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Exudation: an expanding technique for continuous production and release of secondary metabolites from plant cell suspension and hairy root cultures

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Abstract

This review addresses methods of obtaining secondary metabolites from plant cell suspension and hairy root cultures and their exudates, particularly the physiological mechanisms of secondary metabolites release and trafficking. The efficiency for product recovery of metabolites can be increased by various methods, based on the principle of continuous product release into the cultivation medium. The most common methods for metabolite recovery are elicitation, influencing membrane permeability, and in situ product removal. The biosynthetic pathways can be influenced by cultivation conditions, transformation, or application of elicitors. The membrane permeability can be altered through the application of chemical or physical treatments. Product removal can be greatly increased through a two-phase system and the introduction of absorbents into the cultivation medium. In this review, we describe some improved approaches that have proven useful in these efforts.

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Abbreviations

DW:

Dry weight

FW:

Fresh weight

MS:

Murashige and Skoog

SA:

Salicylic acid

JA:

Jasmonic acid

MJ:

Methyl jasmonate

CWE:

Cell wall elicitor

PEF:

Pulsed electric fields

HHP:

High hydrostatic pressure

US:

Ultrasound

ISPR:

In situ product removal

DMSO:

Dimethylsulfoxide

References

  • Abbasi BH, Tian CL, Murch SJ, Saxena PK, Liu CZ (2007) Light-enhanced caffeic acid derivatives biosynthesis in hairy root cultures of Echinacea purpurea. Plant Cell Rep 26:1367–1372

    Article  PubMed  CAS  Google Scholar 

  • Abbott JA, Medina-Bolivar F, Martin EM, Engelberth AS, Villagarcia H, Clausen EC, Carrier DJ (2010) Purification of resveratrol, arachidin-1, and arachidin-3 from hairy root cultures of peanut (Arachis hypogaea) and determination of their antioxidant activity and cytotoxicity. Biotechnol Prog 26:1344–1351

    Article  PubMed  CAS  Google Scholar 

  • Almagro L, Perez AJL, Pedreno MA (2011) New method to enhance ajmalicine production in Catharanthus roseus cell cultures based on the use of cyclodextrins. Biotechnol Lett 33:381–385

    Article  PubMed  CAS  Google Scholar 

  • Amdoun R, Khelifi L, Khelifi-Slaoui M, Amroune S, Asch M, Assaf-Ducrocq C, Gontier E (2010) Optimization of the culture medium composition to improve the production of hyoscyamine in elicited Datura stramonium L. hairy roots using the response surface methodology (RSM). Int J Mol Sci 11:4726–4740

    Article  CAS  Google Scholar 

  • Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681

    Article  PubMed  CAS  Google Scholar 

  • Badri DV, Loyola-Vargas VM, Du J, Stermitz FR, Broeckling CD, Iglesias-Andreu L, Vivanco JM (2008) Transcriptome analysis of Arabidopsis roots treated with signaling compounds: a focus on signal transduction, metabolic regulation and secretion. New Phytol 179:209–223

    Article  PubMed  CAS  Google Scholar 

  • Bagger CL, Sørensen H, Sørensen JC (1998) High-quality oils, proteins, and bioactive products for food and non-food purposes based on biorefining of cruciferous oilseed crops. In: Gueguen J, Popineau Y (eds) Plant proteins from European crops. Springer, Berlin, pp 272–278

    Google Scholar 

  • Bais HP, Walker TS, Schweizer HP, Vivanco JA (2002) Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of Ocimum basilicum. Plant Physiol Biochem 40:983–995

    Article  CAS  Google Scholar 

  • Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32

    Article  PubMed  CAS  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  PubMed  CAS  Google Scholar 

  • Baker CJ, O’Neill NR, Deahl K, Lydon J (2002) Continuous production of extracellular antioxidants in suspension cells attenuates the oxidative burst detected in plant microbe interactions. Plant Physiol Biochem 40:641–644

    Article  Google Scholar 

  • Bakkali AT, Jaziri M, Foriers A, Vander Heyden Y, Vanhaelen N, Homes J (1997) Lawsone accumulation in normal and transformed cultures of henna, Lawsonia inermis. Plant Cell Tissue Organ Cult 51:83–87

    Article  Google Scholar 

  • Banerjee S, Rahman L, Uniyal GC, Ahuja PS (1998) Enhanced production of valepotriates by Agrobacterium rhizogenes induced hairy root cultures of Valeriana wallichii DC. Plant Sci 131:203–208

    Article  CAS  Google Scholar 

  • Barkakati P, Begum A, Das ML, Rao PG (2010) Adsorptive separation of ginsenoside from aqueous solution by polymeric resins: equilibrium, kinetic and thermodynamic studies. Chem Eng J 161:34–45

    Article  CAS  Google Scholar 

  • Baskaran P, Jayabalan N (2009) Psoralen production in hairy roots and adventitious roots cultures of Psoralea coryfolia. Biotechnol Lett 31:1073–1077

    Article  PubMed  CAS  Google Scholar 

  • Bauer N, Kiseljak D, Jelaska S (2009) The effect of yeast extract and methyl jasmonate on rosmarinic acid accumulation in Coleus blumei hairy roots. Biol Plantarum 53:650–656

