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Review Article

Bioreactor-based advances in plant tissue and cell culture: challenges and prospects

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, , ORCID Icon, ORCID Icon, ORCID Icon, & ORCID Icon show all
Pages 20-34 | Received 02 Nov 2017, Accepted 04 Jun 2018, Published online: 15 Nov 2018

References

  • Denchev PD, Kuklin AI, Scragg AH. Somatic embryo production in bioreactors. J Biotechnol. 1992;26:99–109.
  • Giri C, Shyamkumar B, Anjaneyulu C. Progress in tissue culture, genetic transformation and applications of biotechnology to trees: an overview. Trees. 2004;18:115–135.
  • Guan Y, Li S-G, Fan X-F, et al. Application of somatic embryogenesis in woody plants. Front Plant Sci. 2016;7:938.
  • Uchendu EE, Shukla MR, Reed BM, et al. Improvement of ginseng by in vitro culture: challenges and opportunities. Compr Biotechnol. 2011;4:317–329.
  • Takayama S, Misawa M. Mass propagation of Begonia hiemalis plantlet by shake culture. Plant. Cell Physiol. 1981;22:461–467.
  • Hvoslef-Eide AK, Olsen OAS, Lyngved R. Bioreactor design for propagation of somatic embryos. Plant Cell Tiss Organ Cult. 2005;81:265–276.
  • Takayama S, Akita M. Bioengineering aspects of bioreactor application in plant propagation. In: Dutta S, Ibaraki Y, editors. Plan Tissue Culture Engineering. Dordrecht: Springer; 2006, p. 83–100.
  • Furusaki S, Takeda T. Bioreactors for plant cell culture. Ref Mod Life Sci. 2017; doi: 10.1016/B978-0-12-809633-8.09076-2
  • Palomares LA, Ramírez OT. Bioreactor scale-up. In: Flickinger MC, editor. Encyclopedia of industrial biotechnology: Bioprocess, bioseparation, and cell technology. Hoboken (NJ): John Wiley & Sons, Inc.; 2009 doi: 10.1002/9780470054581.eib143
  • Kong L, Holtz CT, Nairn CJ, et al. Application of airlift bioreactors to accelerate genetic transformation in American chestnut. Plant Cell Tiss Organ Cult. 2014;117:39–50.
  • Kuklin AI, Denchev PD, Atanassov AI, et al. Alfalfa embryo production in airlift vessels via direct somatic embryogenesis. Plant Cell Tiss Organ Cult. 1994;38:19–23.
  • Teng W-L, Liu Y-J, Tsai Y-C, et al. Somatic embryogenesis of carrot in bioreactor culture systems. Hortic Sci. 1994;29:1349–1352.
  • Tapia E, Sequeida A, Castro A, et al. Development of grapevine somatic embryogenesis using an airlift bioreactor as an efficient tool in the generation of transgenic plants. J Biotechnol. 2009;139:95–101.
  • Jiménez JA, Alonso-Blázquez N, López-Vela D, et al. Influence of culture vessel characteristics and agitation rate on gaseous exchange, hydrodynamic stress, and growth of embryogenic cork oak (Quercus suber L.) cultures. In Vitro Cell Dev Biol Plant. 2011;47:578–588.
  • AL-Mashhadani MKH, Wilkinson SJ, Zimmerman WB. Airlift bioreactor for biological applications with microbubble mediated transport processes. Chemic Eng Sci. 2015;137:243–253.
  • Georgiev MI, Weber J. Bioreactors for plant cells: hardware configuration and internal environment optimization as tools for wider commercialization. Biotechnol Lett. 2014;36:1359–1367.
  • Georgiev MI, Eibl R, Zhong JJ. Hosting the plant cells in vitro: recent trends in bioreactors. Appl Microbiol Biotechnol. 2013;97:3787–3800.
  • Sun X, Linden JC. Shear stress effects on plant cell suspension cultures in a rotating wall vessel bioreactor. J Indust Microbiol Biotechnol. 1999;22:44–47.
