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Front. Biol.    2015, Vol. 10 Issue (2) : 177-193    https://doi.org/10.1007/s11515-015-1355-1
REVIEW
Bioreactor technology for clonal propagation of plants and metabolite production
Nazmul H. A. Mamun1,Ulrika Egertsdotter1,2,Cyrus K. Aidun1,3,*()
1. G.W. Woodruff School of Mechanical Engineering, Georgia Institute of Technology, Atlanta, GA 30332, USA
2. Department of Forest Genetics and Plant Physiology, Ume? Plant Science Center, Swedish University of Agricultural Sciences, 901 83 Ume?, Sweden
3. Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA 30332, USA
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Abstract

Plant cell culture in bioreactors is an enabling tool for large scale production of clonal elite plants in agriculture, horticulture, forestry, pharmaceutical sectors, and for biofuel production. Advantages of bioreactors for plant cell culture have resulted in various types of bioreactors differing in design, operating technologies, instrumentations, and construction of culture vessels. In this review, different types of bioreactors for clonal propagation of plants and secondary metabolites production are discussed. Mechanical and biochemical parameters associated with bioreactor design, such as aeration, flow rate, mixing, dissolved oxygen, composition of built-up gas in the headspace, and pH of the medium, are pivotal for cell morphology, growth, and development of cells within tissues, embryos, and organs. The differences in such parameters for different bioreactor designs are described here, and correlated to the plant materials that have been successfully cultured in different types of bioreactors.
Keywords bioreactor types      mechanical and biochemical parameters      plant cell culture      plant clonal propagation      secondary metabolite production     
Corresponding Author(s): Cyrus K. Aidun   
Just Accepted Date: 05 March 2015   Issue Date: 06 May 2015
 Cite this article:   
Nazmul H. A. Mamun,Ulrika Egertsdotter,Cyrus K. Aidun. Bioreactor technology for clonal propagation of plants and metabolite production[J]. Front. Biol., 2015, 10(2): 177-193.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-015-1355-1
https://academic.hep.com.cn/fib/EN/Y2015/V10/I2/177
Fig.1  Different designs of stirred tank bioreactor; rotation of impeller in the bioreactor provides agitation to the liquid medium that helps to maintain homogeneity of nutrient and O2 in the medium. (A) Schematic of a conventional stirred tank bioreactor (Jay et al.,1992). (B) Stirred tank bioreactor with plastic mesh for immobilization of hairy roots (Cardillo et al., 2010). (C) Centrifugal impeller stirred tank bioreactor that provides an axial inlet and radial outlet of medium causing better mixing, low shear, and higher liquid lift (Wang and Zhong, 1996). (D) Cell lift impeller bioreactor in which cells along with medium are lifted through the draft tube of the impeller and result In either tangential or radial exit of cells, conventional flat bed and marine impellers were also used for comparison (Treat et al., 1989). (E) Bioreactor with double helical ribbon impeller that pumps liquid upward when rotates counter clockwise (Jolicoeur et al., 1992). (F) Rushton turbine and Scaba (SRGT) impellers (Amanullah et al., 1998); in Scaba impeller six curved parabolid blades were used and its rotation resulted in radial flow of fluid in the bioreactor.
Fig.2  Rotating Drum Bioreactor constructed with a vessel having baffles inside contains the culture and the medium at the bottom. Rotation of the vessel facilitates mass transfer under low shear condition (Tanaka et al.,1983).
Fig.3  Bubble column bioreactor. (A) Schematic of a conventional bubble column bioreactor having an air sparger at the bottom that generates air bubbles and provides agitation in the medium. (B) Arcuri et al. (1983) has used a settling zone for cell aggregates in the bubble column bioreactor for continuous operation (bubble formation and medium perfusion). (C) Cone shaped reactor working similar to conventional bubble column bioreactor reduces the possibility of dead zones (Fujimura et al., 1984), (D) bioreactor with cells immobilized on loofa sponges sparging air from the bottom and having medium circulation through an external loop (Ogbonna et al., 2001).
Fig.4  Various designs of airlift bioreactors in which the air or gas is sparged underneath the draft tube of the bioreactor; this causes a pressure difference between inside and outside of the draft tube and results in a fluid circulation in the bioreactor. A–C: Internal loop. D: external loop. (A) Smart and Fowler (1984), (B) Townsley et al. (1983), (C) Chen et al. (2010), and (D) Sajc et al. (1995).
Fig.5  Temporary immersion bioreactor in which the culture and the medium remain in separate containers or in different compartments in the same container so that the culture does not immerse in the medium continuously; instead the medium is pumped to the culture container/compartment, culture is soaked with the medium, and then the medium is drained out. (A) Tisserat and Vandercook (1985) and (B) Escalona et al. (1999).
Fig.6  Diffusion bioreactor having a helical shaped silicone tube permeable to O2, N2, and air that diffuse to the medium from the tube and the stirrer agitates the medium containing the culture (Luttman et al., 1994).
Fig.7  Perfusion bioreactor. (A) Su et al. (1996), (B) Su and Arias (2003), and (C) De Dobbeleer et al. (2006).
