Abstract
A fantastic source of natural products encompassing the vast group of the terpenes, alkaloids, and phenolic compounds is provided by the plants. About 25,000 of these secondary metabolites hold a strong potential in a large domain of industrial and pharmaceutical applications. Plant families, such as Lamiaceae, Asteraceae, and Taxaceae, synthesize several terpenoid classes with a great economic value. Hairy roots, resulting from Agrobacterium rhizogenes–mediated transformation of plant cells, can be harnessed for terpenoid production on a large scale. A. rhizogenes over other transformation systems makes possible an easy regeneration of transgenic plants. Based on the deletion of rol genes located on the wild-type Ri-T-DNA, disarmed versions are created in order to overcome abnormalities of Ri-plants. Terpenoid accumulation from hairy roots can be optimized by elicitation treatment with jasmonates. Ri-T-DNA activation tagging system and transcriptome analyses are powerful tools to isolate new function genes involved in the terpenoid biosynthesis. Such genes encoding enzymes involved in the secondary metabolism can be inserted between the T-DNA borders. Lastly, some pharmacological properties of these plant terpenes/terpenoids involved in the therapy of more or less severe pathologies are reported.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- 2, 4-D:
-
2, 4-Dichlorophenoxyacetic acid
- Ac-MVA:
-
Acetate mevalonate pathway
- BABA:
-
β-aminobutyric acid
- BAP:
-
6-Benzylaminopurine
- CPPU:
-
4-N-(2-chloro-4 pyridyl) –N′-phenylurea
- DMAPP:
-
Dimethylallyl pyrophosphate
- DXP:
-
Deoxyxylulose 5-phosphate
- DXS:
-
1-Deoxy-d-xylulose 5-phosphate synthase
- HMGR:
-
3-Hydroxy-3-methylglutaryl CoA reductase
- IAA:
-
Indole 3 acetic acid
- IPP:
-
Isopentenyl pyrophosphate
- Kin:
-
Kinetin
- MeJA:
-
Methyl jasmonate
- MEP:
-
2-C-methyl-d-erythritol 4-phosphate pathway
References
Poulev A, O’Neal JM, Logendra S, Pouleva RB, Timeva V, Garvey AS, Gleba D, Jenkins IS, Halpern BT, Kneer R, Cragg GM, Raskin I (2003) Elicitation a new window into plant chemodiversity and phytochemical drug discovery. J Med Chem 46:2542–2547
Chaudhuri KN et al (2009) Transgenic mimicry of pathogen attach stimulates growth and secondary metabolite accumulation. Transgenic Res 18:121–128
Tholl D, Lee S (2011) Terpene-specialized metabolism in Arabidopsis thaliana. Am Soc Plant Biol. doi:10.1199/tab.0143
Zwenger S, Basu C (2008) Plant terpenoids: applications and future potentials. Biotechnol Mol Biol Rev 3(1):1–7
Bensaddek L, Villarreal ML, Fliniaux MA (2008) Induction and growth of hairy roots for the production of medicinal compounds. J Integr Biosci 3(1):2–9
Croteau R, Kutchan TM, Lewis NG (2000) Natural products (secondary metabolites). In: Buchanan B, Gruissem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 1250–1318
Bohlmann J, Keeling CI (2008) Terpenoid biomaterials. Plant J 54:656–669
Aharoni A, Jongsma MA, Kim T-Y, Ri M-B, Giri AP, Verstappen FWA, Schwab W, Bouwmeester HJ (2006) Metabolic engineering of terpenoid biosynthesis in plants. Phytochem Rev. doi:10.1007/s11101-005-3747-3
Dubey VS, Bhalla R, Luthra R (2003) An overview of the non-mevalonate pathway for terpenoid biosynthesis in plants. J Biosci 28(5):637–646
Ruiz-May E, Galaz-Avalos R, Loyola-Vargas V (2009) Differential secretion and accumulation of terpene indole alkaloids in hairy roots of Catharanthus roseus treated with methyl jasmonate. Mol Biotechnol 41:278–285
Morgan JA, Shanks JV (1999) Inhibitor studies of tabersonine metabolism in C. roseus hairy roots. Phytochemistry 51:61–68
Sevon N, Oksman-Caldentey KM (2002) Agrobacterium rhizogenes-mediated transformation: root cultures as a source of alkaloids. Planta Med 68:859–868
Sudha CG, Reddy BO, Ravishankar GA, Seeni S (2003) Production of ajmalicine and ajmaline in hairy root cultures of Rauvolfia micrantha Hook F., a rare and endemic medicinal plant. Biotechnol Lett 25:631–636
