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Carrot Cells: A Pioneering Platform for Biopharmaceuticals Production

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Abstract

Carrot (Daucus carota L.) is of importance in the molecular farming field as it constitutes the first plant species approved to produce biopharmaceuticals for human use. In this review, features that make carrot an advantageous species in the molecular farming field are analyzed and a description of the developments achieved with this crop thus far is presented. A guide for genetic transformation procedures is also included. The state of the art comprises ten vaccine prototypes against Measles virus, Hepatitis B virus, Human immunodeficiency virus, Yersinia pestis, Chlamydia trachomatis, Mycobacterium tuberculosis, enterotoxigenic Escherichia coli, Corynebacterium diphtheria/Clostridium tetani/Bordetella pertussis, and Helicobacter pylori; as well as the case of the glucocerebrosidase, an enzyme used for replacement therapy, and other therapeutics. Perspectives for these developments are envisioned and innovations are proposed such as the use of transplastomic technologies-, hairy roots-, and viral expression-based systems to improve yields and develop new products derived from this advantageous plant species.

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References

  1. Hernández, M., Rosas, G., Cervantes, J., Fragoso, G., Rosales-Mendoza, S., & Sciutto, E. (2014). Transgenic plants: A 5-year update on oral antipathogen vaccine development. Expert Review of Vaccines, 27, 1–14.

    Google Scholar 

  2. Virdi, V., & Depicker, A. (2013). Role of plant expression systems in antibody production for passive immunization. The International Journal of Developmental Biology, 57(6–8), 587–593.

    Article  CAS  Google Scholar 

  3. da Cunha, N. B., Vianna, G. R., da Almeida Lima, T., & Rech, E. (2014). Molecular farming of human cytokines and blood products from plants: Challenges in biosynthesis and detection of plant-produced recombinant proteins. Biotechnology Journal, 9(1), 39–50.

    Article  Google Scholar 

  4. Shaaltiel, Y., Bartfeld, D., Hashmueli, S., Baum, G., Brill-Almon, E., Galili, G., et al. (2007). Production of glucocerebrosidase with terminal mannose glycans for enzyme replacement therapy of Gaucher’s disease using a plant cell system. Plant Biotechnology Journal, 5(5), 579–590.

    Article  CAS  Google Scholar 

  5. Protalix. Retrieved October, 2014 from http://www.protalix.com/index.asp.

  6. Marquet-Blouin, E., Bouche, F. B., Steinmetz, A., & Muller, C. P. (2003). Neutralizing immunogenicity of transgenic carrot (Daucus carota L.)-derived measles virus hemagglutinin. Plant Molecular Biology, 51(4), 459–469.

    Article  CAS  Google Scholar 

  7. Food and Agriculture Organization of the United Sations Statistics Division (FAOSTAT). Retrieved October, 2014 from http://faostat3.fao.org/faostat-gateway/go/to/home/E.

  8. United States Department of Agriculture (USDA). Retrieved October, 2014 from http://nutritiondata.self.com/facts/vegetables-and-vegetable-products/2383/2.

  9. Steward, F. C. (1958). Growth and development of cultured cells. III. Interpretation of the growth from free cells to carrot plant. American Journal of Botany, 45, 709–713.

    Article  Google Scholar 

  10. Steward, F. C., Mapes, M. O., & Smith, J. (1958). Growth and development of cultured cells. I. Growth and division of freely suspended cells. American Journal of Botany, 45, 693–713.

    Article  Google Scholar 

  11. Baranski, R. (2008). Genetic transformation of carrot (Daucus carota) and other Apiaceae species. Transgenic Plant Journal, 2, 18–38.

    Google Scholar 

  12. Moscatiello, R., Baldan, B., & Navazio, L. (2013). Plant cell suspension cultures. Methods in Molecular Biology, 953, 77–93.

