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Rice cell suspension culture as a model for producing high-value recombinant proteins and plant specialized metabolites

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Abstract

Rice cell suspension culture (RCSC) is one of the most widely studied plant cell culture systems next to tobacco and carrot. Simple cell culture techniques, scalability and high genetic transformation potential make RCSC an ideal platform to produce high-value recombinant proteins and plant specialized metabolites (PSM). Our understanding of the rice genome and its genetic regulation makes RCSC amenable to efficient genetic engineering with precision genome editing tools such as CRISPR/Cas. Further, the metabolic pool of RCSC can be harnessed and bioengineered to produce recombinant proteins and PSM. This review highlights the studies performed on transgenic RCSC and potential of this platform to synthesize PSM. Recent advancements in RCSC-mediated production and yield enhancement of bioactives using precision molecular biology tools such as CRISPR/Cas, media optimization and challenges associated with the establishment of RCSC are also summarized. This effort is to put the spotlight back on RCSC, which can become an attractive alternative to existing transgenic plant cell suspension culture systems.

Key Message

New developments in transgenic rice cell suspension culture and subsequent bioprocess optimization have potential to advance the field of plant-based biopharmaceutical production. Further use of precise genetic engineering tools can leverage the prospects of rice cell suspension culture for molecular pharming.

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References

  • Abe T, Futsuhara Y (1986) Genotypic variability for callus formation and plant regeneration in rice (Oryza sativa L.). Theor Appl Genet 72:3–10

    CAS  PubMed  Google Scholar 

  • Ahuja S, Roy A, Kumar L, Bharadvaja N (2019) Media optimization using Box Behnken design for enhanced production of biomass, beta-carotene and lipid from Dunaliella salina. Vegetos. https://doi.org/10.1007/s42535-019-00079-4

    Article  Google Scholar 

  • Anjum S, Anjum I, Hano C, Kousar S (2019) Advances in nanomaterials as novel elicitors of pharmacologically active plant specialized metabolites: current status and future outlooks. RSC Adv 9:40404–40423

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arya SS, Mahto BK, Ramkumar TR, Lenka SK (2020a) Sharpening gene editing toolbox in Arabidopsis for plants. J Plant Biochem Biotechnol 29(4):769–784

  • Arya SS, Rookes J, Cahill D, Lenka SK (2020b) Next-generation metabolic engineering approaches towards development of plant cell suspension cultures as specialized metabolite producing biofactories. Biotechnol Adv 45:107635

    CAS  PubMed  Google Scholar 

  • Baek S-H et al (2013) Creation of resveratrol-enriched rice for the treatment of metabolic syndrome and related diseases. PLoS ONE 8:e57930

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baltes NJ, Gil-Humanes J, Voytas DF (2017) Genome engineering and agriculture: opportunities and challenges. In: Weeks DP, Yang B (eds) Progress in molecular biology and translational science, vol 149. Elsevier, New York, pp 1–26

    Google Scholar 

  • Bang HB, Lee YH, Kim SC, Sung CK, Jeong KJ (2016) Metabolic engineering of Escherichia coli for the production of cinnamaldehyde. Microb Cell Fact 15:16

    PubMed  PubMed Central  Google Scholar 

  • Bhatacharya P, Pandey G, Mukherjee KJ (2007) Production and purification of recombinant human granulocyte–macrophage colony stimulating factor (GM-CSF) from high cell density cultures of Pichia pastoris. Bioprocess Biosyst Eng 30:305–312

    CAS  PubMed  Google Scholar 

  • Biswas SK, Kim D-E, Keum Y-S, Saini RK (2018) Metabolite profiling and antioxidant activities of white, red, and black rice (Oryza sativa L.) grains. J Food Meas Charact 12:2484–2492

    Google Scholar 

  • Bonnart R, Volk GM (2010) Increased efficiency using the encapsulation-dehydration cryopreservation technique for Arabidopsis thaliana. CryoLetters 31:95–100

    CAS  PubMed  Google Scholar 

  • Bovy A et al (2002) High-flavonol tomatoes resulting from the heterologous expression of the maize transcription factor genes LC and C1. Plant Cell 14:2509–2526

    CAS  PubMed  PubMed Central  Google Scholar 

  • Box GE, Behnken DW (1960) Some new three level designs for the study of quantitative variables. Technometrics 2:455–475

    Google Scholar 

  • Brown DJ, Beevers H (1987) Growth and respiration of rice (Oryza sativa L.) cells in suspension culture. Plant Cell Tiss Org Cult 10:175–186

    Google Scholar 

  • Butelli E et al (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol 26:1301

    CAS  PubMed  Google Scholar 

  • Caldana C, Scheible W-R, Mueller-Roeber B, Ruzicic S (2007) A quantitative RT-PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Methods 3:7

    PubMed  PubMed Central  Google Scholar 

  • Chandra S, Chakraborty N, Dasgupta A, Sarkar J, Panda K, Acharya K (2015) Chitosan nanoparticles: a positive modulator of innate immune responses in plants. Sci Rep 5:15195

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chee MJY, Lycett GW, Khoo T-J, Chin CF (2017) Bioengineering of the plant culture of Capsicum frutescens with vanillin synthase gene for the production of vanillin. Mol Biotechnol 59:1–8

    CAS  PubMed  Google Scholar 

  • Chen T-L, Lin Y-L, Lee Y-L, Yang N-S, Chan M-T (2004) Expression of bioactive human interferon-gamma in transgenic rice cell suspension cultures. Transgenic Res 13:499–510

    CAS  PubMed  Google Scholar 

  • Chen W et al (2013) A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: application in the study of rice metabolomics. Mol Plant 6:1769–1780

    CAS  PubMed  Google Scholar 

  • Chen L, Yang X, Luo D, Yu W (2016) Efficient production of a bioactive Bevacizumab monoclonal antibody using the 2A self-cleavage peptide in transgenic rice callus. Front Plant Sci 7:1156