    Article  CAS  Google Scholar 

  • Belhadj A, Telef N, Saigne C, Cluzet S, Barrieu F, Hamdi S, Mérillon J-M (2008) Effect of methyl jasmonate in combination with carbohydrates on gene expression of PR proteins, stilbene and anthocyanin accumulation in grapevine cell cultures. Plant Physiol Biochem 46:493–499

    Article  PubMed  CAS  Google Scholar 

  • Binder BYK, Peebles CAM, Shanks JV, San K-Y (2009) The effects of UV-B stress on the production of terpenoid indole alkaloids in Catharanthus roseus hairy roots. Biotechnol Prog 25:861–865

    Article  PubMed  CAS  Google Scholar 

  • Boitel-Conti M, Gontier E, Laberche JC, Ducrocq C, Sangwannorreel BS (1995) Permeabilization of Datura innoxia hairy roots for release of stored tropane alkaloids. Planta Med 61:287–290

    Article  PubMed  CAS  Google Scholar 

  • Boitel-Conti M, Gontier E, Laberche JC, Ducrocq C, SangwanNorreel BS (1996) Inducer effect of Tween 20 permeabilization treatment used for release of stored tropane alkaloids in Datura innoxia Mill hairy root cultures. Plant Cell Rep 16:241–244

    CAS  Google Scholar 

  • Bonfill M, Mangas S, Moyano E, Cusido RM, Palazon J (2011) Production of centellosides and phytosterols in cell suspension cultures of Centella asiatica. Plant Cell Tissue Organ Cult 104:61–67

    Article  CAS  Google Scholar 

  • Bourgaud F, Gravot A, Milesi S, Gontier E (2001) Production of plant secondary metabolites: a historical perspective. Plant Sci 161:839–851

    Article  CAS  Google Scholar 

  • Brodelius P, Pedersen H (1993) Increasing secondary metabolite production in plant cell culture by redirecting transport. Trends Biotechnol 11:30–36

    Article  PubMed  CAS  Google Scholar 

  • Cai Z, Kastell A, Mewis I, Knorr D, Smetanska I (2011a) Polysaccharide elicitors enhance anthocyanin and phenolic acid accumulation in cell suspension cultures of Vitis vinifera. Plant Cell Tissue Organ Cult. doi:10.1007/s11240-11011-10051-11243

  • Cai Z, Riedel H, Saw NMMT, Kütük O, Mewis I, Jäger H, Knorr D, Smetanska I (2011b) Effects of pulsed electric field on secondary metabolism of Vitis vinifera L. cv. Gamay Fréaux suspension culture and exudates. Appl Biochem Biotechnol 164:443–453

    Article  PubMed  CAS  Google Scholar 

  • Cai Z, Riedel H, Saw NMMT, Mewis I, Reineke K, Knorr D, Smetanska I (2011c) Effects of elicitors and high hydrostatic pressure on secondary metabolism of Vitis vinifera suspension culture. Process Biochem 46:1411–1416

    Article  CAS  Google Scholar 

  • Cardillo AB, Otalvaro AAM, Busto VD, Talou JR, Velasquez LME, Giulietti AM (2010) Scopolamine, anisodamine and hyoscyamine production by Brugmansia candida hairy root cultures in bioreactors. Process Biochem 45:1577–1581

    Article  CAS  Google Scholar 

  • Caretto S, Quarta A, Durante M, Nisi R, de Paolis A, Blando F, Mita G (2011) Methyl jasmonate and miconazole differently affect arteminisin production and gene expression in Artemisia annua suspension cultures. Plant Biol 13:51–58

    Article  PubMed  CAS  Google Scholar 

  • Chakraborty A, Chattopadhyay S (2008) Stimulation of menthol production in Mentha piperita cell culture. In Vitro Cell Dev Biol Anim Plant 44:518–524

    Article  CAS  Google Scholar 

  • Chandra S, Chandra R (2011) Engineering secondary metabolite production in hairy roots. Phytochem Rev 10:371–395

    Article  CAS  Google Scholar 

  • Chen H, Chen F (2000) Effect of yeast elicitor on the secondary metabolism of Ti-transformed Salvia miltiorrhiza cell suspension cultures. Plant Cell Rep 19:710–717

    Article  CAS  Google Scholar 

  • Chiang L, Abdullah MA (2007) Enhanced anthraquinones production from adsorbent-treated Morinda elliptica cell suspension cultures in production medium strategy. Process Biochem 42:757–763

    Article  CAS  Google Scholar 

  • Condori J, Sivakumar G, Hubstenberger J, Dolan MC, Sobolev VS, Medina-Bolivar F (2010) Induced biosynthesis of resveratrol and the prenylated stilbenoids arachidin-1 and arachidin-3 in hairy root cultures of peanut: effects of culture medium and growth stage. Plant Physiol Biochem 48:310–318

    Article  PubMed  CAS  Google Scholar 

  • Corrales M, Toepfl S, Butz P, Knorr D, Tauscher B (2008) Extraction of anthocyanins from grape by-products assisted by ultrasonics, high hydrostatic pressure or pulsed electric fields: a comparison. Innov Food Sci Emerg Technol 9:85–91