Lorence A, Medina-Bolivar F, Nessler CL (2004) Camptothecin and 10- hydroxycamptothecin from Camptotheca acuminata hairy roots. Plant Cell Rep 22:437–441
Caspeta L, Nieto I, Zamilpa A, Alvarez L, Quintero R, Villarreal ML (2005) Solanum chrysotrichum hairy root cultures: characterization, scale-up and production of five antifungal saponins for human use. Planta Med 71:1084–1087
Ahn JC, Hwang B, Hiromi T, Kanji I, Kazuo S, Koichiro S (1996) Polyacetylenes in hairy roots of Platycodon grandiflorum. Phytochemistry 42:69–72
Medina-Bolivar F, Condori JRA, Hubstenberger J, Shelton K, O’Keefe SF, Mc Dolan BS (2007) Production and secretion of resveratrol in hairy root cultures of peanut. Phytochemistry 68:1992–2003
Guillon S, Trémouillaux-Guiller J, Pati PK, Rideau M, Gantet P (2006) Hairy root research: recent scenario and exciting prospects. Curr Opin Plant Biol 9:341–346
Zhou X, Wang Y, Liu B, Xu H (2007) Salidroside production of hairy roots of Rhodiola sachalinensis obtained after transformation with Agrobacterium rhizogenes. Biol Pharm Bull 30:439–442
Peebles CAM, Shanks JV, San K-Y (2009) The role of the octadecanoid pathway in the production of terpenoid indole alkaloids in Catharanthus roseus hairy roots under normal and UV-B stress conditions. Biotechnol Bioeng 103(6):1248–1253
Tikhomiroff C, Jolicoeur M (2002) Screening of Catharanthus roseus secondary metabolites by high performance liquid chromatography. J Chromatogr A 955(1):87–93
Guillon S, Trémouillaux-Guiller J, Pati PK, Gantet P (2008) Hairy roots: a powerful tool for plant biotechnological advances. In: Ramawat KG, Mérillon JM (eds) Bioactive molecules and medicinal plants. Springer, Berlin, p 19
Srivastava S, Srivastava AK (2007) Hairy root culture for mass-production of high-value secondary metabolites. Crit Rev Biotechnol 27:29–43
Davioud E, Petit A, Tate ME, Ryder MH, Tempé J (1988) Cucumopine – a new T-DNA-Encoded opine in hairy root crown gall. Phytochemistry 27:2429–243
Trémouillaux-Guiller J, Andreu F, Créche J, Chénieux JC, Rideau M (1987) Variability in tissue cultures of Choisya ternata. Alkaloid accumulation in protoclones and aggregate clones obtained from established strains. Plant Cell Rep 6:375–378
Trémouillaux-Guiller J, Kodja H, Andreu F, Créche J, Chénieux JC, Rideau M (1988) Variability in tissue cultures of Choisya ternata, III Comparing Alkaloid production in cell lines obtained by various strategies. Plant Cell Rep 7:456–458
Canto-Canche B, Loyola-Vargas VM (1999) Chemicals from roots, hairy roots, and their applications. Adv Exp Med Biol 464:235–275
Tripathi L, Tripathi JN (2003) Role of biotechnology in medicinal plants. Trop J Res 2(2):243–253
Khan MY, Saleh A, Kumar V, Rajkumar S (2009) Recent advances in medicinal plant biotechnology. Indian J Biotechnol 8:9–22
Mc Contey ME, Gershenzon J, Croteau RB (2000) Developmental regulation of monoterpenes biosynthesis in glandular trichomes of peppermint. Plant Physiol 122(1):215–223
Martin DM, Toub O, Chiang A, Lo BC, Ohse S, Lund ST, Bohlmann J (2009) The bouquet of grapevine (Vitis vinifera L cv Cabernet Sauvignon) flowers arises from the biosynthesis of sesquiterpene volatiles in pollen grains. Proc Natl Acad Sci USA 106(17):7245–7250
Lücker J, Bowen P, Bohlmann J (2004) Vitis vinifera terpenoid cyclases: functional identification of two sesquiterpene synthase cDNAs encoding (+) -valencene synthase and (−) germacrene D synthase and expression of mono- and sesquiterpene synthases in grapevine flowers and berries. Phytochem 6:2649–2659
Aguiyi JC, Obi CI, Gang SS, Igweh AC (2000) Hypoglycaemic activity of Ocimum gratissimum in rats. Fitoterapia 71(4):444–446
Chaumont JP (2000) Antifungal properties of Ocimum gratissimum essential oils (ethyl cinnamate chemotype). Fitoterapia 71:567–569