    CAS  Google Scholar 

  13. Namdev, P. K., & Dunlop, E. H. (1995). Shear sensitivity of plant cells in suspensions present and future. Applied Biochemistry Biotechnology, 54(1–3), 109–131.

    Article  CAS  Google Scholar 

  14. Larkin, P. J., & Scowcroft, W. R. (1981). Somaclonal variation—A novel source of variability from cell cultures for plant improvement. Theoretical and Applied Genetics, 60, 197–214.

    Article  CAS  Google Scholar 

  15. Rosales-Mendoza, S., Soria-Guerra, R., de Jesús Olivera-Flores, M., López-Revilla, R., Argüello-Astorga, G., Jiménez-Bremont, J., et al. (2007). Expression of Escherichia coli heat-labile enterotoxin b subunit (LTB) in carrot (Daucus carota L.). Plant Cell Reports, 26(7), 969–976.

    Article  CAS  Google Scholar 

  16. Balestrazzi, A., Carbonera, D., & Cella, R. (1991). Transformation of Daucus carota hypocotyls mediated by Agrobacterium tumefaciens. Journal of Genetics and Breeding, 45, 135–140.

    Google Scholar 

  17. Hardegger, M., & Sturm, A. (1998). Transformation and regeneration of carrot (Daucus carota L.). Molecular Breeding, 4, 119–127.

    Article  CAS  Google Scholar 

  18. Pawlicki, N., Sangwan, R., & Sangwan-Norrel, B. (1992). Factors influencing the Agrobacterium tumefaciens-mediated transformation of carrot (Daucus carota L.). Plant Cell, Tissue and Organ Culture, 31, 129–139.

    Article  CAS  Google Scholar 

  19. Martínez-González, L., Rosales-Mendoza, S., Soria-Guerra, R. E., Moreno-Fierros, L., López-Revilla, R., Korban, S., et al. (2011). Oral immunization with a lettuce-derived Escherichia coli heat-labile toxin B subunit induces neutralizing antibodies in mice. Plant Cell, Tissue and Organ Culture, 10, 441–449.

    Article  Google Scholar 

  20. Luchakivskaya, Y., Kishchenko, O., Gerasymenko, I., Olevinskaya, Z., Simonenko, Y., Spivak, M., & Kuchuk, M. (2011). High-level expression of human interferon alpha-2b in transgenic carrot (Daucus carota L.) plants. Plant Cell Reports, 30(3), 407–415.

    Article  CAS  Google Scholar 

  21. Wally, O., Jayaraj, J., & Punja, Z. K. (2008). Comparative expression of beta-glucuronidase with five different promoters in transgenic carrot (Daucus carota L.) root and leaf tissues. Plant Cell Reports, 27(2), 279–287.

    Article  CAS  Google Scholar 

  22. Arango, J., Salazar, B., Welsch, R., Sarmiento, F., Beyer, P., & Al-Babili, S. (2010). Putative storage root specific promoters from cassava and yam: Cloning and evaluation in transgenic carrots as a model system. Plant Cell Reports, 29(6), 651–659.

    Article  CAS  Google Scholar 

  23. Chilton, M. D., Tepfer, D. A., Petit, A., David, C., Casse-Delbart, F., & Tempé, J. (1982). Agrobacterium rhizogenes inserts T-DNA into the genomes of the host plant root cells. Nature, 295, 432–434.

    Article  CAS  Google Scholar 

  24. Skarjinskaia, M., Ruby, K., Araujo, A., Taylor, K., Gopalasamy-Raju, V., Musiychuk, K., et al. (2013). Hairy roots as a vaccine production and delivery system. Advances in Biochemical Engineering/Biotechnology, 134, 115–134.

    Article  Google Scholar 

  25. Kumar, S., Dhingra, A., & Daniell, H. (2004). Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves confers enhanced salt tolerance. Plant Physiology, 136(1), 2843–2854.