Fig.8  A few special types of bioreactors. (A) Magnetically stabilized fluidized bed bioreactor (Bramble et al., 1990). (B) Immobilized plant cell bioreactor (Choi et al., 1995). (C) Reciprocating plate bioreactor (Gagnon et al., 1999). (D) Flow bioreactors– (i) Single-column reactor, (ii) Radial flow reactor (Kino-oka et al., 1999). (E) Disposable bioreactors– (i) Wave bioreactor (Singh, 1999), (ii) Wave and Undertow bioreactor (Terrier et al., 2007), (iii) Slug bubble bioreactor (Terrier et al., 2007). (F) Membrane bioreactor (McDonald et al., 2005).
1 Akita M, Shigeoka T, Koizumi Y, Kawamura M (1994). Mass propagation of shoots of Stevia rebaudiana using a large scale bioreactor. Plant Cell Rep, 13: 180–183
2 Alvard D, Cote F, Teisson C (1993). Comparison of methods of liquid medium culture for banana micropropagation: effects of temporary immersion of explants. Plant Cell Tissue Organ Cult, 32(1): 55–60
https://doi.org/10.1007/BF00040116
3 Amanullah A, Serrano-Carreon L, Castro B, Galindo E, Nienow A W (1998). The influence of impeller type in pilot scale Xanthan fermentations. Biotechnol Bioeng, 57(1): 95–108
https://doi.org/10.1002/(SICI)1097-0290(19980105)57:1<95::AID-BIT12>3.0.CO;2-7
4 Arcuri E J, Nichols J R, Brix T S, Santamarina V G, Buckland B C, Drew S W (1983). Thienamycin production by immobilized cells of Streptomyces cattleya in a bubble column. Biotechnol Bioeng, 15(10): 2399–2411
https://doi.org/10.1002/bit.260251010
5 Attree S M, Pomeroy M K, Fowke L C (1994). Production of vigorous, desiccation tolerant white spruce (Picea glauca [Moench.]Voss.)synthetic seeds in a bioreactor. Plant Cell Rep, 13(11): 601–606
https://doi.org/10.1007/BF00232929
6 Atwell B J, Greenway H (1987). The relationship between growth and oxygen uptake in hypoxic rice seedlings. J Exp Bot, 38(3): 454–465
https://doi.org/10.1093/jxb/38.3.454
7 Ballica R, Ryu D Y (1993). Effects of rheological properties and mass transfer on plant cell bioreactor performance: production of tropane alkaloids. Biotechnol Bioeng, 42(10): 1181–1189
https://doi.org/10.1002/bit.260421008
8 Barry-Etienne D, Bertrand B, Schlonvoigt A, Etienne H (2002). The morphological variability within a population of coffee somatic embryos produced in a bioreactor affects the regeneration and the development of plants in the nursery. Plant Cell Tissue Organ Cult, 68(2): 153–162
https://doi.org/10.1023/A:1013874221569
9 Biddington N L, Robinson T H (1991). Ethylene production during anther culture of Brussel sprouts (Brassica oleracea var. gemmifera) and its relationship with factors that affect embryo production. Plant Cell Tissue Organ Cult, 25: 169–177
10 Bieniek M E, Harrell R C, Cantliffe D J (1995). Enhancement of somatic embryogenesis of Ipomoea batatas in solid cultures and production of mature somatic embryos in liquid cultures for application to a bioreactor production system. Plant Cell Tissue Organ Cult, 41(1): 1–8
https://doi.org/10.1007/BF00124080
11 Bramble J L, Graves D J, Brodelius P (1990). Calcium and phosphate effects on growth and alkaloid production in Coffea arabica experimental results and mathematical model. Biotechnol Bioeng, 37(9): 859–868
https://doi.org/10.1002/bit.260370910
12 Burg S P (1973). Ethylene in plant growth. Proc Nat Acad Sci, USA, 70(2): 591–597
13 Cardillo A B, Otálvaro A á M, Busto V D, Talou J R, Velásquez L M E, Giulietti A M (2010). Scopolamine, anisodamine and hyoscyamine production by Brugmansia candida hairy root cultures in bioreactors. Process Biochem, 45(9): 1577–1581
https://doi.org/10.1016/j.procbio.2010.06.002
14 Chen H B, Kao P M, Huang H C, Shieh C J, Chen C I, Liu Y C (2010). Effects of using various bioreactors on chitinolytic enzymes productin by Paenibacillus taichungensis. Biochem Eng J, 49(3): 337–342
https://doi.org/10.1016/j.bej.2010.01.008
15 Chen S Y, Huang S Y (2000). Shear stress effects on cell growth and L-DOPA production by suspension culture of Stizolobium hassjoo cells in an agitated bioreactor. Bioprocess Eng, 22(1): 5–12
https://doi.org/10.1007/PL00009100
16 Cho J M, Kwon J Y, Lim J A, Kim D I (2007). Increased hGM-CSF production and secretion with pluronic F-68 in transgenic Nicotiana tabacum suspension cell cultures. Biotechnol Bioprocess Eng., 12(6): 594–600