    Article  CAS  Google Scholar 

  • Dong J, Wan G, Liang Z (2010) Accumulation of salicylic acid-induced phenolic compounds and raised activities of secondary metabolic and antioxidative enzymes in Salvia miltiorrhiza cell culture. J Biotechnol 148:99–104

    Article  PubMed  CAS  Google Scholar 

  • Donnez D, Kim K-H, Antoine S, Conreux A, De Luca V, Jeandet P, Clément C, Courot E (2011) Bioproduction of resveratrol and viniferins by an elicited grapevine cell culture in a 2 L stirred bioreactor. Process Biochem 46:1056–1062

    Article  CAS  Google Scholar 

  • Dornenburg H, Knorr D (1997) Challenges and opportunities for metabolite production from plant cell and tissue cultures. Food Technol 51:47–54

    CAS  Google Scholar 

  • Engels C, Neumann G, Gahoonia TS, George E, Schenk M (2000) Assessing the ability of roots for nutrient acquisition. In: Schmidt AL (ed) Root methods. Springer, Berlin, pp 403–459

    Google Scholar 

  • Ersus S, Barrett DM (2010) Determination of membrane integrity in onion tissues treated by pulsed electric fields: use of microscopic images and ion leakage measurements. Innov Food Sci Emerg Technol 11:598–603

    Article  CAS  Google Scholar 

  • Ferri M, Dipalo SCF, Bagni N, Tassoni A (2011a) Chitosan elicits mono-glucosylated stilbene production and release in fed-batch bioreactor cultures of grape cells. Food Chem 124:1473–1479

    Article  CAS  Google Scholar 

  • Ferri M, Righetti L, Tassoni A (2011b) Increasing sucrose concentrations promote phenylpropanoid biosynthesis in grapevine cell cultures. J Plant Physiol 168:189–195

    Article  PubMed  CAS  Google Scholar 

  • Fincan M, Dejmek P (2003) Effect of osmotic pretreatment and pulsed electric field on the viscoelastic properties of potato tissue. J Food Eng 59:169–175

    Article  Google Scholar 

  • Flores HE, Vivanco JM, Loyola-Vargas VM (1999) ‘Radicle’ biochemistry: the biology of root-specific metabolism. Trends Plant Sci 4:220–226

    Article  PubMed  Google Scholar 

  • Fornara V, Onelli E, Sparvoli F, Rossoni M, Aina R, Marino G, Citterio S (2008) Localization of stilbene synthase in Vitis vinifera L. during berry development. Protoplasma 233:83–93

    Article  PubMed  CAS  Google Scholar 

  • Gangopadhyay M, Dewanjee S, Bhattacharya S (2011) Enhanced plumbagin production in elicited Plumbago indica hairy root cultures. J Biosci Bioeng 111:706–710

    Article  PubMed  CAS  Google Scholar 

  • Garcia JAL, Barbas C, Probanza A, Barrientos ML, Manero FJG (2001) Low molecular weight organic acids and fatty acids in root exudates of two Lupinus cultivars at flowering and fruiting stages. Phytochem Anal 12:305–311

    Article  CAS  Google Scholar 

  • Gaume A, Komarnytsky S, Borisjuk N, Raskin I (2003) Rhizosecretion of recombinant proteins from plant hairy roots. Plant Cell Rep 21:1188–1193

    Article  PubMed  CAS  Google Scholar 

  • Georgiev M, Georgiev V, Penchev P, Antonova D, Pavlov A, Ilieva M, Popov S (2010a) Volatile metabolic profiles of cell suspension cultures of Lavandula vera, Nicotiana tabacum and Helianthus annuus, cultivated under different regimes. Eng Life Sci 10:148–157

    CAS  Google Scholar 

  • Georgiev VG, Weber J, Kneschke EM, Denev PN, Bley T, Pavlov AI (2010b) Antioxidant activity and phenolic content of betalain extracts from intact plants and hairy root cultures of the red beet root Beta vulgaris cv. Detroit dark red. Plant Foods Hum Nutr 65:105–111

    Article  PubMed  CAS  Google Scholar 

  • Gleba D, Borisjuk NV, Borisjuk LG, Kneer R, Poulev A, Sarzhinskaya M, Dushenkov S, Logendra S, Gleba YY, Raskin I (1999) Use of plant roots for phytoremediation and molecular farming. Proc Natl Acad Sci USA 96:5973–5977

    Article  PubMed  CAS  Google Scholar 

  • Gueven A, Knorr D (2011) Isoflavonoid production by soy plant callus suspension culture. J Food Eng 103:237–243

    Article  CAS  Google Scholar 

  • Guillon S, Tremouillaux-Guiller J, Pati PK, Rideau M, Gantet P (2006) Hairy root research: recent scenario and exciting prospects—commentary. Curr Opin Plant Biol 9:341–346

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto T, Yamada Y (2003) New genes in alkaloid metabolism and transport. Curr Opin Biotechnol 14:163–168