  • Sánchez Pérez JA, Rodríguez Porcel EM, Casas López JL, et al. Shear rate in stirred tank and bubble column bioreactors. Chemic Eng J. 2006;124:1–5.
  • Del Carmen OSM, Morales-López E, Durán-Páramo E, et al. Shear rate and microturbulence effects on the synthesis of proteases by Jacaratia mexicana cells cultured in a bubble column, airlift, and stirred tank bioreactors. Biotechnol Bioproc E. 2013;18:808–818.
  • Zhong JJ. Bioreactor engineering. In Murray M-Y, editors. Compr Biotechnol. Vol 2, 2nd edn. Amsterdam: Elsevier; 2011. p. 165–177.
  • Georgiev MI, Ludwig-Mueller J, Weber J, et al. Bioactive metabolites production and stress-related hormones in devil’s claw cell suspension cultures grown in bioreactors. Appl Microbiol Biotechnol. 2011;89:1683–1691.
  • Moorhouse SD, Wilson G, Hennerty MJ, et al. A plant cell bioreactor with medium-perfusion for control of somatic embryogenesis in liquid cell suspensions. Plant Growth Regul. 1996;20:53–56.
  • Mirro R, Voll K. Which impeller is right for your cell line? BioProcess Int. 2009;7:52–57.
  • Issa HM. Oxygen mass transfer in an aerated stirred tank with double impellers: A generalized correlation including spacing impact. Int J Chemic Eng. 2016; 2016:1–6.
  • Alok S, Immanuel G. Effect of different impellers and baffles on aerobic stirred tank fermenter using computational fluid dynamics. J Bioprocess Biotechnol. 2014;4:1–9.
  • Archambault J, Williams RD, Lavoie L, et al. Production of somatic embryos in a helical ribbon impeller bioreactor. Biotechnol Bioeng. 1994;44:930–943.
  • Kamen AA, Chavarie C, André G, et al. Design parameters and performance of a surface baffled helical ribbon impeller for the culture of shear sensitive cells. Chem Eng Sci. 1992;47:2375–2380.
  • Jolicoeur M, Chavarie C, Carreau PJ, et al. Development of a helical-ribbon impeller bioreactor for high-density plant cell suspension culture. Biotechnol Bioeng. 1992;39:511–521.
  • Mellor LF, Baker TL, Brown RJ, et al. Optimal 3-D culture of primary articular chondrocytes for use in the rotating wall vessel bioreactor. Aviat Space Environ Med. 2014;85:798–804.
  • Chang HN, Furusaki S. Membrane bioreactors: present and prospects. Adv Biochem Eng Biotechnol. 1991;44:27–64.
  • Wolff C, Beutel S, Scheper T. Tubular membrane bioreactors for biotechnological processes. Appl Microbiol Biotechnol. 2013;97:929–937.
  • Huang T-K, McDonald KA. Molecular farming using bioreactor-based plant cell suspension cultures for recombinant protein production. In: Wang A, Ma S, editors. Molecular Farming in Plants: Recent Advances and Future Prospects. The Netherlands: Springer; 2012. p. 37–67.
  • Ochoa-Villarreal M, Howat S, Hong S-M, et al. Plant cell culture strategies for the production of natural products. BMB Rep. 2016;49:149–158.
  • Sorvari S, Mäkeläinen R, Ahanen K, et al. Membranes to reduce adherence of somatic embryos to the cell lift impeller of a bioreactor. In: Hvoslef-Eide AK, Preil W, editors. Liquid Culture Systems for in vitro Plant Propagation. The Netherlands: Springer; 2008, p. 117–125.
  • Yang RYK, Bayraktar O, Pu HT. Plant-cell bioreactors with simultaneous electropermeabilization and electrophoresis. J Biotechnol. 2003;100:13–22.
  • Luttman R, Florek P, Preil W. Silicone-tubing aerated bioreactors for somatic embryo production. Plant Cell Tiss Organ Cult. 1994;39:157–170.
  • Eibl R, Eibl D. Design of bioreactors suitable for plant cell and tissue cultures. Phytochem Rev. 2008;7:593–598.