https://doi.org/10.1007/BF02931074
17 Choi H J, Tao B Y, Okos M R (1995). Enhancement of secondary metabolite production by immobilized Gossypium arboreum cells. Biotechnol Prog, 11(3): 306–311
https://doi.org/10.1021/bp00033a011
18 Choi Y S, Lee S Y, Kim D I (1999). Cultivation of Digitalis lanata cell suspension in an aqueous two-phase system. J Microbiol Biotechnol, 9(5): 589–592
19 Curtis W R (2005). Application of bioreactor design principles to plant micropropagation. Plant Cell Tissue Organ Cult, 81(3): 255–264
https://doi.org/10.1007/s11240-004-6646-1
20 De Dobbeleer C, Cloutier M, Fouilland M, Legros R, Jolicoeur M (2006). A high-rate perfusion bioreactor for plant cells. Biotechnol Bioeng, 95(6): 1126–1137
https://doi.org/10.1002/bit.21077
21 Debergh P, Aitken-Christie J, Cohen D, Grout B, Arnold S, Zimmerman R, Ziv M (1992). Reconsideration of the term ‘vitrification’ as used in micropropagation. Plant Cell Tissue Organ Cult, 30(2): 135–140
https://doi.org/10.1007/BF00034307
22 Debergh P, Harbaoui Y, Lemeur R (1981). Mass propagation of globe artichoke (Cynara scolymus): evaluation of different hypotheses to overcome vitrification with special reference to water potential. Physiol Plant, 53(2): 181–187
https://doi.org/10.1111/j.1399-3054.1981.tb04130.x
23 Domínguez A, Rivela I, Couto S R, Sanromán M A (2001). Design of a new rotating drum bioreactor for ligninolytic enzyme production by Phanerochaete chrysosporium grown on an inert support. Process Biochem, 37(5): 549–554
https://doi.org/10.1016/S0032-9592(01)00233-3
24 Doran P M (1999). Design of mixing systems for plant cell suspensions in stirred reactors. Biotechnol Prog, 15(3): 319–335
https://doi.org/10.1021/bp990042v
25 Egertsdotter U, Mo L H, von Arnold S (1993). Extracellular proteins in embryogenic suspension cultures of Norway spruce (Picea abies). Physiol Plant, 88(2): 315–321
https://doi.org/10.1111/j.1399-3054.1993.tb05505.x
26 Egertsdotter U, von Arnold S (1995). Importance of arabinogalactan proteins for the development of somatic embryos of Norway spruce (Picea abies). Physiol Plant, 93(2): 334–345
https://doi.org/10.1111/j.1399-3054.1995.tb02237.x
27 Egertsdotter U, von Arnold S (1998). Development of somatic embryos in Norway spruce. J Exp Bot, 49(319): 155–162
https://doi.org/10.1093/jxb/49.319.155
28 Eibl R, Kaiser S, Lombriser R, Eibl D (2010). Disposable bioreactors: the current state-of-the-art and recommended applications in biotechnology. Appl Microbiol Biotechnol, 86(1): 41–49
https://doi.org/10.1007/s00253-009-2422-9
29 El-Sayed A H M M, Rehm H J (1987). Continuous penicillin production by Penicilliumchrysogenum immobilized in calcium alginate beads. Appl Microbiol Biotechnol, 26(3): 215–218
https://doi.org/10.1007/BF00286311
30 Escalona M, Lorenzo J C, Gonzales B L, Daquinta M, Borroto C G, Gonzales J I, Desjardine Y (1999). Pineapple (Ananas cosmos L. Merr) micropropagation in temporary immersion systems. Plant Cell Rep, 18: 743–748
https://doi.org/10.1007/s002990050653
31 Fischer U, Santore U J, Husemann W, Barz W, Alfermann A W (1994). Semicontinuous cultivation of photoautotrophic cell-suspension cultures in a 20-L airlift-reactor. Plant Cell Tissue Organ Cult, 38(2—3): 123–134
https://doi.org/10.1007/BF00033869
32 Fu C C, Wu W T, Lu S Y (2003). Performance of airlift bioreactors with net draft tube. Enzyme Microb Technol, 33(4): 332–342
https://doi.org/10.1016/S0141-0229(03)00151-0
33 Fujimura M, Kato J, Tosa T, Chibata I (1984). Continuous production of L-arginine using immobilized growing Serratia marcescens cells: Effectiveness of supply of oxygen gas. Appl Microbiol Biotechnol, 19(2): 79–84
https://doi.org/10.1007/BF00302445
34 Fung C J, Metchell D A (1995). Baffles increase performance of solid-state fermentation in rotating drum bioreactors. Biotechnol Tech, 9(4): 295–298
https://doi.org/10.1007/BF00151578
35 Gagnon H, Thibault J, Cormier F, Do C B (1999). Vitis vinifera culture in a non-conventional bioreactor: the reciprocating plate bioreactor. Bioprocess Eng, 21(5): 405–413
36 Gaspar T (1991). Vitrification in micropropagation. In: Bajaj Y P S (Ed). Biotechnology in Agriculture and Forestry (vol.17). Berlin: Springer-Verlag, 117–126