Aïdam A, Etse KD, Koba K, Raynaud C, Sanda K, Chaumont JP, Trémouillaux-Guiller J (2008) Capacités morphogénétiques in vitro, performance au champ et production d’huiles essentielles chez Ocimum gratissimum L. Acta Bot Gallica 155:341–354
Lee S-J, Umano K, Shibamoto T, Lee K-G (2005) Identification of volatile components in basil (Ocimum basilicum L.) and thyme leaves (Thymus vulgaris L.) and their antioxidant properties. Food Chem 91:131–137
Koul O, Walia S, Dhaliwal GS (2008) Essential oils as green pesticides: potential and constraints. Biopestic Int 4(1):63–84
Celep F, Kahraman A, Dogan M (2011) A new taxon of the genus Salvia (Lamiaceae) from Turkey. Plant Ecol Evol 144(1):111–114
Fraga BM, Diaz CE, Guadano A, Gonzales-Coloma A (2005) Diterpenes from Salvia broussonetti transformed roots and their insecticidal activity. J Agric Food Chem 53:5200–5206
Kuzma L, Skrzypek Z, Wysokinska H (2006) Diterpenoids and triterpenoids in hairy roots of Salvia sclarea. Plant Cell Tiss Org Cult 8:171–179
Wu SJ, Shi M, Wu JY (2009) Cloning and characterization of the 1-deoxy-d-xylulose 5-phosphate reductoisomerase gene for diterpenoid tanshinone biosynthesis in Salvia miltiorrhiza (Chinese sage) hairy roots. Biotechnol Appl Biochem 52:89–95
Zang Z, Li S, Lian X-Y (2010) An overview of Genus Aesculus L: ethnobotany, phytochemistry, and pharmacological activities. Pharm Crops 1:24–51
Calic-Dragosavac D, Stevovic S, Zdravkovic-Korac S, Milojevic J, Cingel A, Vinterhalter B (2011) Secondary metabolite of horse chestnut in vitro culture. Adv Environ Biol 5(2):267–270
Choi DW, Chung H-J, Ko SM, In DS, Song JS, Woo S-S, Liu JR (2009) Mass production and application tagged hairy root lines for functional genomic of secondary metabolism in ginseng. J Plant Biotechnol 36:294–300
Ernst E (2010) Panax ginseng: an overview of the clinical evidence. J Ginseng Res 34(4):259–263. doi:10.5142/jgr.2010.34.4.259
de Sousa Braz A, Diniz M, de FF M, De Almeida RN (2009) Recent advances in the use of Panax ginseng as an analgesic: a systematic review. Boletin Latinoamericano y del Caribe de Plantas Medicinales y Aromaticas 8(3):188–194
Wang H, Peng D, Xie J (2009) Ginseng leaf-stem: bioactive constituents and pharmacological functions. Chin Med 4:20–28. doi:10.1186/1749-8546-4-20
Pu Z, Zhang P et al (2011) The evaluation of contents of nine ginsenoside monomers in ginseng hairy roots by high performance liquid chromatography (HPLC). J Med Plant Res 5(23):5513–5516
Yue PYK, Mak NK, Cheng YK, Leung KW, Ng TB, Fan DTP, Yeung HW, Wong RNS (2007) Pharmacogenomics and the yin/yang actions of ginseng: anti-tumor, angiomodulating and steroid-like activities of ginsenosides. Chin Med 2:6. doi:10.1186/1749-8546-2-6
Norberg A, Hoa NK, Liepinsh E, Phan DV, Thuan ND, Jörnvall H, Sillard R, Ostenson C-G (2004) A novel insulin-releasing substance, phanoside, from the Gynostemma pentaphyllum. J Biol Chem 279:401361–401367
Chang CK, Chang KS, Lin YC, Liu SY, Chen CY (2005) Hairy root cultures of Gynostemma pentaphyllum Thunb Makino a promising approach for the production of gypenosides as an alternative of ginseng saponins. Biotechnol Lett 27:1165–1169
Pellicer J, Garnatje T, Vallès J (2011) Artemisia (Asteraceae): understanding its evolution using cytogenetic and molecular systematic tools, with emphasis on subgenus Dracunculus. In: Munoz-Torrero D (ed) Recent advances in pharmaceutical sciences. Transworld Research Network, Trivandrum, pp 199–222: ISBN: 978-81-7895-528-5
Hayat HQ, Ashraf M, Khan MA, Mahmood T, Ahmad M, Jabeen S (2009) Phylogeny of Artemisia L: recent developments. Afr J Biotechnol 8(11):2423–2428
Olofsson L, Engström A, Lundgren A, Brodelius PE (2011) Relative expression of genes of terpene metabolism in different tissues of Artemisia annua L. BMC Plant Biol 11:45–57. doi:1186/147-2229-11-45