  • Frahm B, Brod H, Langer U. Improving bioreactor cultivation conditions for sensitive cell lines by dynamic membrane aeration. Cytotechnol. 2009;59:17–30.
  • Ziv M. Silicon effects on growth acclimatization and stress tolerance of bioreactor cultured Ornithogalum dubium plants. Acta Hortic. 2010;865:29–36.
  • Sivanesan I, Park SW. The role of silicon in plant tissue culture. Front Plant Sci. 2014;5:571.
  • Zimmerman WB, Zandi M, Hemaka Bandulasena HC, et al. Design of an airlift loop bioreactor and pilot scales studies with fluidic oscillator induced microbubbles for growth of a microalgae Dunaliella salina. Appl Energy. 2011;88:3357–3369.
  • Li X, Li P, Zu L, et al. Gas-liquid mass transfer characteristics with microbubble aeration – I. Standard stirred tank. Chem Eng Technol. 2016;39:945–952.
  • Han Y, Liu Y, Jiang H, et al. Large scale preparation of microbubbles by multi-channel ceramic membranes: Hydrodynamics and mass transfer characteristics. Can J Chemic Eng. 2017;95:2176–2185. doi: 10.1002/cjce.22825
  • Wei P, Zhang K, Gao W, et al. CFD modeling of hydrodynamic characteristics of slug bubble flow in a flat sheet membrane bioreactor. J Membr Sci. 2013;445:15–24.
  • Terrier B, Courtois D, Henault N, et al. Two new disposable bioreactors for plant cell culture: the wave and undertow bioreactor and the slug bubble bioreactor. Biotechnol Bioeng. 2007;96:914–923.
  • Gòdia F, Solà C. Fluidized-Bed Bioreactors. Biotechnol Prog. 1995;11:479–497.
  • Gharelo RS, Oliaei ED, Bandehagh A, et al. Production of therapeutic proteins through plant tissue and cell culture. J BioSci Biotechnol. 2016;5:93–104.
  • Andrews G. Fluidized-bed bioreactors. Biotechnol Genet Eng Rev. 1988;6:151–178.
  • Nagai N, Kuroiwa I, Kanda T, et al. Improvement of a fixed bed bioreactor for plant cell culture. J Ferment Bioeng. 1994;77:212–214.
  • Eibl R, Kaiser S, Lombriser R, et al. Disposable bioreactors: the current state-of-the-art and recommended applications in biotechnology. Appl Microbiol Biotechnol. 2010;86:41–49.
  • Valdiani A, Talei D, Lattoo SK, et al. Genoproteomics-assisted improvement of Andrographis paniculata: toward a promising molecular and conventional breeding platform for autogamous plants affecting pharmaceutical industry. Crit Rev Biotechnol. 2017;37:803–816.
  • Vallejos JR, Uplekar S, da Silva JF, et al. A case study in converting disposable process scouting devices into disposable bioreactors as a future bioprocessing tool. Biotechnol Bioeng. 2012;109:2790–2797.
  • Eibl R, Eibl D. Design and use of the wave bioreactor for plant cell culture. In: Gupta SD, Ibaraki Y, editors. Plant Tissue Culture Engineering. Dordrecht: Springer; 1st edn. 2008. p. 223–229.
  • Klöckner W, Diederichs S, Büchs J. Orbitally shaken single-use bioreactors. Adv Biochem Eng Biotechnol. 2014;138:45–46.
  • Raven N, Schillberg S, Rasche S. Plant cell-based recombinant antibody manufacturing with a 200 L orbitally shaken disposable bioreactor. Methods Mol Biol. 2016;1385:161–172.
  • Wilson PDG, Hilton MG, Robins RJ, et al. Fermentation studies of transformed root cultures. International Conference on Bioreactors and Biotransformations. London: Elsevier; 1987, p. 38–51.
  • Weathers P, Liu C, Towler M, et al. Mist reactors: principles, comparison of various systems, and case studies. Electron J Integr Biosci. 2008;3:29–37.