    Article  PubMed  CAS  Google Scholar 

  • Hu YH, Yu YT, Piao CH, Liu JM, Yu HS (2011) Methyl jasmonate- and salicylic acid-induced d-chiro-inositol production in suspension cultures of buckwheat (Fagopyrum esculentum). Plant Cell Tissue Organ Cult 106:419–424

    Article  CAS  Google Scholar 

  • Janositz A, Noack AK, Knorr D (2011) Pulsed electric fields and their impact on the diffusion characteristics of potato slices. LWT Food Sci Technol 44:1939–1945

    Article  CAS  Google Scholar 

  • Kai G, Xu H, Zhou C, Liao P, Xiao J, Luo X, You L, Zhang L (2011) Metabolic engineering tanshinone biosynthetic pathway in Salvia miltiorrhiza hairy root cultures. Metab Eng 13:319–327

    Article  PubMed  CAS  Google Scholar 

  • Kaimoyo E, Farag MA, Sumner LW, Wasmann C, Cuello JL, VanEtten H (2008) Sub-lethal levels of electric current elicit the biosynthesis of plant secondary metabolites. Biotechnol Prog 24:377–384

    Article  PubMed  CAS  Google Scholar 

  • Kajani AA, Mofid MR, Abolfazli K, Tafreshi SAH (2010) Encapsulated activated charcoal as a potent agent for improving taxane synthesis and recovery from cultures. Biotechnol Appl Biochem 56:71–76

    Article  PubMed  CAS  Google Scholar 

  • Karwasara V, Jain R, Tomar P, Dixit V (2010) Elicitation as yield enhancement strategy for glycyrrhizin production by cell cultures of Abrus precatorius Linn. In Vitro Cell Dev Biol Anim Plant 46:354–362

    Article  CAS  Google Scholar 

  • Kastell A (2009) Induction of hairy root culture by Agrobacterium rhizogenes in different Brassica plants—impact of phytohormones and precursors in the glucosinolates accumulation. Diploma thesis (Diplomarbeit in german), Berlin University of Technology

  • Kastell A, Cai Z, Mewis I, Smetanska I (2011) Improved production of glucosinolates by jasmonic acid and tryptophan in brassica hairy roots and exudates. Paper presented at World Congress on Biotechnology, Hyderabad

  • Kiddle GA, Doughty KJ, Wallsgrove RM (1994) Salicylic acid-induced accumulation of glucosinolates in oilseed tape (Brassica napus L.) leaves. J Exp Bot 45:1343–1346

    Article  CAS  Google Scholar 

  • Kim Y, Wyslouzil BE, Weathers PJ (2002) Invited review: secondary metabolism of hairy root cultures in bioreactors. In Vitro Cell Dev Biol Anim Plant 38:1–10

    Article  CAS  Google Scholar 

  • Kim YH, Kim Y, Cho E, Kwak S, Kwon S, Bae J, Lee B, Meen B, Huh GH (2004) Alterations in intracellular and extracellular activities of antioxidant enzymes during suspension culture of sweetpotato. Phytochemistry 65:2471–2476

    Article  PubMed  CAS  Google Scholar 

  • Kim OT, Bang KH, Shin YS, Lee MJ, Jung SJ, Hyun DY, Kim YC, Seong NS, Cha SW, Hwang B (2007) Enhanced production of asiaticoside from hairy root cultures of Centella asiatica (L.) Urban elicited by methyl jasmonate. Plant Cell Rep 26:1941–1949

    Article  PubMed  CAS  Google Scholar 

  • Kim OT, Kim SH, Ohyama K, Muranaka T, Choi YE, Lee HY, Kim MY, Hwang B (2010a) Upregulation of phytosterol and triterpene biosynthesis in Centella asiatica hairy roots overexpressed ginseng farnesyl diphosphate synthase. Plant Cell Rep 29:403–411

    Article  PubMed  CAS  Google Scholar 

  • Kim YK, Xu H, Park WT, Park NI, Lee SY, Park SU (2010b) Genetic transformation of buckwheat (Fagopyrum esculentum M.) with Agrobacterium rhizogenes and production of rutin in transformed root cultures. Aust J Crop Sci 4:485–490

    CAS  Google Scholar 

  • Knorr D, Caster C, Dorneburg H, Dorn R, Graf S, Havkinfrenkel D, Podstolski A, Werrman U (1993) Biosynthesis and yield Improvement of food ingredients from plant-cell and tissue-cultures. Food Technol 47:57–63

    CAS  Google Scholar 

  • Komaraiah P, Ramakrishna SV, Reddanna P, Kishor PBK (2003) Enhanced production of plumbagin in immobilized cells of Plumbago rosea by elicitation and in situ adsorption. J Biotechnol 101:181–187

    Article  PubMed  CAS  Google Scholar 

  • Komaraiah P, Kishor PBK, Carlsson M, Magnusson KE, Mandenius CF (2005) Enhancement of anthraquinone accumulation in Morinda citrifolia suspension cultures. Plant Sci 168:1337–1344

    Article  CAS  Google Scholar 

  • Korsangruang S, Soonthornchareonnon N, Chintapakorn Y, Saralamp P, Prathanturarug S (2010) Effects of abiotic and biotic elicitors on growth and isoflavonoid accumulation in Pueraria candollei var. candollei and P. candollei var. mirifica cell suspension cultures. Plant Cell Tissue Organ Cult 103:333–342