Wani MC, Taylor HL, Wall ME, Coggon P, McPhail AT (1971) Plant antitumor agents VI the isolation and structure of taxol a novel antileukemic and antitumor agent from Taxus brevifolia. J Am Chem Soc 93(9):2325–2327
Heinig U, Jennewein S (2009) Taxol: a complex diterpenoid natural product with an evolutionarily obscure origin. Afr J Biotechnol 8(8):1370–1385
Kim JA, Baek K-H, Son YM, Son SH, Shin H (2009) Hairy root cultures of Taxus cuspidate for enhanced production of paclitaxel. J Korean Soc Appl Biol Chem 52(2):144–150
Exposito O, Syklowska-Baranek K, Moyano E, Onrubia M, Bonfill M, Palazon J, Cusido RM (2010) Metabolic responses of Taxus media transformed cell cultures to the addition of methyl jasmonate. Biotechnol Prog 26(4):1145–1153
Lavelle F, Guéritte-Voegelein F, Guénard D (1993) Le taxotère: des aiguilles d’if à la clinique. Bull de cancérologie 80:326–338
Riker AJ, Banfield WM, Wright WH, Keitt WH, Sagen HE (1930) J Agr Res 41:507–540
Willmitzer L, Sanchez-Serrano J, Buschfeld E, Schell J (1982) DNA from Agrobacterium rhizogenes is transferred to and expressed in axenic hairy root plant tissues. Mol Gen Genet 186:16–22
Chilton M-D, Tepfer DA, Petit A, David C, Casse-Delbart F, Tempe J (1982) Agrobacterium rhizogenes inserts T-DNA into the genomes of the host plant root cells. Nature 295:432–434
Bercetche J, Chriqui D, Adam S, David C (1987) Morphogenetic and cellular reorientations induced by Agrobacterium rhizogenes (strains 1855, 2659 and 8196) on carrot, pea and tobacco. Plant Sci 52:195–210
White FF, Nester EW (1980) Hairy root: plasmids encode virulence traits in Agrobacterium rhizogenes. J Bacteriol 141:1134–1141
Tepfer D, Metzger L, Prost R (1989) Use of roots transformed by Agrobacterium rhizogenes in rhizosphere research: applications in studies of cadmium assimilation from sewage sludges. Plant Mol Biol 13:295–302
Veena V, Taylor C (2007) Agrobacterium rhizogenes recent developments and promising applications. In vitro Cell Dev Biol-Plant 43:383–403
Camilleri C, Jouanin L (1991) TR-DNA region carrying the auxin synthesis gene of the Agrobacterium rhizogenes agropine type plasmid PRiAA4: nucleotide sequence analysis and introduction into tobacco plants. Mol Plant Microbe Interact 4:155–162
Slightom JL, Durand-Tardif M, Jouanin L, Tepfer D (1986) Nucleotide sequence analysis of TL-DNA of Agrobacterium rhizogenes agropine type plasmid: identification of open-reading frames. J Biol Chem 261:108–121
Goldmann A, Tempé J, Morel G (1968) Découvertes de nouvelles substances, les opines produites par les cellules des tumeurs. Quelques particularités de diverses souches d’Agrobacterium tumefaciens. CR Sci Biol 162:630–631
Petit A, Delhaye S, Tempé J, Morel G (1970) Recherches sur les guanidines des tissues de crown gall. Mise en évidence d’une relation biochimique spécifique entre les souches d’Agrobacterium tumefaciens et les tumeurs qu’elles induisent. Physiol Vég 8:205
Tepfer D, Tempé J (1981) Production d’agropine par de racines formées sous l’action d’Agrobacterium rhizogenes, souche A4. CR Acad Sci Paris 292:153–156
De Paolis A, Mauro HL, Pomponi M, Cardarelli M, Spano L, Constantino P (1985) Localization of agropine-synthesizing functions in the TR regions of the root inducing plasmid of Agrobacterium rhizogenes 1865. Plasmid 13:1–7
Ayadi R, Tremouillaux-Guiller J (2003) Root formation from transgenic calli of Ginkgo biloba. Tree Physiol 23:437–441
Davioud E, Petit A, Tate ME, Ryder MH, Tempé J (1988) Cucumopine – a new T-DNA- encoded opine in hairy root crown gall. Phytochemistry 27:2429–2433
Tzfira T, Vaidya M, Citovsky V (2004) Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium. Nature 431:92
Tzfira T, Li J, Lacroix B, Citovsky V (2004) Agrobacterium T-DNA integration: molecules and models. Trends Genet 20:375–383
Lacroix B, Vaidya M, Tzfira T, Citovsky V (2005) The VirE3 protein of Agrobacterium mimics a host cell function required for plant genetic transformation. EMBO J 24:428–437