37 Gaspar T, Kevers C, Debergh P, Maene L, Paques M, Boxus P (1987). Vitrification: morphological, physiological, and ecological aspects. In: Bonga J M, Durzan D J (Eds). Cell and Tissue Culture in Forestry (vol. 1). Dordrecht, Holland: Martinus Nijhoff Publishing, 152–166
38 Gaspar T, Kevers C, Franck T, Bisbis B, Billar J P, Huault C, Dily F L, Petit-Paly G, Rideau M, Penel C, Crevecoeur M, Greppin H (1995). Paradoxical results in the analysis of hyperhydric tissues considered as being under stress: questions for a debate. Bulg J Plant Physiol., 21(2—3): 80–97
39 Han J, Zhong J J (2003). Effects of oxygen partial pressure on cell growth and ginsenoside and polysaccharide production in high density cell cultures of Panax notoginseng. Enzyme Microb Technol, 32(3—4): 498–503
https://doi.org/10.1016/S0141-0229(02)00337-X
40 Hohe A, Winkelmann T, Schwenkel H G (1999). CO2 accumulation in bioreactor suspension cultures of Cyclamen persicum Mill. and its effect on cell growth and regeneration of somatic embryos. Plant Cell Rep, 18(10): 863–867
https://doi.org/10.1007/s002990050675
41 Honda H, Hiraoka K, Nagamori E, Omote M, Kato Y, Hiraoka S, Hobayashi T (2002). Enhanced anthocyanin production from grape callus in an air-lift type bioreactor using a viscous additive-supplemented medium. J Biosci Bioeng, 94(2): 135–139
https://doi.org/10.1016/S1389-1723(02)80133-5
42 Hooker B S, Lee J M, An G (1990). Cultivation of plant cells in a stirred vessel: effect of impeller design. Biotechnol Bioeng, 35(3): 296–304
https://doi.org/10.1002/bit.260350311
43 Hu W W, Yao H, Zhong J J (2001). Improvement of Panax notoginseng cell culture for production of ginseng saponin and polysaccharide by high density cultivation in pneumatically agitated bioreactors. Biotechnol Prog, 17(5): 838–846
https://doi.org/10.1021/bp010085n
44 Hu W W, Zhong J J (2001). Effect of bottom clearance on performance of airlift bioreactor in high-density culture of Panax notoginseng cells. J Biosci Bioeng, 92(4): 389–392
https://doi.org/10.1016/S1389-1723(01)80245-0
45 Huang S Y, Shen Y W, Chan H S (2002). Development of a bioreactor operation strategy for L-DOPA production using Stizolobium hassjoo suspension culture. Enzyme Microb Technol, 30(6): 779–791
https://doi.org/10.1016/S0141-0229(02)00058-3
46 Huang T K, McDonald K A (2009). Bioreactor engineering for recombinant protein production in plant cell suspension cultures. Biochem Eng J, 45(3): 168–184
https://doi.org/10.1016/j.bej.2009.02.008
47 Hvoslef-Eide A K, Olsen O A S, Lyngved R, Munster C, Heyerdahl P H (2005). Bioreactor design for propagation of somatic embryos. Plant Cell Tissue Organ Cult, 81(3): 265–276
https://doi.org/10.1007/s11240-004-6647-0
48 Illing S, Harrison S T L (1999). The kinetics and mechanism of Corynebacterium glutamicum aggregate breakup in bioreactors. Chem Eng Sci, 54(4): 441–454
https://doi.org/10.1016/S0009-2509(98)00253-X
49 Ingram B, Mavituna F (2000). Effect of bioreactor configuration on the growth and maturation of Picea sitchensis somatic embryo cultures. Plant Cell Tissue Organ Cult, 61(2): 87–96
https://doi.org/10.1023/A:1006333907907
50 Jackson M B, Fenning T M, Drew M C, Saker L R (1985). Stimulation of ethylene production and gas-space (aerenchyma) formation in adventitious roots of Zea mays L. by small partial pressures of oxygen. Planta, 165(4): 486–492
https://doi.org/10.1007/BF00398093
51 Jay V, Genestier S, Courduroux J C (1992). Bioreactor studies on the effect of dissolved oxygen concentrations on growth and differentiation of carrot (Daucus carota L.) cell cultures. Plant Cell Rep, 11(12): 605–608
https://doi.org/10.1007/BF00236382
52 Jay V, Genestier S, Courduroux J C (1994). Bioreactor studies on the effect of medium pH on carrot (Daucus carota L.) somatic embryogenesis. Plant Cell Tissue Organ Cult, 36(2): 205–209
https://doi.org/10.1007/BF00037721
53 Jianfeng X, Jian X, Aiming H, Pusun F, Zhiguo S (1998). Kinetic and technical studies on large-scale culture of Rhodiola sachalinensis compact callus aggregates with air-lift reactors. J Chem Technol Biotechnol, 72(3): 227–234