    PubMed  PubMed Central  Google Scholar 

  • Cheon S-H, Lee K-H, Kwon J-Y, Choi S-H, Song M-N, Kim D-I (2009) Enhanced delivery of siRNA complexes by sonoporation in transgenic rice cell suspension cultures. J Microbiol Biotechnol 19:781–786

    CAS  PubMed  Google Scholar 

  • Cheon S, Lee K, Kwon J, Ryu H, Yu D, Choi Y, Kim D (2007) Effects of silkworm hemolymph on cell viability and hCTLA4Ig production in transgenic rice cell suspension cultures. J Microbiol Biotechnol 17:1944

    CAS  PubMed  Google Scholar 

  • Chih-Ching C, Ching-chu W, Ching-san S, Chen H, Kwang-chu Y, Chih C, Feng-yun B (1975) Establishment of an efficient medium for anther culture of rice through comparative experiments on the nitrogen sources. Sci Sin 18:659–668

    Google Scholar 

  • Choi H-Y et al (2018) N-glycan remodeling using mannosidase inhibitors to increase high-mannose glycans on acid α-glucosidase in transgenic rice cell cultures. Sci Rep 8:1–11

    Google Scholar 

  • Chronopoulou L, Donati L, Bramosanti M, Rosciani R, Palocci C, Pasqua G, Valletta A (2019) Microfluidic synthesis of methyl jasmonate-loaded PLGA nanocarriers as a new strategy to improve natural defenses in Vitis vinifera. Sci Rep 9:1–9

    Google Scholar 

  • Chung N-D et al (2014) Production of functional human vascular endothelial growth factor165 in transgenic rice cell suspension cultures. Enzyme Microb Technol 63:58–63

    CAS  PubMed  Google Scholar 

  • Corbin JM et al (2016) Semicontinuous bioreactor production of recombinant butyrylcholinesterase in transgenic rice cell suspension cultures. Front Plant Sci 7:412

    PubMed  PubMed Central  Google Scholar 

  • Corbin JM et al (2018) Purification, characterization, and N-glycosylation of recombinant butyrylcholinesterase from transgenic rice cell suspension cultures. Biotechnol Bioeng 115:1301–1310

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cornejo M-J, Luth D, Blankenship KM, Anderson OD, Blechl AE (1993) Activity of a maize ubiquitin promoter in transgenic rice. Plant Mol Biol 23:567–581

    CAS  PubMed  Google Scholar 

  • Cunningham FJ, Goh NS, Demirer GS, Matos JL, Landry MP (2018) Nanoparticle-mediated delivery towards advancing plant genetic engineering. Trends Biotechnol 36:882–897

    CAS  PubMed  Google Scholar 

  • Curtis WR, Emery AH (1993) Plant cell suspension culture rheology. Biotechnol Bioeng 42:520–526

    CAS  PubMed  Google Scholar 

  • Deshpande A, Dhadi SR, Hager EJ, Ramakrishna W (2012) Anticancer activity of rice callus suspension culture. Phytother Res 26:1075–1081

    PubMed  Google Scholar 

  • Ding J, Jia J, Yang L, Wen H, Zhang C, Liu W, Zhang D (2004) Validation of a rice specific gene, sucrose phosphate synthase, used as the endogenous reference gene for qualitative and real-time quantitative PCR detection of transgenes. J Agric Food Chem 52:3372–3377

    CAS  PubMed  Google Scholar 

  • Dong OX, Yu S, Jain R (2020) Marker-free carotenoid-enriched rice generated through targeted gene insertion using CRISPR-Cas9. Nat Commun 11:1178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Engqvist MK, Rabe KS (2019) Applications of protein engineering and directed evolution in plant research. Plant Physiol 179:907–917

    CAS  PubMed  PubMed Central  Google Scholar 

  • Facchini PJ et al (2012) Synthetic biosystems for the production of high-value plant metabolites. Trends Biotechnol 30:127–131

    CAS  PubMed  Google Scholar 

  • Fiedler U, Phillips J, Artsaenko O, Conrad U (1997) Optimization of scFv antibody production in transgenic plants. Immunotechnology 3:205–216

    CAS  PubMed  Google Scholar 

  • Fischer R, Emans N, Schuster F, Hellwig S, Drossard J (1999) Towards molecular farming in the future: using plant-cell-suspension cultures as bioreactors. Biotechnol Appl Biochem 30:109–112

    CAS  PubMed  Google Scholar 

  • Fischer R, Stoger E, Schillberg S, Christou P, Twyman RM (2004) Plant-based production of biopharmaceuticals. Curr Opin Plant Biol 7:152–158

    CAS  PubMed  Google Scholar 

  • Frank T, Reichardt B, Shu Q, Engel K-H (2012) Metabolite profiling of colored rice (Oryza sativa L.) grains. J Cereal Sci 55:112–119

    CAS  Google Scholar 

  • Fu R, Martin C, Zhang Y (2018) Next-generation plant metabolic engineering, inspired by an ancient Chinese irrigation system. Mol Plant 11:47–57

    CAS  PubMed  Google Scholar 

  • Galili G, Höfgen R (2002) Metabolic engineering of amino acids and storage proteins in plants. Metab Eng 4:3–11

    CAS  PubMed  Google Scholar 

  • Gallage NJ et al (2014) Vanillin formation from ferulic acid in Vanilla planifolia is catalysed by a single enzyme. Nat Commun 5:4037

    CAS  PubMed  Google Scholar 

  • Gamborg OLC, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158

    CAS  PubMed  Google Scholar 

  • Goddijn OJ, Pen J (1995) Plants as bioreactors. Trends Biotechnol 13:379–387

    CAS  Google Scholar 

  • Goldstein W, Ingle M, Lasure L (1980) Plant tissue culture as a source of biochemicals. CRC Press, Boca Raton, FL

    Google Scholar 

  • Grotewold E (2008) Transcription factors for predictive plant metabolic engineering: are we there yet? Curr Opin Biotechnol 19:138–144

    CAS  PubMed  Google Scholar 

  • Grotewold E et al (1998) Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. Plant Cell 10:721–740