Gelvin SB (2009) Agrobacterium in the genomics age. Plant Physiol 150:1665–1668
Pitzschke A, Heribert H (2010) New insights into an old story: Agrobacterium-induced tumor formation in plants by plant transformation. EMBO J 29:1021–1028
Pawar PK, Maheshwari VL (2004) Agrobacterium rhizogenes mediated hairy root induction in two medicinally important members of family Solanaceae. India J Biotechnol 3:414–417
Wysokinska H, Chmiel A (1997) Transformed root cultures for biotechnology. Acta Biotechnol 17:131–159
David C, Chilton MD, Tempé J (1984) Conservation of T-DNA in plants regenerated from hairy root cultures. Biotechnology 2:73–76
Tepfer D (1984) Transformation of several species of higher plants by Agrobacterium rhizogenes: sexual transmission of the transformed genotype and phenotype. Cell 37:959
Phelep M, Petit A, Martin L, Duhoux E, Tempé J (1991) Transformation and regeneration of a nitrogen-fixing tree, Allocasuarina Verticillata Lam. Nat Biotechnol 9:461–466
Flores HE, Vivanco JM, Loyola-Vargas VM (1999) ‘Radicle’ biochemistry: the biology of root-specific metabolism. Trends Plant Sci 4:220–226
Huang T-K, Mc Donald KA (2011) Bioreactor systems for in vitro production of foreign proteins using plant cell cultures. Biotechnol Adv 30(2):398–409
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, Berlin, pp 271–283
Rigano MM, Walmsley AM (2005) Expression systems and developments in plant-made vaccines. Immunol Cell Biol 83:271–277
Subroto MA, Artanti N, Sudrajat D, Djanakum A, Widayat E (2001) Agrobacterium rhizogenes-mediated transformation of Solanum nigrum L: spontaneous plant regeneration and endogenous IAA contents. Indon J Agricult Sci 1:53–59
Christensen B, Sriskandarajah S, Serek M, Müller R (2008) Transformation of Kalanchoe blossfeldiana with rol-genes is useful in molecular breeding towards compact growth. Plant Cell Rep 27:1485–1495. doi:1007/s00299-008-0575-0
Mishiba KI, Masahiro N, Yoshiko A, Takashi N, Hiromi K, Katsuo K, Toshikazu T, Jun A, Saburo Y (2006) Production of dwarf potted gentian using wild-type Agrobacterium rhizogenes. Plant Biotechnol 23:33–38
Crane C, Wright E, Dixon RA, Wang ZY (2006) Transgenic Medicago truncatula plants obtained from Agrobacterium tumefaciens-transformed roots and Agrobacterium rhizogenes-transformed hairy roots. Planta 223:1344–1354
Boland W, Garms S (2010) Induced volatiles of Medicago truncatula: molecular diversity and mechanistic aspects of a multiproduct sesquiterpene synthase from M. truncatula. Flavour Fragr J 25:114–116
Guerche P, Jouanin L, Tepfer D, Pelletier G (1987) Genetic transformation of oilseed rape (Brassica napus) by the Ri T-DNA of Agrobacterium rhizogenes and analysis of inheritance of the transformed phenotype. Mol Gen Genet 206:382–386
Casanova E, Trillas MI, Moysset L, Vainstein A (2005) Influence of rol genes in floriculture. Biotechnol Adv 23:3–39
Zdravkovic-Korac S, Muhovski Y, Druart P, Calic D, Radojevic L (2004) Agrobacterium rhizogenes-mediated DNA transfer to Aesculus hippocastanum L and the regeneration of transformed plants. Plant Cell Rep 22:698–704
Komaraiah P, Reddy GV, Reddy PS, Raghavendra AS, Ramakrishna SV, Reddanna P (2003) Enhanced production of antimicrobial sesquiterpenes and lipoxygenases metabolites in elicitor-treated hairy root cultures of Solanum tuberosum. Biotechnol Lett 25:593–597
Saxena G, Banerjee S, Rahman L, Verma PC, Mallavarapu GR, Kumar S (2007) Rose-scented geranium (Pelargonium sp) generated by Agrobacterium rhizogenes mediated Ri insertion for improved essential oil quality. Plant Cell Tiss Org Cult 90:215–223
Jerkovic I, Gaso-Sokac D, Pavlovic H, Marijanovic Z, Gugic M, Petrovic I, Kovac S (2012) Volatile organic compounds from Centaurium erythraea Rafn (Croatia) and the antimicrobial potential of its essential oil. Molecules 17:2058–2072. doi:10.3390/molecules 17022058