    Article  CAS  Google Scholar 

  26. Grabowski, G. A., Barton, N. W., Pastores, G., Dambrosia, J. M., Banerjee, T. K., McKee, M. A., et al. (1995). Enzyme therapy in type 1 Gaucher disease: Comparative efficacy of mannose-terminated glucocerebrosidase from natural and recombinant sources. Annals of Internal Medicine, 122, 33–39.

    Article  CAS  Google Scholar 

  27. Burrow, T. A., & Grabowski, G. A. (2011). Velaglucerase alfa in the treatment of Gaucher disease type 1. Clinical Investigation (London), 1, 285–293.

    Article  CAS  Google Scholar 

  28. Grabowski, G. A., Golembo, M., & Shaaltiel, Y. (2014). Taliglucerase alfa: An enzyme replacement therapy using plant cell expression technology. Molecular Genetics and Metabolism, 112(1), 1–8.

    Article  CAS  Google Scholar 

  29. Pastores, G. M., Petakov, M., & Giraldo, P. (2014). A Phase 3, multicenter, open-label, switchover trial to assess the safety and efficacy of Taliglucerase alfa, a plant cell-expressed recombinant human glucocerebrosidase, in adult and pediatric patients with Gaucher disease previously treated with imiglucerase. Blood Cells, Molecules, & Diseases, 53(4), 253–260.

    Article  CAS  Google Scholar 

  30. van Dussen, L., Zimran, A., Akkerman, E. M., Aerts, J. M., Petakov, M., Elstein, D., et al. (2013). Taliglucerase alfa leads to favorable bone marrow responses in patients with type I Gaucher disease. Blood Cells, Molecules, & Diseases, 50, 206–211.

    Article  Google Scholar 

  31. Protalix. Retrieved October, 2014 from http://www.protalix.com/development-pipeline/overview-development-pipeline.asp.

  32. Protalix. Retrieved October, 2014 from http://www.protalix.com/development-pipeline/prx-112-oral-gaucher-disease.asp.

  33. Armuzzi, A., Lionetti, P., Blandizzi, C., Caporali, R., Chimenti, S., Cimino, L., et al. (2014). Anti-TNF agents as therapeutic choice in immune-mediated inflammatory diseases: Focus on adalimumab. International Journal of Immunopathology and Pharmacology, 27(1 Suppl), 11–32.

    CAS  Google Scholar 

  34. Protalix. Retrieved October, 2014 from http://www.protalix.com/resources/DDW-2014-Poster-TNF.pdf.

  35. Waldek, S., & Feriozzi, S. (2014). Fabry nephropathy: A review—How can we optimize the management of Fabry nephropathy? BMC Nephrology, 15, 72.

    Article  Google Scholar 

  36. Kizhner, T., Azulay, Y., Hainrichson, M., Tekoah, Y., Arvatz, G., Shulman, A., et al. (2014). Characterization of a chemically modified plant cell culture expressed human α-Galactosidase—A enzyme for treatment of Fabry disease. Molecular Genetics and Metabolism,. doi:10.1016/j.ymgme.2014.08.002.

    Google Scholar 

  37. Osman, R., Al Jamal, K. T., Kan, P. L., Awad, G., Mortada, N., El-Shamy, A. E., & Alpar, O. (2013). Inhalable DNase I microparticles engineered with biologically active excipients. Pulmonar Pharmacology Therapy, 26(6), 700–709.

    Article  CAS  Google Scholar 

  38. Protalix. Retrieved October, 2014 from http://www.protalix.com/development-pipeline/prx-110-dnase.asp.

  39. Luchakivskaia, Iu. S., Olevinskaia, Z. M., Kishchenko, E. M., Spivak, N. Ia., & Kuchuk, N. V. (2012). Obtaining of hairy-root, callus and suspension carrot culture (Daucus carota L.) able to accumulate human interferon alpha-2b. i genetika, 46(1), 18–26.