  • Srivastava S, Srivastava AK. In vitro azadirachtin production by hairy root cultivation of Azadirachta indica in nutrient mist bioreactor. Appl Biochem Biotechnol. 2012;166:365–378.
  • Simonetti G, Tocci N, Valletta A, et al. In vitro antifungal activity of extracts obtained from Hypericum perforatum adventitious roots cultured in a mist bioreactor against planktonic cells and biofilm of Malassezia furfur. Nat Prod Res. 2016;30:544–550.
  • Tscheschke B, Dreimann J, von der Ruhr JW, et al. Evaluation of a new mist-chamber bioreactor for biotechnological applications. Biotechnol Bioeng. 2015;112:1155–1164.
  • Wang GR, Qi NM. Influence of mist intervals and aeration rate on growth and second metabolite production of Pseudostellaria heterophylla adventitious roots in a siphon-mist bioreactor. Biotechnol Bioproc Eng. 2010;15:1059–1064.
  • Patyna A, Witczak S. Overview of photobioreactors for the production of biodiesel. Chemik. 2016;70:634–643.
  • Mulumba N, Farag IH. Tubular photobioreactor for microalgae biodiesel production. Int J Eng Sci Technol. 2012;4:703–709.
  • Silva AG, Carter R, Merss FLM, et al. Life cycle assessment of biomass production in microalgae compact photobioreactors. GCB Bioenergy. 2015;7:184–194.
  • Böhme C, Schröder M-B, Jung-Heiliger H, et al. Plant cell suspension culture in a bench-scale with a newly designed membrane stirrer for bubble-free aeration. Appl Microbiol Biotechnol. 1997;48:149–154.
  • Ho CH, Her JM, Duan KJ. Investigation the optimum culture variable for taxol production from Taxus mairei cells by perfusion cultivation. In: Proceedings of the 1999 CIChE Annual Meeting and Conferences of Chemical Engineering Technology (Taiwan); 1999. p. 213–216.
  • Ho C-W, Jian W-T, Lai H-C. Plant regeneration via somatic embryogenesis from suspension cell cultures of Lilium × formolongi Hort. using a bioreactor system. In Vitro Cell Dev Biol Plant.. 2006;42:240–246.
  • Brena B, González-Pombo P, Batista-Viera F. Immobilization of enzymes: a literature survey. Methods Mol Biol. 2013;1051:15–31.
  • Xu J, Ge X, Dolan MC. Towards high-yield production of pharmaceutical proteins with plant cell suspension cultures. Biotechnol Adv. 2011;29:278–299.
  • Archambault J, Volesky B, Kurz WGW. Surface immobilization of plant cells. Biotechnol Bioeng. 1989;33:293–299.
  • Tyler PT, Kurz WGW, Paiva NL, et al. Bioreactors for surface-immobilized cells. Plant Cell Tiss Organ Cult. 1995;42:81–90.
  • Bentebibel S, Moyano E, Palazón J, et al. Effects of immobilization by entrapment in alginate and scale-up on paclitaxel and baccatin III production in cell suspension cultures of Taxus baccata. Biotechnol Bioeng. 2005;89:647–655.
  • Rao SR, Ravishankar GA. Plant cell cultures: Chemical factories of secondary metabolites. Biotechnol Adv. 2002;20:101–153.
  • Bodeutsch T, James EA, Lee JM. The effect of immobilization on recombinant protein production in plant cell culture. Plant Cell Rep. 2001;20:562–566.
  • Asada M, Shuler ML. Stimulation of ajmalicine production and excretion from Catharanthus roseus: effects of adsorption in situ, elicitors and alginate immobilization. Appl Microbiol Biotechnol. 1989;30:475–481.
  • Harris RE, Mason EB. Two machines for in vitro propagation of plants in liquid media. Can J Plant Sci. 1983;63:311–316.
  • Etienne H, Berthouly M. Temporary immersion systems in plant micropropagation. Plant Cell Tiss Org Cult. 2002;69:215–231.
  • Steward FC, Caplin S, Millar FK. Investigations on growth and metabolism of plant cells. I. New techniques for the investigation of metabolism, nutrition and growth in undifferentiated cells. Ann Bot. 1952;16:57–77.