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo B, Itami J, Oikawa K, Motoda Y, Kigawa T, Numata K (2019) Native protein delivery into rice callus using ionic complexes of protein and cell-penetrating peptides. PLoS ONE 14:e0214033

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo HS, Fei JF, Xie Q, Chua NH (2003) A chemical-regulated inducible RNAi system in plants. Plant J 34:383–392

    CAS  PubMed  Google Scholar 

  • Hayashi T, Ohsumi C, Kato Y, Yamanouchi H, Toriyama K, Hinata K (1994) Effects of amino acid medium on cell aggregation in suspension-cultured rice cells. Biosci Biotechnol Biochem 58:256–260

    CAS  Google Scholar 

  • Hellwig S, Drossard J, Twyman RM, Fischer R (2004) Plant cell cultures for the production of recombinant proteins. Nat Biotechnol 22:1415

    CAS  PubMed  Google Scholar 

  • Hong JK, Choi H-Y, Park H-R, Kim D-I, Lee D-Y (2019) Inhibition of autolysosome formation improves rrhGAA production driven by RAmy3D promoter in transgenic rice cell culture. Biotechnol Bioprocess Eng 24:568–578

    CAS  Google Scholar 

  • Hong S-Y, Kwon T-H, Jang Y-S, Kim S-H, Yang M-S (2006) Production of bioactive human granulocyte-colony stimulating factor in transgenic rice cell suspension cultures. Protein Expr Purif 47:68–73

    CAS  PubMed  Google Scholar 

  • Hong S-Y et al (2008) Tumor targeting of humanized fragment antibody secreted from transgenic rice cell suspension culture. Plant Mol Biol 68:413–422

    CAS  PubMed  Google Scholar 

  • Huang J et al (2001) Expression and purification of functional human α-1-antitrypsin from cultured plant cells. Biotechnol Prog 17:126–133

    CAS  PubMed  Google Scholar 

  • Huang J et al (2002) Expression of functional recombinant human lysozyme in transgenic rice cell culture. Transgenic Res 11:229–239

    CAS  PubMed  Google Scholar 

  • Huang L-F, Liu Y-K, Lu C-A, Hsieh S-L, Yu S-M (2005) Production of human serum albumin by sugar starvation induced promoter and rice cell culture. Transgenic Res 14:569–581

    CAS  PubMed  Google Scholar 

  • Huang L-F, Tan C-C, Yeh J-F, Liu H-Y, Liu Y-K, Ho S-L, Lu C-A (2015) Efficient secretion of recombinant proteins from rice suspension-cultured cells modulated by the choice of signal peptide. PLoS ONE 10:e0140812

    PubMed  PubMed Central  Google Scholar 

  • Huang N, Chandler J, Thomas BR, Koizumi N, Rodriguez RL (1993) Metabolic regulation of α-amylase gene expression in transgenic cell cultures of rice (Oryza sativa L.). Plant Mol Biol 23:737–747

    CAS  PubMed  Google Scholar 

  • Huang T-K, McDonald KA (2009) Bioreactor engineering for recombinant protein production in plant cell suspension cultures. Biochem Eng J 45:168–184

    CAS  Google Scholar 

  • Huang T-K, McDonald KA (2012) Bioreactor systems for in vitro production of foreign proteins using plant cell cultures. Biotechnol Adv 30:398–409

    CAS  PubMed  Google Scholar 

  • Islam MR, Kim N-S, Jung J-W, Kim H-B, Han S-C, Yang M-S (2018) Spontaneous pepsin C-catalyzed activation of human pepsinogen C in transgenic rice cell suspension culture: Production and characterization of human pepsin C. Enzyme Microb Technol 108:66–73

    CAS  PubMed  Google Scholar 

  • Iwamoto M, Higo H, Higo K (2004) Strong expression of the rice catalase gene CatB promoter in protoplasts and roots of both a monocot and dicots. Plant Physiol Biochem 42:241–249

    CAS  PubMed  Google Scholar 

  • Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651

    CAS  PubMed  Google Scholar 

  • James E, Lee JM (2006) Loss and recovery of protein productivity in genetically modified plant cell lines. Plant Cell Rep 25:723–727

    CAS  PubMed  Google Scholar 

  • Joersbo M, Brunstedt J (1990) Direct gene transfer to plant protoplasts by mild sonication. Plant Cell Rep 9:207–210

    CAS  PubMed  Google Scholar 

  • Joo S-Y, Lee K-H, Lee Y-I, Kim D-I (2006) Enhanced production of hGM-CSF by medium exchange in transgenic Oryza sativa L. suspension cultures. Enzyme Microb Technol 39:486–489

    CAS  Google Scholar 

  • Jung J-W, Huy N-X, Kim H-B, Kim N-S, Yang M-S (2017) Production of recombinant human acid α-glucosidase with high-mannose glycans in gnt1 rice for the treatment of Pompe disease. J Biotechnol 249:42–50

    CAS  PubMed  Google Scholar 

  • Jung J-W, Kim N-S (2019) Production of functional recombinant cyclic citrullinated peptide monoclonal antibody in transgenic rice cell suspension culture. Transgenic Res 28:177–188

    PubMed  Google Scholar 

  • Jung J-W, Kim N-S, Jang S-H, Shin Y-J, Yang M-S (2016) Production and characterization of recombinant human acid α-glucosidase in transgenic rice cell suspension culture. J Biotechnol 226:44–53

    CAS  PubMed  Google Scholar 

  • Kang S-H, Choi H-Y, Cho J-S, Cheon S-H, Kim J-Y, Kim BB, Kim D-I (2018) Assessment of recovery medium for production of hCTLA4Ig after cryopreservation in transgenic rice cells. Biotechnol Bioprocess Eng 23:218–227

    CAS  Google Scholar 

  • Kargi F, Rosenberg MZ (1987) Plant cell bioreactors: present status and future trends. Biotechnol Prog 3:1–8

    CAS  Google Scholar 

  • Kato Y, Yamanouchi H, Hinata K, Ohsumi C, Hayashi T (1994) Involvement of phenolic esters in cell aggregation of suspension-cultured rice cells. Plant Physiol 104:147–152