    Article  CAS  Google Scholar 

  • Kuzma L, Bruchajzer E, Wysokinska H (2009) Methyl jasmonate effect on diterpenoid accumulation in Salvia sclarea hairy root culture in shake flasks and sprinkle bioreactor. Enzyme Microb Technol 44:406–410

    Article  CAS  Google Scholar 

  • Langcake P, Pryce RJ (1976) The production of resveratrol by Vitis vinifera and other members of the Vitaceae as a response to infection or injury. Physiol Plant Pathol 9:77–86

    Article  CAS  Google Scholar 

  • Lee CWT, Shuler ML (2000) The effect of inoculum density and conditioned medium on the production of ajmalicine and catharanthine from immobilized Catharanthus roseus cells. Biotechnol Bioeng 67:61–71

    Article  PubMed  CAS  Google Scholar 

  • Li M, Peebles CAM, Shanks JV, San K-Y (2011) Effect of sodium nitroprusside on growth and terpenoid indole alkaloid production in Catharanthus roseus hairy root cultures. Biotechnol Prog 27:625–630

    Article  PubMed  CAS  Google Scholar 

  • Lijavetzky D, Almagro L, Belchi-Navarro S, Martinez-Zapater J, Bru R, Pedreno M (2008) Synergistic effect of methyljasmonate and cyclodextrin on stilbene biosynthesis pathway gene expression and resveratrol production in Monastrell grapevine cell cultures. BMC Res Notes 1:132

    Article  PubMed  CAS  Google Scholar 

  • Lin LD, Wu JY (2002) Enhancement of shikonin production in single- and two-phase suspension cultures of Lithospermum erythrorhizon cells using low-energy ultrasound. Biotechnol Bioeng 78:81–88

    Article  PubMed  CAS  Google Scholar 

  • Liu CZ, Guo C, Wang YC, Ouyang F (2002) Effect of light irradiation on hairy root growth and artemisinin biosynthesis of Artemisia annua L. Process Biochem 38:581–585

    Article  CAS  Google Scholar 

  • Martinoia E, Klein M, Geisler M, Bovet L, Forestier C, Kolukisaoglu U, Muller-Rober B, Schulz B (2002) Multifunctionality of plant ABC transporters—more than just detoxifiers. Planta 214:345–355

    Article  PubMed  CAS  Google Scholar 

  • Martinoia E, Maeshima M, Neuhaus HE (2007) Vacuolar transporters and their essential role in plant metabolism. J Exp Bot 58:83–102

    Article  PubMed  CAS  Google Scholar 

  • Mathur A, Gangwar A, Mathur AK, Verma P, Uniyal GC, Lal RK (2010) Growth kinetics and ginsenosides production in transformed hairy roots of American ginseng—Panax quinquefolium L. Biotechnol Lett 32:457–461

    Article  PubMed  CAS  Google Scholar 

  • Merbach W, Mirus E, Knof G, Remus R, Ruppel S, Russow R, Gransee A, Schulze J (1999) Release of carbon and nitrogen compounds by plant roots and their possible ecological importance. J Plant Nutr Soil Sci 162:373–383

    Article  CAS  Google Scholar 

  • Moreno PRH, Vanderheijden R, Verpoorte R (1995) Cell and tissue cultures of Catharanthus roseus—a literature survey 2: updating from 1988 to 1993. Plant Cell Tissue Organ Cult 42:1–25

    Article  Google Scholar 

  • Mulder-Krieger T, Verpoorte R, Svendsen AB, Scheffer JJC (1988) Production of essential oils and flavours in plant cell and tissue cultures. A review. Plant Cell Tissue Organ Cult 13:85–154

    Article  CAS  Google Scholar 

  • Neumann G, Roemheld V (2002) Root-induced changes in the availability of nutrients in the rhizosphere. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dehker, New York, pp 617–649

    Google Scholar 

  • Olsen NV, Grunert KG, Sonne AM (2010) Consumer acceptance of high-pressure processing and pulsed-electric field: a review. Trends Food Sci Technol 21:464–472

    Article  CAS  Google Scholar 

  • Pavlov A, Popov S, Kovacheva E, Georgiev M, Ilieva M (2005) Volatile and polar compounds in Rosa damascena Mill 1803 cell suspension. J Biotechnol 118:89–97

    Article  PubMed  CAS  Google Scholar 

  • Pawar K, Yadav A, Shouche Y, Thengane S (2011) Influence of endophytic fungal elicitation on production of inophyllum in suspension cultures of Calophyllum inophyllum L. Plant Cell Tissue Organ Cult 106:345–352

    Article  CAS  Google Scholar 

  • Peč J, Flores-Sanchez I, Choi Y, Verpoorte R (2010) Metabolic analysis of elicited cell suspension cultures of Cannabis sativa L. by 1H-NMR spectroscopy. Biotechnol Lett 32:935–941

    Article  PubMed  CAS  Google Scholar 

  • Petersen M, Simmonds MSJ (2003) Molecules of interest—rosmarinic acid. Phytochemistry 62:121–125