  40. World Health Organization (WHO). Retrieved September, 2014 from http://www.who.int/immunization/diseases/measles/en/index.html.

  41. Mossong, J., Nokes, D. J., Edmunds, W. J., Cox, M., Ratnam, S., & Muller, C. (1999). Modeling the impact of subclinical measles transmission in vaccinated populations with waning immunity. American Journal of Epidemiology, 150, 1238–1249.

    Article  CAS  Google Scholar 

  42. Naniche, D., Varior-Krishnan, G., Cervoni, F., Wild, T. F., Rossi, B., Rabourdin-Combe, C., & Gerlier, D. (1993). Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. Journal of Virology, 67, 6025–6032.

    CAS  Google Scholar 

  43. Wild, T. F., Malvoisin, E., & Buckland, R. (1991). Measles virus: both hemagglutinin and fusion glycoproteins are required for fusion. The Journal of General Virology, 72, 439–442.

    Article  CAS  Google Scholar 

  44. McFarlin, D. E., Bellini, W. J., Mingioli, E. S., Behar, T. N., & Trudgett, A. (1980). Monospecific antibody to the haemagglutinin of measles virus. The Journal of General Virology, 48, 425–442.

    Article  CAS  Google Scholar 

  45. Giraudon, P., & Wild, F. (1985). Correlation between epitopes on hemagglutinin of measles virus and biological activities: Passive protection by monoclonal antibodies is related to their hemagglutination inhibiting activity. Virology, 144, 46–58.

    Article  CAS  Google Scholar 

  46. Theisen, D. M., Bouche, F. B., El Kasmi, K. C., von der Ahe, I., Ammerlaan, W., Demotz, S., & Muller, C. P. (2000). Differential antigenicity of recombinant polyepitope-antigens based on loop- and helix-forming B and T cell epitopes. Journal of Immunological Methods, 242, 145–157.

    Article  CAS  Google Scholar 

  47. Theisen, D. M., Bouche, F. B., El Kasmi, K. C., von der Ahe, I., Ammerlaan, W., Demotz, S., et al. (2003). Neutralising immunogenicity of a polyepitope antigen expressed in a transgenic food plant: A novel antigen to protect against measles. Vaccine, 21(17–18), 2065–2072.

    Google Scholar 

  48. Bouche, F. B., Steinmetz, A., Yanagi, Y., & Muller, C. P. (2005). Induction of broadly neutralizing antibodies against measles virus mutants using a polyepitope vaccine strategy. Vaccine, 23(17–18), 2074–2077.

    Article  CAS  Google Scholar 

  49. World Health Organization (WHO). Retrieved September, 2014 from http://www.who.int/mediacentre/factsheets/fs204/en/index.html.

  50. Huang, Z., Elkin, G., Maloney, B. J., Beuhner, N., Arntzen, C. J., Thanavala, Y., & Mason, H. S. (2005). Virus-like particle expression and assembly in plants: Hepatitis B and Norwalk viruses. Vaccine, 23(15), 1851–1858.

    Article  CAS  Google Scholar 

  51. Youm, J. W., Won, Y. S., Jeon, J. H., Ryu, C. J., Choi, Y. K., Kim, H. C., et al. (2007). Oral immunogenicity of potato-derived HBsAg middle protein in BALB/c mice. Vaccine, 25(3), 577–584.

    Article  CAS  Google Scholar 

  52. Lou, X. M., Yao, Q. H., Zhang, Z., Peng, R. H., Xiong, A. S., & Wang, H. K. (2007). Expression of the human hepatitis B virus large surface antigen gene in transgenic tomato plants. Clinical and Vaccine Immunology, 14(4), 464–469.

    Article  CAS  Google Scholar 

  53. Deineko, E. V., Zagorskaya, A. A., Pozdnyakov, S. G., Filipenko, E. A., Permyakova, N. V., Sidorchuk, Y. V., et al. (2009). Comparative analysis of HBV M-antigen production in leaves of individual transgenic carrot plants. Doklady Biochemistry and Biophysics, 425, 76–79.