  • Teisson C, Alvard D, Lartaud M, et al. Temporary immersion for plant tissue culture. In: Plant Biotechnology and In vitro Biology in the 21st Century, Proceedings of the IXth International Congress of Plant Tissue and Cell Culture, Section H: Novel micropropagation methods. Jerusalem 1999, p. 629–632.
  • Latawa J, Shukla MR, Saxena PK. An efficient temporary immersion system for micropropagation of hybrid hazelnut. Botany. 2016;94:1–8.
  • Hui AV, Bhatt A, Sreeramanan S, et al. Establishment of a shoot proliferation protocol for banana (ABB group) cv. ‘Pisang Awak’ via temporary immersion system. J Plant Nut. 2013;36:529–538.
  • Pérez M, Bueno MA, Escalona M, et al. Temporary immersion systems (RITA®) for the improvement of cork oak somatic embryogenic culture proliferation and somatic embryo production. Trees. 2013;27:1277–1284.
  • Florez SL, Curtis MS, Shaw SE, et al. A temporary immersion plant propagation bioreactor with decoupled gas and liquid flows for enhanced control of gas phase. Biotechnol Progress. 2016;32:337–345.
  • Jimenez E, Perez N, Feria M, et al. Improved Production of potato microtubers using a temporary immersion system. Plant Cell Tiss Org Cult. 1999;59:19–23.
  • Jova MC, Kosky RG, Perez M, et al. Production of Yam microtubers using a temporary immersion system. Plant Cell Tiss Organ Cult. 2005;83:103–107.
  • Georgiev V, Schumann A, Pavlov A, et al. Temporary immersion systems in plant biotechnology. Eng Life Sci. 2014;14:607–621.
  • Welander M, Persson J, Asp H, et al. Evaluation of a new vessel system based on temporary immersion system for micropropagation. Sci Hortic. 2014;179:227–232.
  • Landey RB, Cenci A, Georget F, et al. High genetic and epigenetic stability in Coffea arabica plants derived from embryogenic suspensions and secondary embryogenesis as revealed by AFLP, MSAP and the phenotypic variation rate. PLoS One. 2013;8:e56372.
  • Mallón R, Covelo P, Vieitez AM. Improving secondary embryogenesis in Quercus robur: Application of temporary immersion for mass propagation. Trees Struct Funct. 2012;26:731–741.
  • Hua HW, Huang TD, Huang HS. Micropropagation of self-rooting juvenile clones by secondary somatic embryogenesis in Hevea brasiliensis. Plant Breed. 2010;129:202–207.
  • Goel MK, Kukreja AK, Bisht NS. In vitro manipulations in St. John’s wort (Hypericum perforatum L.) for incessant and scale up micropropagation using adventitious roots in liquid medium and assessment of clonal fidelity using RAPD analysis. Plant Cell Tiss Organ Cult. 2009;96:1–9.
  • Martínez-Estrada M, Caamal-Velázquez JH, Salinas-Ruíz J, et al. Assessment of somaclonal variation during sugarcane micropropagation in temporary immersion bioreactors by intersimple sequence repeat (ISSR) markers. In Vitro Celldevbiol-Plant. 2017;53:553–560.
  • Krishna H, Alizadeh M, Singh D, et al. Somaclonal variations and their applications in horticultural crops improvement. 3 Biotech. 2016;6:54.
  • Slazak B, Sliwinska E, Saługa M, et al. Micropropagation of Viola uliginosa (Violaceae) for endangered species conservation and for somaclonal variation-enhanced cyclotide biosynthesis. Plant Cell Tiss Organ Cult. 2015;120:179–190.
  • Gómez D, Hernández L, Valle B, et al. Temporary immersion bioreactors (TIB) provide a versatile, cost-effective and reproducible in vitro analysis of the response of pineapple shoots to salinity and drought. Acta Physiol Plant. 2017;39:277.
  • Zhao J, Li ZT, Cui J, et al. Efficient somatic embryogenesis and Agrobacterium-mediated transformation of pothos (Epipremnum aureum) ‘Jade’. Plant Cell Tiss Organ Cult. 2013;114:237–247.