54 Jiménez E, Pérez N, de Feria M, Barbón R, Capote A, Chavez M, Quiala E, Pérez J C (1999). Improved production of potato microtubers using a temporary immersion system. Plant Cell Tissue Organ Cult, 59(1): 19–23
55 Jolicoeur M, Chavarie C, Carreau P J, Archambault J (1992). Development of a helical-ribbon impeller bioreactor for high-density plant cell suspension culture. Biotechnol Bioeng, 39(5): 511–521
https://doi.org/10.1002/bit.260390506
56 Kantarci N, Borak F, Ulgen K O (2005). Bubble column reactors. Process Biochem, 40(7): 2263–2283
https://doi.org/10.1016/j.procbio.2004.10.004
57 Kessell R H J, Carr A H (1972). The effect of dissolved oxygen concentration on growth and differentiation of carrot (Daucus carota) tissue. J Exp Bot, 23(4): 996–1007
https://doi.org/10.1093/jxb/23.4.996
58 Ke?ler M, ten Hoopen J G, Furusaki S (1999). The effect of the aggregate size on the production of ajmalicine and tryptamine in Catharanthus roseus suspension culture. Enzyme Microb Technol, 24(5—6): 308–315
https://doi.org/10.1016/S0141-0229(98)00121-5
59 Kevers C, Coumans M, Coumans-Gilles M F, Gasper T (1984). Physiological and biochemical events leading to vitrification of plants cultured in vitro. Physiol Plant, 61(1): 69–74
https://doi.org/10.1111/j.1399-3054.1984.tb06102.x
60 Kim J H, Yoo Y J (2002). Optimization of SOD biosynthesis by controlling sucrose concentration in the culture of carrot hairy root. J Microbiol Biotechnol, 12(4): 617–621
61 Kino-Oka R, Hitaka Y, Taya M, Tone S (1999). High-density culture of red beet hairy roots by considering medium flow condition in a bioreactor. Chem Eng Sci, 54(15—16): 3179–3186
https://doi.org/10.1016/S0009-2509(98)00345-5
62 Klvana M, Legros R, Jolicoeur M (2005). In situ extraction strategy affects benzophenanthridine alkaloid production fluxes in suspension cultures of Eschscholtzia californica. Biotechnol Bioeng, 89(3): 280–289
https://doi.org/10.1002/bit.20306
63 Kurata H, Furusaki S (1993). Immobilized Coffea arabica cell culture using a bubble-column reactor with controlled light intensity. Biotechnol Bioeng, 42(4): 494–502
https://doi.org/10.1002/bit.260420413
64 Langer E S (2011). Trends in perfusion bioreactors- the next revolution in bioprocessing. BioProcess Int., 9(10): 18–22
65 Lee-Parsons C W, Shuler M L (2002). The effect of ajmalicine spiking and resin addition timing on the production of indole alkaloids from Catharanthus roseus cell cultures. Biotechnol Bioeng, 79(4): 408–415
https://doi.org/10.1002/bit.10235
66 Loc N H, Tuan C V, Binh D H N, Phuong T T B, Kim T G, Yang M S (2009). Accumulation of sesquiterpenes and polysaccharides in cells of zedoary (Curcuma zedoaria Roscoe) cultured in a 10 L bioreactor. Biotechnol Bioprocess Eng., 14(5): 619–624
https://doi.org/10.1007/s12257-009-0013-3
67 Lorenzo J C, Gonzalez B L, Escalona M, Teisson C, Espinosa P, Borroto C (1998). Suggarcane shoot formation in an improved temporary immersion system. Plant Cell Tissue Organ Cult, 54(3): 197–200
https://doi.org/10.1023/A:1006168700556
68 Luo J, Mei X G, Liu L, Hu D W (2002). Improved paclitaxel production by fed-batch suspension cultures of Taxus chinensis in bioreactors. Biotechnol Lett, 24(7): 561–565
https://doi.org/10.1023/A:1014816609350
69 Luttman R, Florek P, Preil W (1994). Silicone-tubing aerated bioreactors for somatic embryo production. Plant Cell Tissue Organ Cult, 39(2): 157–170
https://doi.org/10.1007/BF00033923
70 Mandels M (1972). The culture of plant cells. Adv Biochem Eng, 2: 201–215
https://doi.org/10.1007/BFb0006670
71 McAlister B, Finnie J, Watt M P, Blakeway F (2005). Use of the temporary immersion bioreactor system (RITA (R)) for production of commercial Eucalyptus clones in Mondi Forests (SA). Plant Cell Tissue Organ Cult, 81(3): 347–358
https://doi.org/10.1007/s11240-004-6658-x
72 McDonald K A, Hong L M, Trombly D M, Xie Q, Jackman A P (2005). Production of human alpha-1-antitrypsin from transgenic rice cell culture in a membrane bioreactor. Biotechnol Prog, 21(3): 728–734
https://doi.org/10.1021/bp0496676
73 Molle F, Fressinet G (1992). Les semences arti?cielles. Phytoma., 441: 39–44