    Article  CAS  Google Scholar 

  54. Mouquet, H. (2014). Antibody B cell responses in HIV-1 infection. Trends in Immunology,. doi:10.1016/j.it.2014.08.007.

    Google Scholar 

  55. Lindh, I., Wallin, A., Kalbina, I., Sävenstrand, H., Engström, P., Andersson, S., & Strid, A. (2009). Production of the p24 capsid protein from HIV-1 subtype C in Arabidopsis thaliana and Daucus carota using an endoplasmic reticulum-directing SEKDEL sequence in protein expression constructs. Protein Expression and Purification, 66(1), 46–51.

    Article  CAS  Google Scholar 

  56. Weekly Epidemiological Record (WER) (Vol. 79, pp. 301–308). Retrieved October, 2014 from http://www.who.int/wer.

  57. Center for Disease Control and Prevention (CDCP). Retrieved October, 2014 from http://www.bt.cdc.gov/training/historyofbt/index.asp.

  58. Henderson, D. A. (1999). The looming threat of bioterrorism. Science, 283, 1279–1282.

    Article  CAS  Google Scholar 

  59. Du, Y. D., Rosqvist, R., & Forsberg, A. (2002). Role of fraction 1 of Yersinia pestis in inhibition of phagocytosis. Infection and Immunity, 70, 1453–1460.

    Article  CAS  Google Scholar 

  60. Nakajima, R., Motin, V. L., & Brubaker, R. R. (1995). Suppression of cytokines in mice by protein A-V fusion peptide and restoration of synthesis by active immunization. Infection and Immunity, 63, 3021–3029.

    CAS  Google Scholar 

  61. Rosales-Mendoza, S., Soria-Guerra, R. E., Moreno-Fierros, L., Han, Y., Alpuche-Solís, A. G., & Korban, S. S. (2011). Transgenic carrot tap roots expressing an immunogenic F1-V fusion protein from Yersinia pestis are immunogenic in mice. Journal of Plant Physiology, 168(2), 174–180.

    Article  CAS  Google Scholar 

  62. Rey-Ladino, J., Ross, A. G., & Cripps, A. W. (2014). Immunity, immunopathology, and human vaccine development against sexually transmitted Chlamydia trachomatis. Human Vaccines & Immunotherapeutics, 10(9), 2664–2673.

    Article  Google Scholar 

  63. Kalbina, I., Wallin, A., Lindh, I., Engström, P., Andersson, S., & Strid, K. (2011). A novel chimeric MOMP antigen expressed in Escherichia coli, Arabidopsis thaliana, and Daucus carota as a potential Chlamydia trachomatis vaccine candidate. Protein Expression and Purification, 80(2), 194–202.

    Article  CAS  Google Scholar 

  64. Centers for Disease Control and Prevention (CDCP). Retrieved September, 2014 from http://www.cdc.gov/tb/topic/globaltb/default.htm.

  65. World Health Organization (WHO). Retrieved September, 2014 from http://www.who.int/tb/vaccinesfaqs/en/.

  66. Uvarova, E. A., Belavin, P. A., Permyakova, N. V., Zagorskaya, A. A., Nosareva, O. V., Kakimzhanova, A. A., & Deineko, E. V. (2013). Oral immunogenicity of plant-made Mycobacterium tuberculosis ESAT6 and CFP10. Biomed Research International, 2013, 316304.

    Article  Google Scholar 

  67. Hadfield, T., McEvoy, P., Polotsky, Y., Tzinserling, V., & Yakovlev, A. (2000). The pathology of diphtheria. Journal of Infectious Diseases, 181(Suppl 1), S116–S120.