Piatczak E, Krolicka A, Wysokinska H (2006) Genetic transformation of Centaurium erythraea Rafn by Agrobacterium rhizogenes and the production of secoiridoids. Plant Cell Rep 25:1308–131
Yang DC, Choi YE (2000) Production of transgenic plants via Agrobacterium rhizogenes-mediated transformation of Panax ginseng. Plant Cell Rep 19:491–496
Gorpenchenko T, Kiselev K, Bulgakov V, Tchernoded G, Bragina E, Khodakovskaya M, Koren OG, Batygina T, Zhuravlev Y (2006) The Agrobacterium rhizogenes rolC-gene-induced somatic embryogenesis and shoot organogenesis in Panax ginseng transformed calluses. Planta 223:457–467
Kang HJ, Anbazhagan VR, You XL, Moon HK, Yi JS, Choi YE (2006) Production of transgenic Aralia elata regenerated from Agrobacterium rhizogenes-mediated transformed roots. Plant Cell Tiss Org Cult 85:187–196
Kim JA, Kim Y-S, Choi Y-E (2011) Triterpenoid production and phenotypic changes in hairy roots of Codonopsis lanceolata and the plants regenerated from them. Plant Biotechnol Rep 5:255–263. doi:10.1007/s11816-011-0180-5
Inoue F, Sugiura H, Tabuchi A, Kawasawa DE, Minami M (2003) Plant regeneration of peppermint, Mentha piperita from the hairy roots generated from microsegment infected with Agrobacterium rhizogenes. Plant Biotechnol 20:169–172
Christey MC (2001) Use of Ri-mediated transformation for production of transgenic plants. In Vitro Cell Dev Biol Plant 3:687–700
Ackermann C (1977) C pflanzen aus Agrobacterium rhizogenes-tumoren aus Nicotiana tabacum. Plant Sci Lett 8:23–30
Vinterhalter B, Ninković S, Cingel A, Vinterhalter D (2006) Shoot and root culture of Hypericum perforatum L. transformed with Agrobacterium rhizogenes A4M70GUS. Biol Plant 50:767–770
David C, Petit A, Tempé J (1988) T-DNA length variability in mannopine hairy root: more than 50 kilobasepairs of pRi T-DNA can integrate in plant cells. Plant Cell Rep 7:92–95
Fründt C, Meyer AD, Ichikawa T, Meins F (1998) A tobacco homologue of the Ri-plasmid orf 13 gene causes cell proliferation in carrot discs. Mol Gen Genet 259:559–568
Franche C, Duhoux E (2001) Du transfert d’ADN à l’obtention d’une plante transgénique. In: Elsevier (ed) La transgenèse végétale Bio campus, Amsterdam
Collier R, Fuchs B, Walter N, Kevin Lutke W, Taylor CG (2005) Ex vitro composite plants: an inexpensive, rapid method for root biology. Plant J 43:449–457
Bottino PJ, Raineri D, Nester FW, Gordon MP (1989) Agrobacterium-mediated DNA transfer. J Tiss Cult Methods 12(4):135–138
Sheki H, Nishizawa T, Tanaka N, Niwa Y, Yoshida S, Muranaka T (2005) Hairy root-activation tagging: a high-throughput system for activation tagging in transformed hairy roots. Plant Mol Biol 59:793–807
Voinnet O, Baulcombe DC (1997) Systemic signalling in gene silencing. Nature 389:553
Busov V, Yordanov Y, Gou J, Meilan R, Ma C, Regan S, Strauss S (2011) Activation tagging is an effective gene tagging system in Populus. Tree Genet Genomes 7:91–101
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
Ayliffe MA, Pallotta M, Langridge P, Pryor AJ (2007) A barley activation tagging system. Plant Mol Biol 64(3):329–347
Lee C-Y, Agrawal DC, Chu T-M, Wang C-S, Yu S-M, Chen JJW, Tsay H-S (2008) T-DNA activation tagging as a tool to isolate Salvia miltiorrhiza Bunge transgenic lines for higher yields of pharmacological tanshinones. Planta Med 74(7):780–786
Choi D-W, Jung JD, Ha YI, Park H-W, In DS, Chung HJ, Liu JR (2005) Analysis of transcripts in methyl jasmonate-treated ginseng hairy roots to identify genes involved in the biosynthesis of ginsenosides and other secondary metabolites. Plant Cell Rep 23:557–566
Jian B, Hou W, Wu C, Liu B, Liu W, Song S, Bi Y, Han T (2009) Agrobacterium rhizogenes-mediated transformation of Superroot-derived Lotus corniculatus plants: a valuable tool for functional genomics. BMC Plant Biol 9:78–92
Zang L, Ding R, Chai Y, Bonfil M, Moyano E, Oksman-Caldentey K-M, Xu T, Pi Y, Wang Z, Zhang H, Kai G, Liao Z, Sun X, Tang K (2004) Engineering tropane biosynthetic pathway in Hyoscyamus niger hairy root cultures. Proc Natl Acad Sci USA 101(17):6786–6791