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim B-G et al (2014a) Production of monoclonal antibody against FimA protein from Porphyromonas gingivalis in rice cell suspension culture. Plant Cell Tiss Org Cult 118:293–304

    CAS  Google Scholar 

  • Kim B-R, Nam H-Y, Kim S-U, Kim S-I, Chang Y-J (2003) Normalization of reverse transcription quantitative-PCR with housekeeping genes in rice. Biotechnol Lett 25:1869–1872

    CAS  PubMed  Google Scholar 

  • Kim J et al (2020) Profiles of plant core-fucosylated N-glycans of acid alpha-glucosidases produced in transgenic rice cell suspension cultures treated with eight different conditions. Enzyme Microb Technol 134:109482

    CAS  PubMed  Google Scholar 

  • Kim M-S, Nam H-J, Kim M-S, Kwon J-Y, Kim D-I (2013a) Enhanced production of hCTLA4Ig by suppressing cell death in transgenic rice cell suspension cultures. KSBB J 28:260–268

    Google Scholar 

  • Kim N-S, Jang S-H, Yu H-Y, Chung N-D, Kwon T-H, Yang M-S, Kim T-G (2013b) Amylase and cysteine proteinase gene knockdown in rice cells using RNA interference for enhancing production of recombinant proteins. Plant Cell Tiss Org Cult 114:97–107

    CAS  Google Scholar 

  • Kim N-S, Kim T-G, Jang Y-S, Shin Y-J, Kwon T-H, Yang M-S (2008a) Amylase gene silencing by RNA interference improves recombinant hGM-CSF production in rice suspension culture. Plant Mol Biol 68:369–377

    CAS  PubMed  Google Scholar 

  • Kim N-S et al (2008b) Improvement of recombinant hGM-CSF production by suppression of cysteine proteinase gene expression using RNA interference in a transgenic rice culture. Plant Mol Biol 68:263

    CAS  PubMed  Google Scholar 

  • Kim N-S, Yu H-Y, Chung N-D, Kwon T-H, Yang M-S (2014b) High-level production of recombinant trypsin in transgenic rice cell culture through utilization of an alternative carbon source and recycling system. Enzyme Microb Technol 63:21–27

    CAS  PubMed  Google Scholar 

  • Kim N-S, Yu H-Y, Chung N-D, Shin Y-J, Kwon T-H, Yang M-S (2011) Production of functional recombinant bovine trypsin in transgenic rice cell suspension cultures. Protein Expr Purif 76:121–126

    CAS  PubMed  Google Scholar 

  • Kim T-G, Kim B-G, Jeong D-K, Jang Y-S, Lee J-Y, Yang M-S (2012) Production of monoclonal antibodies against the FimA protein of Porphyromonas gingivalis in Nicotiana benthamiana. Biotechnol Bioprocess Eng 17:420–426

    CAS  Google Scholar 

  • Kim T-G, Baek M-Y, Lee E-K, Kwon T-H, Yang M-S (2008c) Expression of human growth hormone in transgenic rice cell suspension culture. Plant Cell Rep 27:885–891

    CAS  PubMed  Google Scholar 

  • Kim T-G, Yang M-S, Moon J-H, Lee J-Y (2016a) Production of monoclonal antibodies against 53-kDa protein of Porphyromonas gingivalis in transgenic rice cell suspension culture. Plant Cell Tiss Org Cult 126:387–397

    CAS  Google Scholar 

  • Kim Z-H et al (2016b) Evaluation of the wound-healing activity of rice cell extracts in vitro. Microbiol Biotechnol Lett 44:285–292

    CAS  Google Scholar 

  • Kizhner T, Azulay Y, Hainrichson M, Tekoah Y, Arvatz G, Shulman A, Ruderfer I, Aviezer D, Shaaltiel Y (2015) Characterization of a chemically modified plant cell culture expressed human α-Galactosidase-A enzyme for treatment of Fabry disease. Mol Genet Metab 114:259–267

    CAS  PubMed  Google Scholar 

  • Klimek-Chodacka M, Oleszkiewicz T, Lowder LG, Qi Y, Baranski R (2018) Efficient CRISPR/Cas9-based genome editing in carrot cells. Plant Cell Rep 37:575–586

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kolewe ME, Henson MA, Roberts SC (2011) Analysis of aggregate size as a process variable affecting paclitaxel accumulation in Taxus suspension cultures. Biotechnol Prog 27:1365–1372

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kozera B, Rapacz M (2013) Reference genes in real-time PCR. J Appl Genet 54:391–406

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar N, Pruthi V (2014) Potential applications of ferulic acid from natural sources. Biotechnol Rep 4:86–93

    CAS  Google Scholar 

  • Kumar P, Augustine R, Singh AK, Bisht NC (2017) Feeding behaviour of generalist pests on Brassica juncea: implication for manipulation of glucosinolate biosynthesis pathway for enhanced resistance. Plant Cell Environ 40:2109–2120

    CAS  PubMed  Google Scholar 

  • Kuo YC, Tan CC, Ku JT, Hsu WC, Su SC, Lu CA, Huang LF (2013) Improving pharmaceutical protein production in Oryza sativa. Int J Mol Sci 14:8719–8739

    PubMed  PubMed Central  Google Scholar 

  • Kwon J-Y, Cheon S-H, Nam H-J, Choi H-Y, Kim D-I (2013a) Process characterization of hCTLA4Ig production in transgenic rice cell cultures using a 3-L bioreactor. Appl Biochem Biotechnol 171:1276–1288

    CAS  PubMed  Google Scholar 

  • Kwon J-Y, Jeong S-H, Choi J-W, Pak Y-Y, Kim D-I (2013b) Assessment of long-term cryopreservation for production of hCTLA4Ig in transgenic rice cell suspension cultures. Enzyme Microb Technol 53:216–222