    Article  Google Scholar 

  68. Guiso, N. (2009). Bordetella pertussis and pertussis vaccines. Clinical Infectious Diseases, 49(10), 1565–1569.

    Article  Google Scholar 

  69. Centers for Disease Control and Prevention (CDCP). Retrieved September, 2014 from http://www.cdc.gov/vaccines/pubs/pinkbook/tetanus.html.

  70. Brodzik, R., Spitsin, S., Pogrebnyak, N., Tzinserling, V., & Yakovlev, A. (2009). Generation of plant-derived recombinant DTP subunit vaccine. Vaccine, 27(28), 3730–3734.

    Article  CAS  Google Scholar 

  71. World Health Organization (WHO). Retrieved October 2014 from http://www.who.int/mediacentre/factsheets/fs204/en/index.html.

  72. Wenneras, C., & Erling, V. (2004). Prevalence of enterotoxigenic Escherichia coli-associated diarrhoea and carrier state in the developing world. Journal of Health, Population, and Nutrition, 22(4), 370–382.

    Google Scholar 

  73. Sixma, T. K., Pronk, S. E., Kalk, K. H., Wartna, E. S., van Zanten, B. A., Witholt, B., & Hol, W. G. (1991). Crystal structure of a cholera toxin-related heat-labile enterotoxin from E. coli. Nature, 351, 371–377.

    Article  CAS  Google Scholar 

  74. Lopez, A. L., Gonzales, M. L., Aldaba, J. G., & Nair, G. B. (2014). Killed oral cholera vaccines: History, development and implementation challenges. Therapeutic Advances in Vaccines, 2(5), 123–136.

    Article  CAS  Google Scholar 

  75. Rosales-Mendoza, S., Soria-Guerra, R. E., López-Revilla, R., Moreno-Fierros, L., & Alpuche-Solís, A. (2008). Ingestion of transgenic carrots expressing the Escherichia coli heat-labile enterotoxin B subunit protects mice against cholera toxin challenge. Plant Cell Reports, 27(1), 79–84.

    Article  CAS  Google Scholar 

  76. Anderl, F., & Gerhard, M. (2014). Helicobacter pylori vaccination: Is there a path to protection? World Journal of Gastroenterology, 20(34), 11939–11949.

    Article  CAS  Google Scholar 

  77. Michetti, P., Kreiss, C., Kotloff, K. L., Porta, N., Blanco, J. L., Bachmann, D., et al. (1999). Oral immunization with urease and Escherichia coli heat-labile enterotoxin is safe and immunogenic in Helicobacter pylori-infected adults. Gastroenterology, 116(4), 804–812.

    Article  CAS  Google Scholar 

  78. Zhang, H., Liu, M., Li, Y., He, H., Yang, G., & Zheng, C. (2010). Oral immunogenicity and protective efficacy in mice of a carrot-derived vaccine candidate expressing UreB subunit against Helicobacter pylori. Protein Expression and Purification, 69(2), 127–131.

    Article  CAS  Google Scholar 

  79. Noh, S. A., Lee, H. S., Huh, G. H., Oh, M. J., Paek, K. H., Shin, J. S., & Bae, J. M. (2012). A sweet potato SRD1 promoter confers strong root-, taproot-, and tuber-specific expression in Arabidopsis, carrot, and potato. Transgenic Research, 21(2), 265–278.

    Article  CAS  Google Scholar 

  80. Mihaliak, C. A., Webb, S., Miller, T., Fanton, M., Kirk, D., Cardineau G., et al. (2005). Development of plant cell produced vaccines for animal health applications. In: Proceedings of the 108th Annual Meeting of the United States Animal Health Association, Greensboro, NC (pp. 158–163).

  81. Salazar-González, J. A., Bañuelos-Hernández, B., & Rosales-Mendoza, S. (2015). Current status of viral expression systems in plants and perspectives for oral vaccines development. Plant Molecular Biology. doi:10.1007/s11103-014-0279-5.