  • Pathi KM, Tula S, Tuteja N. High frequency regeneration via direct somatic embryogenesis and efficient Agrobacterium-mediated genetic transformation of tobacco. Plant Signal Behav. 2013;8:e24354.
  • Nyaboga EN, Njiru JM, Tripathi L. Factors influencing somatic embryogenesis, regeneration, and Agrobacterium-mediated transformation of cassava (Manihot esculenta Crantz) cultivar TME14. Front Plant Sci. 2015;6:411.
  • Smertenko A, Bozhkov PV. Somatic embryogenesis: life and death processes during apical–basal patterning. J Exp Bot. 2014;65:1343–1360.
  • Quainoo AK, Dwomon IB. The effect of abscisic acid in the conversion of cocoa somatic embryos into plantlets. Front Sci. 2012;2:6–10.102.
  • Viaene T, Landberg K, Thelander M, et al. Directional auxin transport mechanisms in early diverging land plants. Curr Biol. 2014;24:2786–2791.
  • Campos NA, Panis B, Carpentier SC. Somatic embryogenesis in coffee: The evolution of biotechnology and the integration of omics technologies offer great opportunities. Front Plant Sci. 2017;8:1460.
  • Ghoshdastidar AJ, Tong AZ. Treatment of 2,4-D, mecoprop, and dicamba using membrane bioreactor technology. Environ Sci Pollut Res Int. 2013;20:5188–5197.
  • Laere E, Ling APK, Wong YP, et al. Plant-based vaccines: Production and challenges. J Bot. 2016;2016:1.
  • Ganapathy M. Plants as bioreactors- A review. Adv Tech Biol Med. 2016;4:1000161.
  • Yan N, Fan C, Chen Y, et al. The potential for microalgae as bioreactors to produce pharmaceuticals. Int J Mol Sci. 2016;17:E962.
  • Hirschl S, Ralser C, Asam C, et al. Expression and characterization of functional recombinant Bet v 1.0101 in the chloroplast of Chlamydomonas reinhardtii. Int Arch Allergy Immunol. 2017;173:44–50.
  • Stiles AR, Liu CZ. Hairy root culture: bioreactor design and process intensification. Adv Biochem Eng Biotechnol. 2013;134:91–114.
  • Mishra BN, Ranjan R. Growth of hairy-root cultures in various bioreactors for the production of secondary metabolites. Biotechnol Appl Biochem. 2008;49:1–10.
  • Jaremicz Z, Luczkiewicz M, Kokotkiewicz A, et al. Production of tropane alkaloids in Hyoscyamus niger (black henbane) hairy roots grown in bubble-column and spray bioreactors. Biotechnol Lett. 2014;36:843–853.
  • Cao Q, Xiang T, Meng S, et al. Genetic stability analysis of exogenous gene in long-term cultured cucumber hairy roots. Acta Hort Sin. 2012;39:1589–1598.
  • Mankin SL, Hill DS, Olhoft PM, et al. Disarming and sequencing of Agrobacterium rhizogenes strain K599 (NCPPB2659) plasmid pRi2659. In Vitro Cell Dev. Biol. Plant. 2007;43:521–535.
  • Gerszberg A, Hnatuszko-Konka K, Kowalczyk T, et al. Tomato (Solanum lycopersicum L.) in the service of biotechnology. Plant Cell Tiss Organ Cult. 2015;120:881–902.
  • Du S, Xiang T, Song Y, et al. Transgenic hairy roots of Tetrastigma hemsleyanum: induction, propagation, genetic characteristics and medicinal components. Plant Cell Tiss Organ Cult. 2015;122:373–382.
  • Shiao TI, Ellis MH, Dolferus R, et al. Overexpression of alcohol dehydrogenase or pyruvate decarboxylase improves growth of hairy roots at reduced oxygen concentrations. Biotechnol Bioeng. 2002;77:455–461.