    CAS  PubMed  Google Scholar 

  • Kwon J-Y, Lee K-H, Cheon S-H, Kim D-I (2012) Application of anoxia with glucose addition for the enhanced production of hCTLA4Ig in transgenic rice suspension cell cultures. Enzyme Microb Technol 50:298–303

    CAS  PubMed  Google Scholar 

  • Kwon JY, Yang YS, Cheon SH, Nam HJ, Jin GH, Kim DI (2013c) Bioreactor engineering using disposable technology for enhanced production of hCTLA4Ig in transgenic rice cell cultures. Biotechnol Bioeng 110:2412–2424

    CAS  PubMed  Google Scholar 

  • Kyozuka J, Fujimoto H, Izawa T, Shimamoto K (1991) Anaerobic induction and tissue-specific expression of maize Adh1 promoter in transgenic rice plants and their progeny. Mol Gen Genet 228:40–48

    CAS  PubMed  Google Scholar 

  • Lee H, Kim D, Lim S-M, Kwon S (2017) Rice callus extracts for enhancing skin wound healing. Biotechnol Bioprocess Eng 22:352–358

    CAS  Google Scholar 

  • Lee S-J et al (2007) Production and characterization of human CTLA4Ig expressed in transgenic rice cell suspension cultures. Protein Expr Purif 51:293–302

    CAS  PubMed  Google Scholar 

  • Lee T-J, Shultz RW, Hanley-Bowdoin L, Thompson WF (2004) Establishment of rapidly proliferating rice cell suspension culture and its characterization by fluorescence-activated cell sorting analysis. Plant Mol Biol Rep 22:259–267

    CAS  Google Scholar 

  • Lenka SK, Boutaoui N, Paulose B, Vongpaseuth K, Normanly J, Roberts SC, Walker EL (2012) Identification and expression analysis of methyl jasmonate responsive ESTs in paclitaxel producing Taxus cuspidata suspension culture cells. BMC Genomics 13:148

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lenka SK, Nims NE, Vongpaseuth K, Boshar RA, Roberts SC, Walker EL (2015) Jasmonate-responsive expression of paclitaxel biosynthesis genes in Taxus cuspidata cultured cells is negatively regulated by the bHLH transcription factors TcJAMYC1, TcJAMYC2, and TcJAMYC4. Front Plant Sci 6:115

    PubMed  PubMed Central  Google Scholar 

  • Li J et al (2016) Gene replacements and insertions in rice by intron targeting using CRISPR–Cas9. Nat Plants 2:16139

    CAS  PubMed  Google Scholar 

  • Li Q-F, Sun SS, Yuan D-Y, Yu H-X, Gu M-H, Liu Q-Q (2010) Validation of candidate reference genes for the accurate normalization of real-time quantitative RT-PCR data in rice during seed development. Plant Mol Biol Rep 28:49

    Google Scholar 

  • Li Y-F, Zhu R, Xu P (2005) Activation of the gene promoter of barley β-1, 3-glucanase isoenzyme GIII is salicylic acid (SA)-dependent in transgenic rice plants. J Plant Res 118:215–221

    CAS  PubMed  Google Scholar 

  • Lin Z et al (2017) Metabolomic analysis of pathways related to rice grain chalkiness by a notched-belly mutant with high occurrence of white-belly grains. BMC Plant Biol 17:39

    PubMed  PubMed Central  Google Scholar 

  • Linsmaier EM, Skoog F (1965) Organic growth factor requirements of tobacco tissue cultures. Physiol Plant 18:100–127

    CAS  Google Scholar 

  • Liu L, Shao Z, Zhang M, Wang Q (2015a) Regulation of carotenoid metabolism in tomato. Mol Plant 8:28–39

    CAS  PubMed  Google Scholar 

  • Liu Y-K, Li Y-T, Lu C-F, Huang L-F (2015b) Enhancement of recombinant human serum albumin in transgenic rice cell culture system by cultivation strategy. N Biotechnol 32:328–334

    CAS  PubMed  Google Scholar 

  • Liu Y-K, Lu C-W, Chang J-Y, Lu C-F, Tan C-C, Huang L-F (2018) Optimization of the culture medium for recombinant protein production under the control of the αAmy3 promoter in a rice suspension-cultured cell expression system. Plant Cell Tiss Organ Cult 132:383–391

    CAS  Google Scholar 

  • Liu Y, Yang H, Sakanishi A (2006) Ultrasound: mechanical gene transfer into plant cells by sonoporation. Biotechnol Adv 24:1–16

    CAS  PubMed  Google Scholar 

  • Lu X, Tang K, Li P (2016) Plant metabolic engineering strategies for the production of pharmaceutical terpenoids. Front Plant Sci 7:1647

    PubMed  PubMed Central  Google Scholar 

  • Lue M-Y, Lee H (1994) Protein phosphatase inhibitors enhance the expression of an α-amylase gene, αAmy3, in cultured rice cells. Biochem Biophys Res Commun 205:807–816

    CAS  PubMed  Google Scholar 

  • Luo J et al (2008) AtMYB12 regulates caffeoyl quinic acid and flavonol synthesis in tomato: expression in fruit results in very high levels of both types of polyphenol. Plant J 56:316–326

    CAS  PubMed  Google Scholar 

  • Macharoen K, Du M, McDonald KA, Nandi S (2019) Simplified lab scale and pilot scale bioreactor processes for recombinant butyrylcholinesterase production in transgenic rice cell suspension cultures. In: 2019 AIChE Annual Meeting. AIChE

  • Manela N et al (2015) Phenylalanine and tyrosine levels are rate-limiting factors in production of health promoting metabolites in Vitis vinifera cv. Gamay Red cell suspension. Front Plant Sci 6:538

    PubMed  PubMed Central  Google Scholar 

  • Mansoor S, Amin I, Hussain M, Zafar Y, Briddon RW (2006) Engineering novel traits in plants through RNA interference. Trends Plant Sci 11:559–565

    CAS  PubMed  Google Scholar 

  • McDonald KA, Hong LM, Trombly DM, Xie Q, Jackman AP (2005) Production of human α-1-antitrypsin from transgenic rice cell culture in a membrane bioreactor. Biotechnol Prog 21:728–734