    Article  PubMed  CAS  Google Scholar 

  • Prakash G, Srivastava AK (2011) Integrated yield and productivity enhancement strategy for biotechnological production of azadirachtin by suspension culture of Azadirachta indica. Asia Pac J Chem Eng 6:129–137

    Article  CAS  Google Scholar 

  • Rao SR, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20:101–153

    Article  PubMed  CAS  Google Scholar 

  • Roberts SC, Naill M, Gibson DM, Shuler ML (2003) A simple method for enhancing paclitaxel release from Taxus canadensis cell suspension cultures utilizing cell wall digesting enzymes. Plant Cell Rep 21:1217–1220

    Article  PubMed  CAS  Google Scholar 

  • Roja G, Bhangale AS, Juvekar AR, Eapen S, D’Souza SF (2005) Enhanced production of the polysaccharide arabinogalactan using immobilized cultures of Tinospora cordifolia by elicitation and in situ adsorption. Biotechnol Prog 21:1688–1691

    Article  PubMed  CAS  Google Scholar 

  • Santamaria AR, Mulinacci N, Valletta A, Innocenti M, Pasqua G (2011) Effects of elicitors on the production of resveratrol and viniferins in cell cultures of Vitis vinifera L. cv Italia. J Agric Food Chem 59:9094–9101

    Article  PubMed  CAS  Google Scholar 

  • Sanz MK, Hernandez XE, Tonn CE, Guerreiro E (2000) Enhancement of tessaric acid production in Tessaria absinthioides cell suspension cultures. Plant Cell Rep 19:821–824

    Article  Google Scholar 

  • Schreiner M, Krumbein A, Knorr D, Smetanska I (2011) Enhanced glucosinolates in root exudates of Brassica rapa ssp. rapa mediated by salicylic acid and methyl jasmonate. J Agric Food Chem 59:1400–1405

    Article  PubMed  CAS  Google Scholar 

  • Shanks JV, Morgan J (1999) Plant ‘hairy root’ culture. Curr Opin Biotechnol 10:151–155

    Article  PubMed  CAS  Google Scholar 

  • Shi M, Kwok KW, Wu Jian Y (2007) Enhancement of tanshinone production in Salvia miltiorrhiza Bunge (red or Chinese sage) hairy-root culture by hyperosmotic stress and yeast elicitor. Biotechnol Appl Biochem 46:191–196

    Article  PubMed  CAS  Google Scholar 

  • Shinde AN, Malpathak N, Fulzele DP (2009) Enhanced production of phytoestrogenic isoflavones from hairy root cultures of Psoralea corylifolia L. using elicitation and precursor feeding. Biotechnol Bioprocess Eng 14:288–294

    Article  CAS  Google Scholar 

  • Shinde AN, Malpathak N, Fulzele D (2010) Impact of nutrient components on production of the phytoestrogens daidzein and genistein by hairy roots of Psoralea corylifolia. J Nat Med 64:346–353

    Article  PubMed  CAS  Google Scholar 

  • Smetanska I (2006) Impact of elicitors on glucosinolate production in plants and exudates of turnip (Brassica rapa). Dissertation, Berlin University of Technology

  • Smetanska I (2008) Production of secondary metabolites using plant cell cultures. Food Biotechnol 111:187–228

    Article  CAS  Google Scholar 

  • Soliva-Fortuny R, Balasa A, Knorr D, Martin-Belloso O (2009) Effects of pulsed electric fields on bioactive compounds in foods: a review. Trends Food Sci Technol 20:544–556

    Article  CAS  Google Scholar 

  • Srivastava S, Srivastava AK (2007) Hairy root culture for mass-production of high-value secondary metabolites. Crit Rev Biotechnol 27:29–43

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tassoni A, Fornalè S, Franceschetti M, Musiani F, Michael AJ, Perry B, Bagni N (2005) Jasmonates and Na-orthovanadate promote resveratrol production in Vitis vinifera cv. Barbera cell cultures. New Phytol 166:895–905

    Article  PubMed  CAS  Google Scholar 

  • Tharayil N, Triebwasser DJ (2010) Elucidation of a diurnal pattern of catechin exudation by Centaurea stoebe. J Chem Ecol 36:200–204

    Article  PubMed  CAS  Google Scholar 

  • Trejo-Tapia G, Cuevas-Celis J, Salcedo-Morales G, Trejo-Espino JL, Arenas-Ocampo ML, Jimenez-Aparicio A (2007) Beta vulgaris L. suspension cultures permeabilized with triton X-100 retain cell viability and betacyanines production ability: a digital image analysis study. Biotechnol Prog 23:359–363

    Article  PubMed  CAS  Google Scholar 

  • Udomsuk L, Jarukamjorn K, Tanaka H, Putalun W (2011) Improved isoflavonoid production in Pueraria candollei hairy root cultures using elicitation. Biotechnol Lett 33:369–374

    Article  PubMed  CAS  Google Scholar 

  • Verma PC, Trivedi I, Singh H, Shukla AK, Kumar M, Upadhyay SK, Pandey P, Hans AL, Singh PK (2009) Efficient production of gossypol from hairy root cultures of cotton (Gossypium hirsutum L.). Curr Pharm Biotechnol 10:691–700