74 Mordocco A M, Brumbley J A, Lakshmanan P (2009). Development of a temporary immersion system (RITAA (R)) for mass production of sugarcane (Saccharum spp. interspecific hybrids). In Vitro Cell Dev Biol Plant, 45(4): 450–457
https://doi.org/10.1007/s11627-008-9173-7
75 Mostafa S S, Gu X S (2003). Strategies for improved dCO2 removal in large-scale fed-batch cultures. Biotechnol Prog, 19(1): 45–51
https://doi.org/10.1021/bp0256263
76 Namdev P K, Dunlop E H (1995). Shear sensitivity of plant cells in suspnesions- present and future. Appl Biochem Biotechnol, 54(1-3): 109–131
https://doi.org/10.1007/BF02787914
77 Niemenak N, Saare-Surminski K, Rohsius C, Ndoumou D O, Lieberei R (2008). Regeneration of somatic embryos in Theobroma cacao L. in temporary immersion bioreactor and analyses of free amino acids in different tissues. Plant Cell Rep, 27(4): 667–676
https://doi.org/10.1007/s00299-007-0497-2
78 Ogbonna J C, Mashima H, Tanaka H (2001). Scale up of fuel ethanol production form sugar beet juice using loofa sponge immobilized bioreactor. Bioresour Technol, 76(1): 1–8
https://doi.org/10.1016/S0960-8524(00)00084-5
79 Pal S, Das S, Dey S (2003). Peroxidase and arabinogalactan protein as by-products during somatic embryo cultivation in air-lift bioreactor. Process Biochem, 38(10): 1471–1477
https://doi.org/10.1016/S0032-9592(03)00036-0
80 Pan Z W, Wang H Q, Zhong J J (2000). Scale-up study on suspension cultures of Taxus chinensis cells for production of taxanediterpene. Enzyme Microb Technol, 27(9): 714–723
https://doi.org/10.1016/S0141-0229(00)00276-3
81 Pandey A (1992). Recent process developments in solid-state fermentation. Process Biochem, 27(2): 109–117
https://doi.org/10.1016/0032-9592(92)80017-W
82 Paques M, Boxus P (1987). Vitrification: review of literature. Acta Hortic, 212: 155–166
83 Perata P, Alpi A (1991). Ethanol-induced injuries to carrot cells- the role of acetaldehyde. Plant Physiol, 95(3): 748–752
https://doi.org/10.1104/pp.95.3.748
84 Pérez A, Nápoles L, Carvajal C, Hernandez M, Lorenzo J C (2004). Effect of sucrose, inorganic salts, inositol, and thiamine on protease excretion during pineapple culture in temporary immersion bioreactors. In Vitro Cell Dev Biol Plant, 40(3): 311–316
https://doi.org/10.1079/IVP2004529
85 Piehl G W, Berlin J, Mollenschott C, Lehmann J (1988). Growth and alkaloid production of a cell suspension culture of Thalictrum rugosum in shake flasks and membrane-stirrer reactors with bubble free aeration. Appl Microbiol Biotechnol, 29(5): 456–461
https://doi.org/10.1007/BF00269068
86 Prakash G, Srivastava A K (2008). Statistical elicitor optimization studies for the enhancement of azadirachtin production in bioreactor Azadirachta indica cell cultivation. Biochem Eng J, 40(2): 218–226
https://doi.org/10.1016/j.bej.2007.12.017
87 Preil W (1991). Application of bioreactors in plant micropropagation. In: Debergh P C, Zimmerman R H (Eds). Micropropagation, technology and application. Dordrecht, Netherlands: Kluwer Academic Publishers, 425–455
88 Preil W, Florek P, Wix U, Beck A (1988). Towards mass propagation by use of bioreactors. Acta Hortic, 226: 99–106
89 Rosensweig R E (1979). Fluidization: Hydrodynamic stabilization with a magnetic field. Science, 204(6): 57–60
https://doi.org/10.1126/science.204.4388.57
90 Rout G R, Mohapatra A, Jain S M (2006). Tissue culture of ornamental pot plant: A critical review on present scenario and future prospects. Biotechnol Adv, 24(6): 531–560
https://doi.org/10.1016/j.biotechadv.2006.05.001
91 Rout G R, Samantaray S, Das P (2000). In vitro manipulation and propagation of medicinal plants. Biotechnol Adv, 18(2): 91–120
https://doi.org/10.1016/S0734-9750(99)00026-9
92 Sajc L, Vunjak-Novakovic G, Grubisic D, Kova?evi? N, Vukovi? D, Bugarski B (1995). Production of anthraquinones by immobilized Frangula alnus Mill. plant cells in a four-phase air-lift bioreactor. Appl Microbiol Biotechnol, 43(3): 416–423
https://doi.org/10.1007/BF00218443
93 Schlatmann J E, Nuutila A M, van Gulik W M, ten Hoopen H J G, Verpoorte R, Heijnen J J (1993). Scaleup of ajmalicine production by plant cell cultures of Catharanthus roseus. Biotechnol Bioeng, 41(2): 253–262
https://doi.org/10.1002/bit.260410212
94 Schubert S, Schubert E, Mengel K (1990). Effect of low pH of the root medium on proton release, growth, and nutrient uptake of field beans (Vicia faba). Plant Soil, 124(2): 239–244
