bracteatum, potential commercial source of codeine. Econ Bot 36:433–441
Sevón N, Oksman-Caldentey KM (2002) Agrobacterium rhizogenes-mediated transformation: root cultures as a source of alkaloids. Planta Med 68:859–868
Shad V, Deepa MA (2015) Elicitation, bioconversion and quantification of berberine from Cissampelos pareira callus cultures. Int J Pharm Sci Res 6:2636–2640
Shad V, Deepa MA (2016) In vitro studies and Agrobacterium rhizogenes mediated transformation of Cissampelos pareira - a highly recalcitrant species. Int J Pharm Bio Sci 7:312–317
Sharafi A, Sohi HH, Mousavi A, Azadi P, Razavi K, Ntui VO (2013a) A reliable and efficient protocol for inducing hairy roots in Papaver bracteatum. Plant Cell Tiss Org 113:1–9
Sharafi A, Sohi HH, Mousavi A, Azadi P, Dehsara B, Khalifani BH (2013b) Enhanced morphinan alkaloid production in hairy root cultures of Papaver bracteatum by over-expression of salutaridinol 7-O-acetyltransferase gene via Agrobacterium rhizogenes mediated transformation. World J Microbiol Biotechnol 29:2125–2131
Sharma P, Padh H, Shrivastava N (2013) Hairy root cultures: a suitable biological system for studying secondary metabolic pathways in plants. Eng Life Sci 13:62–75
Sreekanth D, Arunasree MK, Roy KR, Reddy TC, Reddy GV, Reddanna P (2007) Betanin a betacyanin pigment purified from fruits of Opuntia ficus-indica induces apoptosis in human chronic myeloid leukemia cell line-K562. Phytomedicine 4:739–746
Steiner U, Schliemann W, Böhm H, Strack D (1999) Tyrosinase involved in betalain biosynthesis of higher plants. Planta 208:114–124
Stintzing FC, Carle R (2007) Betalains – emerging prospects for food scientists. Trends Food Sci Technol 18:514–525
Stintzing FC, Schieber A, Carle R (2002) Betacyanins in fruits from red-purple pitaya, Hylocereus polyrhizus (Weber) Britton & Rose. Food Chem 77:101–106
Strack D, Vogt T, Schliemann W (2003) Recent advances in betalain research. Phytochemistry 62:247–269
Taya M, Yakura K, Kino-Oka M, Tone S (1994) Influence of medium constituents on enhancement of pigment production by batch culture of red beet hairy roots. J Ferment Bioeng 77:215–217
Vaillant F, Pérez A, Dávila I, Dornier M, Reynes M (2005) Colorant and antioxidant properties of red-purple pitahaya (Hylocereus sp.) Fruits 60:1–10
Verma R, Juvekar AR, Gopalkrishan R, Eapen S (2006) Protoberberine alkaloids from the hairy root cultures of Tinospora cordifolia transformed with Agrobacterium rhizogenes. Planta Med 72:S-018
Wang BH, Lu ZX, Polya GM (1997) Inhibition of eukaryote protein kinases by isoquinoline and oxazine alkaloids. Planta Med 63:494–498
Wang CQ, Song H, Gong XZ, Hu QG, Liu F, Wang BS (2007) Correlation of tyrosinase activity and betacyanin biosynthesis induced by dark in C3 halophyte Suaeda salsa seedlings. Plant Sci 173:487–494
Wink M (1998a) A short history of alkaloids. In: Robert MF, Wink M (eds) Alkaloid. Biochemistry, ecology and medicinal applications. Plenum, New York
Wink M (1998b) Modes of action of alkaloids. In: Robert MF, Wink M (eds) Alkaloid. Biochemistry, ecology and medicinal applications. Plenum, New York
Xool-Tamayo J, Serrano-Gamboa G, Monforte-González M, Mirón-López G, Vázquez-Flota F (2017) Development of newly sanguinarine biosynthetic capacity in in vitro rootless shoots of Argemone mexicana L. Mexican prickly poppy. Biotechnol Lett 39:323–330
Yin J, Xing H, Ye J (2008) Efficacy of berberine in patients with type 2 diabetes mellitus. Metabolism 57:712–717
Yoshimatsu K, Shimomura K (1992) Transformation of opium poppy (Papaver somniferum L.) with Agrobacterium rhizogenes MAFF 03-01724. Plant Cell Rep 11:132–136
Zdarilová A, Vrzal R, Rypka M, Ulrichová J, Dvorák Z (2006) Investigation of sanguinarine and chelerythrine effects on CYP1A1 expression and activity in human hepatoma cells. Food Chem Toxicol 44:242–249
Zhang L, Ding R, Chai Y, Bonfill M, Moyano E, Oksma-Caldentey KM, Xu T et al (2004) Engineering tropane biosynthetic pathway in Hyoscyamus niger hairy root cultures. Proc Natl Acad Sci 101:6786–6791
Zhao L, Sander GW, Shanks JV (2013) Perspectives of the metabolic engineering of terpenoid indole alkaloids in Catharanthus roseus hairy roots. Adv Biochem Eng Biotechnol 134:23–54
Zhou L, Yang Y, Wang X, Liu S, Shang W, Yuan G, Li F, Tang J, Chen M, Chen J (2007) Berberine stimulates glucose transport through a mechanism distinct from insulin. Metabolism 56:405–412
Acknowledgments
Y T-O received a scholarship from Sistema Nacional de Investigadores (Mexico) as assistant of researcher (FV-F).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Vázquez-Flota, F., de Lourdes Miranda-Ham, M., Castro-Concha, L., Tamayo-Ordoñez, Y. (2017). Synthesis of Benzylisoquinoline Alkaloids and Other Tyrosine-Derived Metabolites in Hairy Root Cultures. In: Malik, S. (eds) Production of Plant Derived Natural Compounds through Hairy Root Culture . Springer, Cham. https://doi.org/10.1007/978-3-319-69769-7_9
Download citation
DOI: https://doi.org/10.1007/978-3-319-69769-7_9
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-69768-0
Online ISBN: 978-3-319-69769-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)