Cheng A-X, Lou Y-G, Mao Y-B, Lu S, Wang L-J, Chen X-Y (2007) Plant terpenoids: biosynthesis and ecological functions. J Integr Plant Biol 49(2):179–186
Ma Y, Yuan L, Wu B, X’en L, Chen S, Lu S (2012) Genome-wide identification and characterization of novel genes involved in terpenoid biosynthesis in Salvia miltiorrhiza. J Exp Bot 1–15. doi:10.1093/jxb/err466
Faria JMS, Nunes IS, Figueiredo AC, Pedro LG, Trindade H, Barroso JG (2009) Biotransformation of menthol and geraniol by hairy root cultures of Anethum graveolens: effect on growth and volatile components. Biotechnol Lett 31:897–903. doi:10.1007/s10529-009-9934-3
Hu Z-B, Du M (2006) Hairy root and its application in plant genetic engineering. J Integr Plant Biol 4(2):121–127
Bulgakov VP (2008) Functions of rol genes in plant secondary metabolism. Biotechnol Adv 26:318–324
Taneja J, Jaggi M, Wankhede DP, Sinha AK (2010) Effect of loss of T-DNA genes on MIA biosynthetic pathway gene regulation and alkaloid accumulation in Catharanthus roseus hairy roots. Plant Cell Rep 29:1119–1129
Mannan A, Shaheen N, Arshad W, Qureshi RA, Zia M, Mirza B (2008) Hairy roots induction and artemisinin Artemisia dubia and Artemisia indica. Afr J Biotechnol 7(18):3288–3292
Giri A, Narasu ML (2000) Transgenic hairy roots – recent trends and applications. Biotechnol Adv 18:1–22
Bais HP, Walker TS, Schweizer HP, Vivanco JM (2002) Root specific elicitation and microbial activity of rosmarinic acid in hairy root cultures of Ocimum basilicum. Plant Physiol Biochem 40:983–995
Uddin MR, Li X, Won OJ, Park SU, Pyon JY (2011) Herbicidal activity of phenolic compounds from hairy root cultures of Fagopyrum tataricum. Weed Res. doi:10.1111/j.01365-3180.2011.00894.x
Demole E, Lederer E, Mercier DE (1962) Isolement et détermination de la structure du jasmonate de méthyle constituant odorant caractéristique de l’essence de jasmin. Helvetica Chimica Acta 45:675–685
Rohwer CL, Erwin JE (2008) Horticultural applications of jasmonates: a review. J Horticultural Sci Biotechnol 83(3):283–304
Frankfater CR, Dowd MK, Triplett BA (2009) Effect of elicitors on the production of gossypol and methylated gossypol in cotton hairy roots. Plant Cell Tiss Org Cult 98:341–349
Ashrafi S, Mofid MR, Otroshi M, Ebrahimi M, Khosroshahli M (2010) Effects of plant growth regulators on the callogenesis and taxol production in cell suspension of Taxus baccata L. Trakia J Sci 8(2):36–43
Syklowska-Baranek K, Pietrosiuk A, Kokoszka A, Furmanowa M (2009) Enhancement of taxane production in hairy root culture of Taxus x media var. Hicksii. J Plant Physiol 166:1950–1954
Ge X, Wu J (2005) Induction and potentiation of diterpenoid tanshinone accumulation in Salvia miltiorrhiza hairy roots by β-aminobutyric acid. Appl Microbiol Biotechnol 68:183–188
Ge X, Wu J (2005) Tanshinone production and isoprenoid pathways in Salvia miltiorrhiza hairy roots induced by Ag+ and yeast elicitor. Plant Sci 168:487–491
Verpoorte R, van der Heijden R, ten Hoopen HJG, Memelink J (1999) Metabolic engineering of plant secondary metabolite pathways for the production of fine chemicals. Biotechnol Lett 21:467–479
Sivakumar G, Liu C, Towler MJ, Weathers PJ (2010) Biomass production of hairy roots of Artemisia annua and Arachis hypogaea in a scaled-up Mist bioreactor. Biotechnol Bioeng 107(5):802–813
Jeong GT, Park DH, Hwang B, Park K, Kim SW, Woo JC (2002) Studies on mass production of transformed –Panax ginseng hairy roots in bioreactor. Appl Biochem Biotechnol 98:1115–1127
Hahn EJ, Kim YS, Yu KW, Jeong CS, Paek KY (2003) Adventitious root cultures of Panax ginseng c.v. Meyer and ginsenoside production through large scale bioreactor system. J Plant Biotechnol 5:1–6
Salim AA, Chin Y-W, Kinghorn AD (2008) Drug discovery from plants. In: Ramawat KG, Mérillon JM (eds) Bioactive molecules and medicinal plants. Springer, Berlin, pp 1–24