    CAS  PubMed  Google Scholar 

  • McElroy D, Wu R (1997) Rice actin gene and promoter. U.S. Patent

  • McElroy D, Zhang W, Cao J, Wu R (1990) Isolation of an efficient actin promoter for use in rice transformation. Plant Cell 2:163–171

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mehrtens F, Kranz H, Bednarek P, Weisshaar B (2005) The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol 138:1083–1096

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mercx S, Tollet J, Magy B, Navarre C, Boutry M (2016) Gene inactivation by CRISPR-Cas9 in Nicotiana tabacum BY-2 suspension cells. Front Plant Sci 7:40

    PubMed  PubMed Central  Google Scholar 

  • Miki D, Shimamoto K (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol 45:490–495

    CAS  PubMed  Google Scholar 

  • Mishra R, Joshi RK, Zhao K (2018) Genome editing in rice: Recent advances, challenges, and future implications. Front Plant Sci 9:1361

    PubMed  PubMed Central  Google Scholar 

  • Mitsuhara I et al (1996) Efficient promoter cassettes for enhanced expression of foreign genes in dicotyledonous and monocotyledonous plants. Plant Cell Physiol 37:49–59

    CAS  PubMed  Google Scholar 

  • Moon KB, Park JS, Park YI, Song IJ, Lee HJ, Cho HS, Jeon JH, Kim HS (2020) Development of systems for the production of plant-derived biopharmaceuticals. Plants 1:30

    Google Scholar 

  • Mordor-Intelligence (2019) Bioparmaceuticals market—growth, treands, and forcast (2020–2025)

  • Müller AJ, Grafe R (1978) Isolation and characterization of cell lines of Nicotiana tabacum lacking nitrate reductase. Mol Gen Genet 161:67–76

    Google Scholar 

  • Müller E, Lörz H, Lütticke S (1996) Variability of transgene expression in clonal cell lines of wheat. Plant Sci 114:71–82

    Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    CAS  Google Scholar 

  • Mustafa NR, De Winter W, Van Iren F, Verpoorte R (2011) Initiation, growth and cryopreservation of plant cell suspension cultures. Nat Protoc 6:715–742

    CAS  PubMed  Google Scholar 

  • Nam H-J, Kwon J-Y, Choi H-Y, Kang S-H, Jung H-S, Kim D-I (2017) Production and purification of recombinant glucocerebrosidase in transgenic rice cell suspension cultures. Appl Biochem Biotechnol 181:1401–1415

    CAS  PubMed  Google Scholar 

  • Nitzsche W (1980) One year storage of dried carrot callus. Z Pflanzenphysiol 100:269–271

    Google Scholar 

  • Nocarova E, Fischer L (2009) Cloning of transgenic tobacco BY-2 cells; an efficient method to analyse and reduce high natural heterogeneity of transgene expression. BMC Plant Biol 9:44

    PubMed  PubMed Central  Google Scholar 

  • Nordlund E et al (2018) Plant cells as food–a concept taking shape. Food Res Int 107:297–305

    CAS  PubMed  Google Scholar 

  • Nourbakhsh-Rey M, Libault M (2016) Decipher the molecular response of plant single cell types to environmental stresses. Biomed Res Int 2016:1–8

    Google Scholar 

  • O’Connor SE (2015) Engineering of secondary metabolism. Annu Rev Genet 49:71–94

    CAS  PubMed  Google Scholar 

  • Ohira K, Ojima K, Fujiwara A (1973) Studies on the nutrition of rice cell culture I. A simple, defined medium for rapid growth in suspension culture. Plant Cell Physiol 14:1113–1121

    CAS  Google Scholar 

  • Oliva M, Ovadia R, Perl A, Bar E, Lewinsohn E, Galili G, Oren-Shamir M (2015) Enhanced formation of aromatic amino acids increases fragrance without affecting flower longevity or pigmentation in Petunia× hybrida. Plant Biotechnol J 13:125–136

    CAS  PubMed  Google Scholar 

  • Orella MJ et al (2019) Lignin-KMC: a toolkit for simulating lignin biosynthesis. ACS Sustain Chem Eng 7(22):18313-18322

  • Owen C, Patron NJ, Huang A, Osbourn A (2017) Harnessing plant metabolic diversity. Curr Opin Chem Biol 40:24–30

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oyarce P et al (2019) Introducing curcumin biosynthesis in Arabidopsis enhances lignocellulosic biomass processing. Nat Plants 5:225

    CAS  PubMed  Google Scholar 

  • Page MT, Parry MA, Carmo-Silva E (2019) A high-throughput transient expression system for rice. Plant Cell Environ 42:2057–2064

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pan Q et al (2012) Overexpression of ORCA3 and G10H in Catharanthus roseus plants regulated alkaloid biosynthesis and metabolism revealed by NMR-metabolomics. PLoS ONE 7:e43038

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pandey A et al (2014) Co-expression of Arabidopsis transcription factor, At MYB 12, and soybean isoflavone synthase, Gm IFS 1, genes in tobacco leads to enhanced biosynthesis of isoflavones and flavonols resulting in osteoprotective activity. Plant Biotechnol J 12:69–80

    CAS  PubMed  Google Scholar 

  • Park C-I, Lee S-J, Kang S-H, Jung H-S, Kim D-I, Lim S-M (2010) Fed-batch cultivation of transgenic rice cells for the production of hCTLA4Ig using concentrated amino acids. Process Biochem 45:67–74

    CAS  Google Scholar 

  • Peled-Zehavi H, Oliva M, Xie Q, Tzin V, Oren-Shamir M, Aharoni A, Galili G (2015) Metabolic engineering of the phenylpropanoid and its primary, precursor pathway to enhance the flavor of fruits and the aroma of flowers. Bioengineering 2:204–212

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Hernández J, Martínez-Trujillo A, Nicasio-Torres P (2019) Optimization of active compounds production by interaction between nitrate and copper in Sphaeralcea angustifolia cell suspension using Response Surface Methodology. Plant Cell Tiss Organ Cult 136:407–413