https://doi.org/10.1007/BF00009266
95 Scragg A H (1995). The problems associated with high biomass levels in plant cell suspensions. Plant Cell Tissue Organ Cult, 43(2): 163–170
https://doi.org/10.1007/BF00052172
96 Seki M, Ohzora C, Takeda M, Furusaki S (1997). Taxol (paclitaxel) production using free and immobilized cells of Taxus cuspidate. Biotechnol Bioeng, 53(2): 214–219
https://doi.org/10.1002/(SICI)1097-0290(19970120)53:2<214::AID-BIT12>3.0.CO;2-K
97 Seydel P, Christian W, Heike D (2009). Scale-up of Oldenlandia affinis suspension cultures in photobioreactors for cyclotide production. Eng Life Sci, 9(3): 219–226
https://doi.org/10.1002/elsc.200800103
98 Shi Z D, Yuan Y J, Wu J C, Shang G M (2003). Biological responses of suspension cultures of Taxus chinensis var. mairei to shear stresses in the short term. Appl Biochem Biotechnol, 110(2): 61–74
https://doi.org/10.1385/ABAB:110:2:61
99 Sim S J, Chang H N (1993). Increased shikonin production by hairy roots of Lithospermum erythrorhizon in 2 phase bubble column reactor. Biotechnol Lett, 15(2): 145–150
https://doi.org/10.1007/BF00133014
100 Singh V (1999). Disposable bioreactor for cell culture using wave-induced agitation. Cytotechnology, 30(1/3): 149–158
https://doi.org/10.1023/A:1008025016272
101 Small J G, Potgiether G P, Botha F C (1989). Anoxic seed germination of Erythrina caffra: Ethanol fermentation and response to metabolic inhibitors. J Exp Bot, 40(3): 375–381
https://doi.org/10.1093/jxb/40.3.375
102 Smart N J, Fowler M W (1984). Mass cultivation of Catharanthus roseus cells using a nonmechanically agitated bioreactor. Appl Biochem Biotechnol, 9(3): 209–216
https://doi.org/10.1007/BF02798487
103 Su W W, Arias R (2003). Continuous plant cell perfusion culture: bioreactor characterization and secreted enzyme production. J Biosci Bioeng, 95(1): 13–20
https://doi.org/10.1016/S1389-1723(03)80142-1
104 Su W W, He B J, Liang H, Sun S (1996). A perfusion air-lift bioreactor for high density plant cell cultivation and secreted protein production. J Biotechnol, 50(2—3): 225–233
105 Su W W, Lei F, Kao N P (1995). High density cultivation of Anchusaofficinalis in a stirred-tank bioreactor with in situ filtration. Appl Microbiol Biotechnol, 44(3—4): 293–299
https://doi.org/10.1007/BF00169919
106 Sun H (2010). The effect of hydrodynamic stress on plant embryo development. Ph.D. thesis, Georgia Institute of Technology, Atlanta, GA
107 Sun X, Linden J C (1999). Shear stress effects on plant cell suspension cultures in a rotating wall vessel bioreactor. J Ind Microbiol Biotechnol, 22(1): 44–47
https://doi.org/10.1038/sj.jim.2900600
108 Tanaka H, Nishijima F, Suwa M, Iwamoto T (1983). Rotating drum fermentor for plant cell suspension cultures. Biotechnol Bioeng, 25(10): 2359–2370
https://doi.org/10.1002/bit.260251007
109 Teng W L, Liu Y J, Tsai Y C, Soong T S (1994). Somatic embryogenesis of carrot in bioreactor culture systems. HortScience, 29(11): 1349–1352
110 Terashima M, Ejirim Y, Hashikawa N, Yoshida H (2000). Effects of sugar concentration on recombinant human alpha(1)-antitrypsin production by genetically engineered rice cell. Biochem Eng J, 6(3): 201–205
https://doi.org/10.1016/S1369-703X(00)00088-7
111 Terrier B, Courtois D, Henault N, Cuvier A, Bastin M, Aknin A, Dubreuil J, Petiard V (2007). Two new disposable bioreactors for plant cell culture: the wave and undertow bioreactor and the slug bubble bioreactor. Biotechnol Bioeng, 96(5): 914–923
https://doi.org/10.1002/bit.21187
112 Thanh N T, Murthy H N, Pandey D M, Yu K W, Hahn E J, Paek K Y (2006b). Effect of carbon dioxide on cell gwowth and saponin production in suspension cultures of Panax ginseng. Biol Plant, 50(4): 752–754
https://doi.org/10.1007/s10535-006-0123-0
113 Thomas D S, Murashige T (1979). Volatile emissions of plant tissue cultures. I. Identification of the major components. In Vitro, 15(9): 654–658
https://doi.org/10.1007/BF02618242
114 Tikhomiroff C, Allais S, Klvana M, Hisiger S, Jolicoeur M (2002). Continuous selective extraction of secondary metabolites from Catharanthus roseus hairy roots with silicon oil in a two-liquid-phase bioreactor. Biotechnol Prog, 18(5): 1003–1009