  • Gantait S, Kundu S, Ali N, et al. Synthetic seed production of medicinal plants: a review on influence of explants, encapsulation agent and matrix. Acta Physiol Plant. 2015;37:98.
  • Micheli M, Bececco V, Gardi T, et al. Encapsulation of black mulberry microcuttings: studies on capsules and synthetic seeds. Acta Hortic. 2017;1155:65–70.
  • Gomes F, Clemente M, Figueiredo P, et al. Castanea spp. hybrid clones in vitro conservation: synthetic seeds vs. slow growth storage. Acta Hortic. 2017;1155:37–44.
  • Attree SM, Pomeroy MK, Fowke LC. Production of vigorous, desiccation tolerant white spruce (Picea glauca [Moench.] Voss.) synthetic seeds in a bioreactor. Plant Cell Rep. 1994;13:601–606.
  • Lata H, Chandra S, Khan IA, et al. Cannabis sativa L. micropropagation in temporary immersion bioreactor system. Planta Med. 2010;76:76–P9.
  • Hohe A, Reski R. Optimisation of a bioreactor culture of the moss Physcomitrella patens for mass production of protoplasts. Plant Sci. 2002;163:69–74.
  • Etienne H, Dechamp E, Barry-Etienne D, et al. Bioreactors in coffee micropropagation. Braz J Plant Physiol. 2006;18:45–54.
  • Lai CC, Lin HM, Nalawade SM, et al. Hyperhydricity in shoot cultures of Scrophularia yoshimurae can be effectively reduced by ventilation of culture vessels. J Plant Physiol. 2005;162:355–361.
  • Machado MP, da Silva ALP, Biasi LA, et al. Influence of calcium content of tissue on hyperhydricity and shoot-tip necrosis of in vitro regenerated shoots of Lavandula angustifolia Mill. Braz Arch Biol Technol. 2014;57:636–643.
  • Saldanha CW, Otoni CG, Rocha DI, et al. CO2-enriched atmosphere and supporting material impact the growth, morphophysiology and ultrastructure of in vitro Brazilian-ginseng [Pfaffia glomerata (Spreng.) Pedersen] plantlets. Plant Cell Tiss Organ Cult. 2014;118:87–99.
  • Kliphuis AMJ, Martens DE, Janssen M, et al. Effect of O2:CO2 ratio on the primary metabolism of Chlamydomonas reinhardtii. Biotechnol Bioeng. 2011;108:2390–2402.
  • Giusti S, Mazzei D, Cacopardo L, et al. Environmental control in flow bioreactors. Processes. 2017;5:16.
  • Yuk IH, Baskar D, Duffy PH, et al. Overcoming challenges in WAVE bioreactors without feedback controls for pH and dissolved oxygen. Biotechnol Progress. 2011;27:1397–1406.
  • Cardarelli M, Cardona Suárez CM. Influence of ozone treatments on in vitro propagation of Lilium in bioreactor. Acta Hortic. 2017;1155:381–386.
  • Lauridsen H, Hansen K, Nørgård MØ, et al. From tissue to silicon to plastic: three-dimensional printing in comparative anatomy and physiology. R Soc Open Sci. 2016;3:150643
  • Weyand B, Nöhre M, Schmälzlin E, et al. Noninvasive oxygen monitoring in three-dimensional tissue cultures under static and dynamic culture conditions. Biores Open Access. 2015;4:266–277.
  • Schmälzlin E, van Dongen JT, Klimant I, et al. An optical multifrequency phase-modulation method using microbeads for measuring intracellular oxygen concentrations in plants. Biophys J. 2005;89:1339–1345.
  • Ast C, Schmälzlin E, Löhmannsröben HG, et al. Optical oxygen micro- and nanosensors for plant applications. Sensors (Basel). 2012;12:7015–7032.
  • Zabalza A, van Dongen JT, Froehlich A, et al. Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiol. 2009;149:1087–1098.
  • Thibeaux R, Perrin E, Smaniotto B, et al. Using X-ray computed tomography for quantification of cell proliferation within a perfusion bioreactor. Comput Methods Biomech Biomed Eng. 2015;18:2072–2073.