    Google Scholar 

  • Phillips GC, Garda M (2019) Plant tissue culture media and practices: an overview. Vitro Cell Dev Biol Plant 55:242–257

    Google Scholar 

  • Rahman N, Dhadi SR, Deshpande A, Ramakrishna W (2016) Rice callus suspension culture inhibits growth of cell lines of multiple cancer types and induces apoptosis in lung cancer cell line. BMC Complement Altern Med 16:427

    PubMed  PubMed Central  Google Scholar 

  • Ramkumar TR, Lenka SK, Arya SS, Bansal KC (2020) A short history and perspectives on plant genetic transformation. In: Rustgi S, Luo H (eds) Biolistic DNA delivery in plants: methods and protocols. Springer, New York, pp 39–68. https://doi.org/10.1007/978-1-0716-0356-7_3

    Chapter  Google Scholar 

  • Rao SR, Ford KL, Cassin AM, Roessner U, Patterson JH, Bacic A (2010) Proteomic and metabolic profiling of rice suspension culture cells as a model to study abscisic acid signaling response pathways in plants. J Proteome Res 9:6623–6634

    CAS  PubMed  Google Scholar 

  • Ren Y-Y, West CA (1992) Elicitation of diterpene biosynthesis in rice (Oryza sativa L.) by chitin. Plant Physiol 99:1169–1178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ryu KH, Huang L, Kang HM, Schiefelbein J (2019) Single-cell RNA sequencing resolves molecular relationships among individual plant cells. Plant Physiol 179:1444–1456

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sakai M et al (2007) Production of 2-phenylethanol in roses as the dominant floral scent compound from L-phenylalanine by two key enzymes, a PLP-dependent decarboxylase and a phenylacetaldehyde reductase. Biosci Biotechnol Biochem 71:2408–2419

    CAS  PubMed  Google Scholar 

  • Santos RB, Abranches R, Fischer R, Sack M, Holland T (2016) Putting the spotlight back on plant suspension cultures. Front Plant Sci 7:297

    PubMed  PubMed Central  Google Scholar 

  • Secchi G (2008) Role of protein in cosmetics. Clin Dermatol 26:321–325

    PubMed  Google Scholar 

  • Shakya P, Marslin G, Siram K, Beerhues L, Franklin G (2019) Elicitation as a tool to improve the profiles of high-value secondary metabolites and pharmacological properties of Hypericum perforatum. J Pharm Pharmacol 71:70–82

    CAS  PubMed  Google Scholar 

  • Sheu J-J, Yu T-S, Tong W-F, Yu S-M (1996) Carbohydrate starvation stimulates differential expression of rice α-amylase genes that is modulated through complicated transcriptional and posttranscriptional processes. J Biol Chem 271:26998–27004

    CAS  PubMed  Google Scholar 

  • Shin YJ, Chong YJ, Yang MS, Kwon TH (2011) Production of recombinant human granulocyte macrophage-colony stimulating factor in rice cell suspension culture with a human-like N-glycan structure. Plant Biotechnol J 9:1109–1119

    CAS  PubMed  Google Scholar 

  • Shin YJ, Hong SY, Kwon TH, Jang YS, Yang MS (2003) High level of expression of recombinant human granulocyte-macrophage colony stimulating factor in transgenic rice cell suspension culture. Biotechnol Bioeng 82:778–783

    CAS  PubMed  Google Scholar 

  • Shoji T (2019) The recruitment model of metabolic evolution: jasmonate-responsive transcription factors and a conceptual model for the evolution of metabolic pathways. Front Plant Sci 10:560

    PubMed  PubMed Central  Google Scholar 

  • Sil B, Jha S (2014) Plants: the future pharmaceutical factory. Am J Plant Sci 5:319

    Google Scholar 

  • Su C-F, Kuo I-C, Chen P-W, Huang C-H, Seow SV, Chua KY, Yu S-M (2012) Characterization of an immunomodulatory Der p 2-FIP-fve fusion protein produced in transformed rice suspension cell culture. Transgenic Res 21:177–192

    CAS  PubMed  Google Scholar 

  • Su WW (2008) Bioreactor engineering for recombinant protein production using plant cell suspension culture. In: Dutta Gupta S, Ibaraki Y (eds) Plan tissue culture engineering. Springer, Dordrecht, pp 135–159

    Google Scholar 

  • Su WW, Lee KT (2007) Plant cell and hairy root cultures-Process characteristics, products, and applications. In: Yang ST (ed) Bioprocessing for value-added products from renewable resources. Elsevier, New York, pp 263–292

    Google Scholar 

  • Sun Q, Tsai S-L, Chen W (2019) Artificial scaffolds for enhanced biocatalysis. Methods Enzymol 617:363–383

    CAS  PubMed  Google Scholar 

  • Suprasanna P, Ganapathi T, Ramaswamy N, Surendranathan K, Rao P (1998) Aroma synthesis in cell and callus cultures of rice. Rice Genet News 15:123–125

    Google Scholar 

  • Takagi H et al (2005) A rice-based edible vaccine expressing multiple T cell epitopes induces oral tolerance for inhibition of Th2-mediated IgE responses. Proc Natl Acad Sci 102:17525–17530

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tekoah Y et al (2015) Large-scale production of pharmaceutical proteins in plant cell culture-the protalix experience. Plant Biotechnol J 13:1199–1208

    CAS  PubMed  Google Scholar 

  • Terada R, Shimamoto K (1990) Expression of CaMV35S-GUS gene in transgenic rice plants. Mol Gen Genet 220:389–392

    CAS  Google Scholar 

  • Terashima M, Murai Y, Kawamura M, Nakanishi S, Stoltz T, Chen L, Drohan W, Rodriguez RL, Katoh S (1999) Production of functional human α1-antitrypsin by plant cell culture. Appl Microbiol Biotechnol 52:516–523