    Article  PubMed  CAS  Google Scholar 

  • Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51

    Article  PubMed  CAS  Google Scholar 

  • Wallaart TE, Pras N, Quax WJ (1999) Isolation and identification of dihydroartemisinic acid hydroperoxide from Artemisia annua: a novel biosynthetic precursor of artemisinin. J Nat Prod 62:1160–1162

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Tan RX (2002) Artemisinin production in Artemisia annua hairy root cultures with improved growth by altering the nitrogen source in the medium. Biotechnol Lett 24:1153–1156

    Article  CAS  Google Scholar 

  • Wang YC, Zhang HX, Zhao B, Yuan XF (2001) Improved growth of Artemisia annua L. hairy roots and artemisinin production under red light conditions. Biotechnol Lett 23:1971–1973

    Article  CAS  Google Scholar 

  • Wang JW, Zheng LP, Wu JY, Tan RX (2006) Involvement of nitric oxide in oxidative burst, phenylalanine ammonia-lyase activation and taxol production induced by low-energy ultrasound in Taxus yunnanensis cell suspension cultures. Nitric Oxide Biol Chem 15:351–358

    Article  CAS  Google Scholar 

  • Wang JW, Zheng LP, Zhang B, Zou T (2009) Stimulation of artemisinin synthesis by combined cerebroside and nitric oxide elicitation in Artemisia annua hairy roots. Appl Microbiol Biotechnol 85:285–292

    Article  PubMed  CAS  Google Scholar 

  • Wang CT, Liu H, Gao XS, Zhang HX (2010) Overexpression of G10H and ORCA3 in the hairy roots of Catharanthus roseus improves catharanthine production. Plant Cell Rep 29:887–894

    Article  PubMed  CAS  Google Scholar 

  • Weathers PJ, Towler MJ, Xu JF (2010) Bench to batch: advances in plant cell culture for producing useful products. Appl Microbiol Biotechnol 85:1339–1351

    Article  PubMed  CAS  Google Scholar 

  • Wiktorowska E, Dlugosz M, Janiszowska W (2010) Significant enhancement of oleanolic acid accumulation by biotic elicitors in cell suspension cultures of Calendula officinalis L. Enzyme Microb Technol 46:14–20

    Article  CAS  Google Scholar 

  • Wink M (1994) The cell-culture medium—a functional extracellular compartment of suspension-cultured cells. Plant Cell Tissue Organ Cult 38:307–319

    Article  CAS  Google Scholar 

  • Wink M (2010) Biochemistry of plant secondary metabolism. Blackwell, London

  • Woodley JM, Bisschops M, Straathof AJJ, Ottens M (2008) Future directions for in situ product removal (ISPR). J Chem Technol Biotechnol 83:121–123

    Article  CAS  Google Scholar 

  • Wu JY, Ge XC (2004) Oxidative burst, jasmonic acid biosynthesis, and taxol production induced by low-energy ultrasound in Taxus chinensis cell suspension cultures. Biotechnol Bioeng 85:714–721

    Article  PubMed  CAS  Google Scholar 

  • Xu M, Jin H, Dong J, Zhang M, Xu X, Zhou T (2011a) Abscisic acid plays critical role in ozone-induced taxol production of Taxus chinensis suspension cell cultures. Biotechnol Prog. doi:10.1002/btpr.1660

  • Xu M, Yang B, Dong J, Lu D, Jin H, Sun L, Zhu Y, Xu X (2011b) Enhancing hypericin production of Hypericum perforatum cell suspension culture by ozone exposure. Biotechnol Prog 27:1101–1106

    Article  CAS  Google Scholar 

  • Yan Q, Hu ZD, Tan RX, Wu JY (2005) Efficient production and recovery of diterpenoid tanshinones in Salvia miltiorrhiza hairy root cultures with in situ adsorption, elicitation and semi-continuous operation. J Biotechnol 119:416–424

    Article  PubMed  CAS  Google Scholar 

  • Yan Q, Wu J, Liu R (2011) Modeling of tanshinone synthesis and phase distribution under the combined effect of elicitation and in situ adsorption in Salvia miltiorrhiza hairy root cultures. Biotechnol Lett 33:813–819

    Article  PubMed  CAS  Google Scholar 

  • Yazaki K (2005) Transporters of secondary metabolites. Curr Opin Plant Biol 8:301–307

    Article  PubMed  CAS  Google Scholar 

  • Yazaki K (2006) ABC transporters involved in the transport of plant secondary metabolites. FEBS Lett 580:1183–1191

    Article  PubMed  CAS  Google Scholar 

  • Ye H, Huang LL, Chen SD, Zhong JJ (2004) Pulsed electric field stimulates plant secondary metabolism in suspension cultures of Taxus chinensis. Biotechnol Bioeng 88:788–795

    Article  PubMed  CAS  Google Scholar 

  • Yue XG, Zhang W, Deng MC (2011) Hyper-production of (13)C-labeled trans-resveratrol in Vitis vinifera suspension cell culture by elicitation and in situ adsorption. Biochem Eng J 53:292–296