Amin A, Mousa M (2007) Merits of anti-cancer plants from the Arabian Gulf region. Cancer Ther 5:55–66
Thoppil RJ, Bishayee A (2011) Terpenoids as potential chemopreventive and therapeutic agents in liver cancer. World J Hepatol 3(9):228–249
Zao K, Sun L, Ma X, Li X, Wang X, Ping W, Zhou D (2011) Improved taxol production in Nodulisporium sylviforme derived from inactivated protoplast fusion. Afr J Biotechnol 10(20):4175–4182
Gligorov J, Lotz J-P (2004) Preclinical pharmacology of the taxanes: implications of the differences. Oncologist 9(Suppl 2):3–8
Qian Z, Gong K, Zhang L, Lv J, Jing F, Wang Y, Guan S, Wang G, Tang K (2007) A simple and efficient procedure to enhance artemisinin content in Artemisia annua L by seeding to salinity stress. Afr J Biotechnol 6(12):1410–1413
Francis G, Kerem Z, Makkar HPS, Becker K (2002) The biological action of saponins in animal systems: a review. Br J Nutr 88:587–605
Bibi Y, Nisa S, Zia M, Waheed A, Ahmed S, Chaudhary F (2012) In vitro cytotoxic activity of Aesculus indica against breast adenocarcinoma cell line (MCF-7) and phytochemical analysis. Pak J Pharm Sci 25(1):183–187
Agnihotri S, Wakode S, Agnithori A (2010) An overview on anti-inflammatory properties and chemo-profiles of plants used in traditional medicine. Indian J Nat Prod Resour 1(2):150–167
Kabera J, Gasogo A, Uwamariya A, Ugirinshuti V, Nyetera P (2011) Insecticidal effects of essential oils of Pelargonium graveolens and Cymbopogon citrates on Sitophilus zeamais (Motsch.). Afr J Food Sci 5(6):366–375
Sallaud C, Rontein D, Onillon S, Jabès F, Duffé P, Giacalone C, Thoraval S, Escoffier C, Herbette G, Leonhardt N, Causse M, Tissier A (2009) A novel pathway for sesquiterpene biosynthesis from Z, Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaites. Plant Cell 21:301–317
Laurain D, Trémouillaux-Guiller J, Chénieux J-C, van Beek TA (1997) Production of ginkgolide and bilobalide in transformed and gametophyte derived cell cultures of Ginkgo biloba. Phytochemistry 46:127–130
Choi PS, Kim YD, Choi KM, Chung HJ, Choi DW, Liu JR (2004) Plant regeneration from hairy-root cultures transformed by infection with Agrobacterium rhizogenes in Catharanthus roseus. Plant Cell Rep 22:828–831
Mehrotra S, Kukreja AK, Khanuja SPS, Mishra BN (2008) Genetic transformation studies and scale up of hairy root culture of Glycyrrhiza glabra in bioreactor. Electronic J Biotechnol 5:199–222
Giri A, Ravindra ST, Dhingra V, Narasu ML (2001) Influence of different strains of Agrobacterium rhizogenes on induction of hairy roots and artemisinin production in Artemisia annua. Curr Sci 81:378–382
Sandhu NS, Kaur S, Chopra D (2010) Equisetum arvense: pharmacology and phytochemistry – a review. Asian J Pharm Clin Res 3(3):146–150
Makoto I, Ohta S, Komoto N, Ushijima M, Kodera Y, Hayama M, Shirota O, Sekita S, Kuroyanagi M (2008) Rapid identification of terpenoid saponins in the root of Codonopsis lanceolata by liquid chromatography-mass spectrometry. J Nat Med 62(4):423–429. doi:10.1007/s11418-008-0270-z
Makky EA, Mashitah MY, Ibrahim MM (2012) Impact of medicinal plant phytocomponents against antibiotic resistant bacteria. J Chem Pharm Res 4(1):881–893
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer-Verlag Berlin Heidelberg
About this entry
Cite this entry
Trémouillaux-Guiller, J. (2013). Hairy Root Culture: An Alternative Terpenoid Expression Platform. In: Ramawat, K., Mérillon, JM. (eds) Natural Products. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-22144-6_136
Download citation
DOI: https://doi.org/10.1007/978-3-642-22144-6_136
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-22143-9
Online ISBN: 978-3-642-22144-6
eBook Packages: Chemistry and Materials ScienceReference Module Physical and Materials ScienceReference Module Chemistry, Materials and Physics