    CAS  PubMed  Google Scholar 

  • Terashima M, Ejiri Y, Hashikawa N, Yoshida H (2000) Effects of sugar concentration on recombinant human α1-antitrypsin production by genetically engineered rice cell. Biochem Eng J 6:201–205

    CAS  PubMed  Google Scholar 

  • Thilmony R, Guttman M, Thomson JG, Blechl AE (2009) The LP2 leucine-rich repeat receptor kinase gene promoter directs organ-specific, light-responsive expression in transgenic rice. Plant Biotechnol J 7:867–882

    CAS  PubMed  Google Scholar 

  • Toriyama K, Hinata K (1985) Cell suspension and protoplast culture in rice. Plant Sci 41:179–183

    CAS  Google Scholar 

  • Torres E et al (1999) Rice cell culture as an alternative production system for functional diagnostic and therapeutic antibodies. Transgenic Res 8:441–449

    CAS  PubMed  Google Scholar 

  • Trexler MM, McDonald KA, Jackman AP (2005) A cyclical semicontinuous process for production of human α1-antitrypsin using metabolically induced plant cell suspension cultures. Biotechnol Prog 21:321–328

    CAS  PubMed  Google Scholar 

  • Tulecke W, Nickell LG (1959) Production of large amounts of plant tissue by submerged culture. Science 130:863–864

    CAS  PubMed  Google Scholar 

  • Tzin V, Malitsky S, Aharoni A, Galili G (2009) Expression of a bacterial bi-functional chorismate mutase/prephenate dehydratase modulates primary and secondary metabolism associated with aromatic amino acids in Arabidopsis. Plant J 60:156–167

    CAS  PubMed  Google Scholar 

  • Tzin V, Malitsky S, Zvi MMB, Bedair M, Sumner L, Aharoni A, Galili G (2012) Expression of a bacterial feedback-insensitive 3-deoxy-d-arabino-heptulosonate 7-phosphate synthase of the shikimate pathway in Arabidopsis elucidates potential metabolic bottlenecks between primary and secondary metabolism. New Phytol 194:430–439

    CAS  PubMed  Google Scholar 

  • Tzin V et al (2015) Altered levels of aroma and volatiles by metabolic engineering of shikimate pathway genes in tomato fruits. AIMS Bioengin 2:75–92

    CAS  Google Scholar 

  • Udomsom N et al (2016) Function of AP2/ERF transcription factors involved in the regulation of specialized metabolism in Ophiorrhiza pumila revealed by transcriptomics and metabolomics. Front Plant Sci 7:1861

    PubMed  PubMed Central  Google Scholar 

  • Uragami A, Sakai A, Nagai M, Takahashi T (1989) Survival of cultured cells and somatic embryos of Asparagus officinalis cryopreserved by vitrification. Plant Cell Rep 8:418–421

    CAS  PubMed  Google Scholar 

  • Usman B, Nawaz G, Zhao N, Liu Y, Li R (2020) Generation of high yielding and fragrant rice (Oryza sativa L.) lines by CRISPR/Cas9 targeted mutagenesis of three homoeologs of cytochrome P450 gene family and OsBADH2 and transcriptome and proteome profiling of revealed changes triggered by mutations. Plants 9(6):788

    CAS  PubMed Central  Google Scholar 

  • Vlad D, Abu-Jamous B, Wang P, Langdale JA (2019) A modular steroid-inducible gene expression system for use in rice. BMC Plant Biol 19:1–14

    CAS  Google Scholar 

  • Walsh G (2018) Biopharmaceutical benchmarks. Nat Biotechnol 36:1136–1145

    CAS  PubMed  Google Scholar 

  • Wang J, Jiang J, Oard JH (2000) Structure, expression and promoter activity of two polyubiquitin genes from rice (Oryza sativa L.). Plant Sci 156:201–211

    CAS  PubMed  Google Scholar 

  • Wang L et al (2010) A dynamic gene expression atlas covering the entire life cycle of rice. Plant J 61:752–766

    CAS  PubMed  Google Scholar 

  • Wilson SA, Maindarkar SN, McKee MC, Vilkhovoy M, Henson MA, Roberts SC (2020) A population balance model to modulate shear for the control of aggregation in Taxus suspension cultures. Biotechnol Prog 36:e2932

    CAS  PubMed  Google Scholar 

  • Wilson SA, Roberts SC (2012) Recent advances towards development and commercialization of plant cell culture processes for the synthesis of biomolecules. Plant Biotechnol J 10:249–268

    CAS  PubMed  Google Scholar 

  • Xu J, Zhang N (2014) On the way to commercializing plant cell culture platform for biopharmaceuticals: present status and prospect. Pharm Bioprocess 2:499

    PubMed  PubMed Central  Google Scholar 

  • Xu Y et al (2019) Intron-targeted gene insertion in rice using CRISPR/Cas9: a case study of the Pi-ta gene. Crop J 8:424–431

    Google Scholar 

  • Yu D, Song MN, Lim JA, Kim DI (2008) Effects of culture media on hCTLA4Ig production and protein expression patterns in transgenic rice cell suspension cultures. Biotechnol Bioprocess Eng 13:424–430

    CAS  Google Scholar 

  • Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333

    CAS  PubMed  Google Scholar 

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Acknowledgements

Sagar Arya acknowledges Deakin University, Australia for providing PhD fellowship.

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Authors and Affiliations

  1. TERI-Deakin Nanobiotechnology Centre, The Energy and Resources Institute, Gurugram, Haryana, 122001, India

    Sagar S. Arya, Divyani D. Kumari & Sangram K. Lenka

  2. School of Life and Environmental Sciences, Deakin University, Geelong, VIC, 3216, Australia

    Sagar S. Arya, James E. Rookes & David M. Cahill

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  1. Sagar S. Arya
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Arya, S.S., Kumari, D.D., Rookes, J.E. et al. Rice cell suspension culture as a model for producing high-value recombinant proteins and plant specialized metabolites. Plant Cell Tiss Organ Cult 145, 463–486 (2021). https://doi.org/10.1007/s11240-021-02028-z

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