https://doi.org/10.1021/bp0255558
115 Tisserat B, Murashige T (1977). Effects of ethephon, ethylene, and 2,4-Dichlorophenoxyacetic acid on asexual embryogenesis in vitro. Plant Physiol, 60(3): 437–439
https://doi.org/10.1104/pp.60.3.437
116 Tisserat B, Vandercook C E (1985). Development of an automated plant culture system. Plant Cell Tissue Organ Cult, 5(2): 107–117
https://doi.org/10.1007/BF00040307
117 Tokashiki M, Arai T, Hamamoto K, Ishimaru K (1990). High density culture of hybridoma cells using a perfusion culture vessel with an external centrifuge. Cytotechnology, 3(3): 239–244
https://doi.org/10.1007/BF00365487
118 Townsley P M, Webster F, Kutney J P, Salisbury P, Hewitt G, Kawamura N, Choi L, Kurihara T, Jacoli G G (1983). The recycling air lift transfer fermenter for plant cell. Biotechnol Lett, 5(1): 13–18
https://doi.org/10.1007/BF00189957
119 Treat W J, Engler C R, Soltes E J (1989). Culture of photomixotrophic soybean and pine in a modified fermenter using a novel impeller. Biotechnol Bioeng, 34(9): 1191–1202
https://doi.org/10.1002/bit.260340910
120 Vinocur B, Carmi T, Altman A, Ziv M (2000). Enhanced bud regeneration in aspen (Populus tremula L.) roots cultured in liquid media. Plant Cell Rep, 19(12): 1146–1154
https://doi.org/10.1007/s002990000243
121 von Arnold S, Bozhkov P, Clapham D, Dyachok J, Filonova L, H?gberg K A, Ingouff M, Wiweger M (2005). Propagation of Norway spruce via somatic embryogenesis. Plant Cell Tissue Organ Cult, 81: 323–329
https://doi.org/10.1007/s11240-004-6662-1
122 Wang G R, Qi N M, Wang Z M (2010). Application of stir-tank bioreactor for perfusion culture and continuous harvest of Glycyrrhiza inflate suspension cells. Afr J Biotechnol, 9(3): 347–351
123 Wang S J, Zhong J J (1996). A novel centrifugal impeller bioreactor I. Fluid circulation, mixing, and liquid velocity profiles. Biotechnol Bioeng, 51(5): 511–519
https://doi.org/10.1002/(SICI)1097-0290(19960905)51:5<511::AID-BIT2>3.0.CO;2-F
124 Wang Z Y, Zhong J J (2002). Combination of conditioned medium and elicitation enhances taxoid production in bioreactor cultures of Taxus chinensis cells. Biochem Eng J, 12(2): 93–97
https://doi.org/10.1016/S1369-703X(02)00044-X
125 Williams R D, Chauret N, Bédard C, Archambault J (1992). Effect of polymeric adsorbents on the production of sanguinarine by Papaver somniferum cell-cultures. Biotechnol Bioeng, 40: 971–977
https://doi.org/10.1002/bit.260400813
126 Wongsamuth R, Doran P M (1997). The filtration properties of Atropa belladonna plant cell suspensions; effects of hydrodynamic shear and elevated carbon dioxide levels on culture and filtration parameters. J Chem Technol Biotechnol, 69(1): 15–26
https://doi.org/10.1002/(SICI)1097-4660(199705)69:1<15::AID-JCTB674>3.0.CO;2-J
127 Yang R Y K, Bayraktar O, Pu H T (2003). Plant-cell bioreactors with simultaneous electropermeabilization and electrophoresis. J Biotechnol, 100(1): 13–22
https://doi.org/10.1016/S0168-1656(02)00226-2
128 Zhong C, Yuan Y J (2009). Responses of Taxus cuspidatato hydrodynamics in bubble column bioreactors with different sparging nozzle sizes. Biochem Eng J, 45(2): 100–106
https://doi.org/10.1016/j.bej.2009.03.001
129 Zhong J J, Fujiyama K, Seki T, Yoshida T (1994). A quantitative analysis of shear effects on cell suspension and cell culture of Perilla frutescens in bioreactors. Biotechnol Bioeng, 44(5): 649–654
https://doi.org/10.1002/bit.260440512
130 Ziv M (1991). Vitrification: Morphological and physiological disorders of in vitro plants. In: Debergh P G, Zimmerman R H, (Eds). Micorpropagation: Technology and Application. Dordrecht, The Netherlands: Kluwer Academic Publishers, 45–69
131 Ziv M (2005). Simple bioreactors for mass propagation of plants. Plant Cell Tissue Organ Cult, 81(3): 277–285
https://doi.org/10.1007/s11240-004-6649-y
132 Zobayed S M A, Saxena P K (2003). In vitro-grown roots: a superior explant for prolific shoot regeneration of St. John?s wort (Hypericum perforatum L. cv ?New Stem?) in a temporary immersion bioreactor. Plant Sci, 165(3): 463–470
https://doi.org/10.1016/S0168-9452(03)00064-5
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