  82. Yusibov, V., Streatfield, S. J., Kushnir, N., Roy, G., & Padmanaban, A. (2013). Hybrid viral vectors for vaccine and antibody production in plants. Current Pharmaceutical Design, 19(31), 5574–5586.

    Article  CAS  Google Scholar 

  83. Orellana-Escobedo, L., Korban, S. S., & Rosales-Mendoza, S. (2014). Seed-based expression strategies. In: S. Rosales Mendoza (Ed.), Genetically engineered plants as a source of vaccines against wide spread diseases—An integrated view. New York: Springer. ISBN 978-1-4939-0850-9.

  84. Thomas, J., Guiltinan, M., Bustos, S., Thomas, T., & Nessler, C. (1989). Carrot (Daucus carota) hypocotyls transformation using Agrobacterium tumefaciens. Plant Cell Reports, 8, 354–357.

    Article  CAS  Google Scholar 

  85. Tokuji, Y., & Fukuda, H. (1999). A rapid method for transformation of carrot (Daucus carota L.) by using direct somatic embryogenesis. Bioscience, Biotechnology, and Biochemistry, 63, 519–523.

    Article  CAS  Google Scholar 

  86. Wurtele, E., & Bulka, K. (1989). A simple, efficient method for the Agrobacterium-mediated transformation of carrot callus cells. Plant Science, 61, 253–262.

    Article  CAS  Google Scholar 

  87. Deroles, S., Smith, M., & Lee, C. (2002). Factors affecting transformation of cell cultures from three dicotyledoneous pigment- producing species using microprojectile bombardment. Plant Cell, Tissue and Organ Culture, 70, 69–76.

    Article  CAS  Google Scholar 

  88. Rojas, E., Loza, E., Olivera, M., & Gomez, M. (2009). Expression of rabies virus G protein in carrots (Daucus carota). Transgenic Research, 18, 911–919.

    Article  Google Scholar 

  89. Annon, A., Rathore, K., & Crosby, K. (2014). Overexpression of a tobacco osmotin gene in carrot (Daucus carota L.) enhances drought tolerance. In Vitro Cellular & Developmental Biology-Plant, 50, 299–306.

    Article  CAS  Google Scholar 

  90. Boston, R., Becwar, M., Ryan, R., Goldsbrough, P., Larkings, B., & Hodges, (1987). Expression from heterologous promoters in electroporated carrot protoplasts. Plant Physiology, 83, 742–746.

    Article  CAS  Google Scholar 

  91. Dirks, R., & Sidorov, Tulmans C. (1996). A new protoplast culture system in Daucus carota L. and its application for mutant selection and transformation. Theoretical Applied Genetics, 93, 809–815.

    Article  CAS  Google Scholar 

  92. Scott, R., & Draper, J. (1987). Transformation of carrot tissues derived from embryogenic suspensión cells: A useful model system for gene expression studies in plants. Plant Molecular Biology, 8, 265–274.

    Article  CAS  Google Scholar 

  93. Gilbert, M., Zhang, Y., & Punja, Z. (1996). Introduction and expression of chitinase encoding genes in carrot following Agrobacterium-mediated transformation. In Vitro Cellular & Developmental Biology-Plant, 32, 171–178.

    Article  CAS  Google Scholar 

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We thank Omar González-Ortega for English edition.

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  1. Laboratorio de Biofarmacéuticos Recombinantes, Facultad de Ciencias Químicas, Universidad Autónoma de San Luis Potosí, Av. Dr. Manuel Nava 6, 78210, San Luis Potosí, SLP, Mexico

    Sergio Rosales-Mendoza & Marlene Anahí Tello-Olea

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Correspondence to Sergio Rosales-Mendoza.

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Rosales-Mendoza, S., Tello-Olea, M.A. Carrot Cells: A Pioneering Platform for Biopharmaceuticals Production. Mol Biotechnol 57, 219–232 (2015). https://doi.org/10.1007/s12033-014-9837-y

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