    Article  CAS  Google Scholar 

  • Zabala M, Angarita M, Restrepo J, Caicedo L, Perea M (2010) Elicitation with methyl-jasmonate stimulates peruvoside production in cell suspension cultures of Thevetia peruviana. In Vitro Cell Dev Biol Anim Plant 46:233–238

    Article  CAS  Google Scholar 

  • Zamboni A, Vrhovsek U, Kassemeyer HH, Mattivi F, Velasco R (2006) Elicitor-induced resveratrol production in cell cultures of different grape genotypes (Vitis spp.). Vitis 45:63–68

    CAS  Google Scholar 

  • Zamboni A, Gatto P, Cestaro A, Pilati S, Viola R, Mattivi F, Moser C, Velasco R (2009) Grapevine cell early activation of specific responses to DIMEB, a resveratrol elicitor. BMC Genomics 10:363

    Article  PubMed  CAS  Google Scholar 

  • Zang YX, Kim DH, Park BS, Hong SB (2009) Metabolic engineering of indole glucosinolates in chinese cabbage hairy roots expressing Arabidopsis CYP79B2, CYP79B3, and CYP83B1. Biotechnol Bioprocess Eng 14:467–473

    Article  CAS  Google Scholar 

  • Zare K, Nazemiyeh H, Movafeghi A, Khosrowshahli M, Motallebi-Azar A, Dadpour M, Omidi Y (2010) Bioprocess engineering of Echium italicum L.: induction of shikonin and alkannin derivatives by two-liquid-phase suspension cultures. Plant Cell Tissue Organ Cult 100:157–164

    Article  CAS  Google Scholar 

  • Zhai DD, Zhong JJ (2010) Simultaneous analysis of three bioactive compounds in Artemisia annua hairy root cultures by reversed-phase high-performance liquid chromatography-diode array detector. Phytochem Anal 21:524–530

    Article  PubMed  CAS  Google Scholar 

  • Zhang C, Fevereiro PS (2007) The effect of heat shock on paclitaxel production in Taxus yunnanensis cell suspension cultures: role of abscisic acid pretreatment. Biotechnol Bioeng 96:506–514

    Article  PubMed  CAS  Google Scholar 

  • Zhang CH, Fevereiro PS, He G, Chen Z (2007) Enhanced paclitaxel productivity and release capacity of Taxus chinensis cell suspension cultures adapted to chitosan. Plant Sci 172:158–163

    Article  CAS  Google Scholar 

  • Zhang HC, Liu JM, Lu HY, Gao SL (2009) Enhanced flavonoid production in hairy root cultures of Glycyrrhiza uralensis Fisch by combining the over-expression of chalcone isomerase gene with the elicitation treatment. Plant Cell Rep 28:1205–1213

    Article  PubMed  CAS  Google Scholar 

  • Zhang HL, Xue SH, Pu F, Tiwari RK, Wang XY (2010) Establishment of hairy root lines and analysis of gentiopicroside in the medicinal plant Gentiana macrophylla. Russ J Plant Physiol 57:110–117

    Article  CAS  Google Scholar 

  • Zhang HC, Liu JM, Chen HM, Gao CC, Lu HY, Zhou H, Li Y, Gao SL (2011) Up-regulation of licochalcone A biosynthesis and secretion by Tween 80 in hairy root cultures of Glycyrrhiza uralensis Fisch. Mol Biotechnol 47:50–56

    Article  PubMed  CAS  Google Scholar 

  • Zhao JL, Zhou LG, Wu JY (2010) Promotion of Salvia miltiorrhiza hairy root growth and tanshinone production by polysaccharide-protein fractions of plant growth-promoting rhizobacterium Bacillus cereus. Process Biochem 45:1517–1522

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to Irene Hemmerich from Berlin University of Technology and Inga Mewis from Leibniz Institute of Vegetable and Ornamental Crops Grossbeeren and Erfurt, for their continuous advice and help. We also want to thank Russell Cooper from Georg-August University Gottingen for help with linguistic questions.

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Authors and Affiliations

  1. Institute of Food Biotechnology and Food Chemistry, Berlin University of Technology, Königin-Luise Str. 22, 14195, Berlin, Germany

    Zhenzhen Cai, Anja Kastell, Dietrich Knorr & Iryna Smetanska

  2. Department of Plant Food Processing, University of Applied Science Weihenstephan-Triesdorf, Steingruber Str. 2, 91746, Weidenbach, Germany

    Iryna Smetanska

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  1. Zhenzhen Cai
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  2. Anja Kastell
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  3. Dietrich Knorr
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  4. Iryna Smetanska
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Correspondence to Zhenzhen Cai.

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Communicated by R. Reski.

A contribution to the Special Issue: Plant Molecular Pharming in 2012 and Beyond.

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Cai, Z., Kastell, A., Knorr, D. et al. Exudation: an expanding technique for continuous production and release of secondary metabolites from plant cell suspension and hairy root cultures. Plant Cell Rep 31, 461–477 (2012). https://doi.org/10.1007/s00299-011-1165-0

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  • DOI: https://doi.org/10.1007/s00299-011-1165-0

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