  • Staedler YM, Masson D, Schönenberger J. Plant tissues in 3D via X-ray tomography: Simple contrasting methods allow high-resolution imaging. PLoS One. 2013;8:e75295. 2013
  • Karunakaran C, Lahlali R, Zhu N, et al. Factors influencing real time internal structural visualization and dynamic process monitoring in plants using synchrotron-based phase contrast X-ray imaging. Sci Rep. 2015;5:12119.
  • Zermatten E, Vetsch JR, Ruffoni D, et al. Micro-computed tomography based computational fluid dynamics for the determination of shear stresses in scaffolds within a perfusion bioreactor. Ann Biomed Eng. 2014;42:1085–1094.
  • Teixeria da Silva JA, Dobránszki J. Plant thin cell layers: update and perspectives. Folia Hort. 2015;27:183–190.
  • Teixeira da Silva JA. The role of thin cell layers in regeneration and transformation in orchids. Plant Cell Tiss Organ Cult. 2013;113:149–161.
  • Chapman LAC, Whiteley JP, Byrne HM, et al. Mathematical modelling of cell layer growth in a hollow fibre bioreactor. J Theor Biol. 2017;418:36–56.
  • Seviour RJ, McNeil B, Fazenda ML, et al. Operating bioreactors for microbial exopolysaccharide production. Critic Rev Biotechnol. 2011;31:170–185.
  • Schmid J, Sieber V, Rehm B. Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front Microbiol. 2015;6:496.
  • Mahboubi A, Ylitervo P, Doyen W, et al. Reverse membrane bioreactor: Introduction to a new technology for biofuel production. Biotechnol Adv. 2016; 34:954–975.
  • Erland LAE, Saxena PK. Melatonin natural health products and supplements: Presence of serotonin and significant variability of melatonin content. J Clin Sleep Med. 2017;13:275–281.
  • Erland LAE, Murch SJ, Reiter RJ, et al. A new balancing act: The many roles of melatonin and serotonin in plant growth and development. Plant Signal Behav. 2015;10:e1096469
  • Verma P, Sharma A, Ahmad Khan S, et al. Over-expression of Catharanthus roseus tryptophan decarboxylase and strictosidine synthase in rol gene integrated transgenic cell suspensions of Vinca minor. Protoplasma. 2015;252:373–381.
  • Jones AMP, Saxena PK, Murch SJ. Elicitation of secondary metabolism in Echinacea purpurea L. by gibberellic acid and triazoles. Eng Life Sci. 2009;9:205–210.
  • Talei D, Valdiani A, Maziah M, et al. Analysis of the anticancer phytochemicals in Andrographis paniculata Nees. under salinity stress. Biomed Res Int. 2013;2013:1.
  • Rosnow J, Offermann S, Park J, et al. In vitro cultures and regeneration of Bienertia sinuspersici (Chenopodiaceae) under increasing concentrations of sodium chloride and carbon dioxide. Plant Cell Rep. 2011;30:1541–1553.
  • Khattak MSK, Abiri R, Valdiani A, et al. Somatic embryogenesis and in-vitro regeneration of rice (Oryza sativa L.) cultivars under one-step and multiple-step salinity stresses. J Plant Breed Genet. 2017;5:99–111.
  • Yogalakshmi KN, Joseph K. Effect of transient sodium chloride shock loads on the performance of submerged membrane bioreactor. Biores Technol. 2010;101:7054–7061.
  • Wang J, Pathak N, Chekli L, et al. Performance of a novel fertilizer-drawn forward osmosis aerobic membrane bioreactor (FDFO-MBR): Mitigating salinity build-up by integrating microfiltration. Water. 2017;9:21.
  • Bosio VE, Islan GA, Martínez YN, et al. Nanodevices for the immobilization of therapeutic enzymes. Crit Rev Biotechnol. 2016;36:447–464.
  • Lopez-Ponnada EV, Lynn TJ, Peterson M, et al. Application of denitrifying wood chip bioreactors for management of residential non-point sources of nitrogen. J Biol Eng. 2017;11:16.

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