Plant Transformation Strategies

  • Verónica Araceli Márquez-Escobar
  • Omar González-Ortega
  • Sergio Rosales-MendozaEmail author


In this chapter, a general outlook on the plant transformation approaches is provided with emphasis in applications related to molecular farming. The rationale of nuclear, chloroplast, and transient expressions mediated by viral vectors are reviewed. Implications of such technologies in terms of protein yields, posttranslational modifications, scalability, and production time scale are critically analyzed. New trends in plant genetic engineering are also identified and perspectives on how these technologies might influence the molecular farming field are provided.


Nuclear transformation Chloroplast transformation Stable transformation Transient transformation Transplastomic technologies 


  1. Arai Y, Shikanai T, Doi Y, Yoshida S, Yamaguchi I, Nakashita H (2004) Production of polyhydroxybutyrate by polycistronic expression of bacterial genes in tobacco plastid. Plant Cell Physiol 45:1176–1184PubMedCrossRefGoogle Scholar
  2. Bally J, Nadai M, Vitel M, Rolland A, Dumain R, Dubald M (2009) Plant physiological adaptations to the massive foreign protein synthesis occurring in recombinant chloroplasts. Plant Physiol 150:1474–1481PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bally J, Paget E, Droux M, Job C, Job D, Dubald M (2008) Both the stroma and thylakoid lumen of tobacco chloroplasts are competent for the formation of disulphide bonds in recombinant proteins. Plant Biotechnol J 6:46–61PubMedGoogle Scholar
  4. Bendich AJ (1987) Why do chloroplasts and mitochondria contain so many copies of their genome? BioEssays 6:279–282PubMedCrossRefGoogle Scholar
  5. Bobik K, Burch-Smith TM (2015) Chloroplast signaling within, between and beyond cells. Front Plant Sci 6:781PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bock R (2015) Engineering plastid genomes: methods, tools, and applications in basic research and biotechnology. Annu Rev Plant Biol 66:211–241PubMedCrossRefGoogle Scholar
  7. Brune B, Hartzell P, Nicotera P, Orrenius S (1991) Spermine prevents endonuclease activation and apoptosis in thymocytes. Exp Cell Res 195:323–329PubMedCrossRefGoogle Scholar
  8. Chaudhary S, Parmenter DL, Moloney MM (1998) Transgenic Brassica carinata as a vehicle for the production of recombinant proteins in seeds. Plant Cell Rep 17:195–200CrossRefGoogle Scholar
  9. Dafny-Yelin M, Levy A, Tzfira T (2008) The ongoing saga of Agrobacterium–host interactions. Trends Plant Sci 13(3):102–105PubMedCrossRefGoogle Scholar
  10. Daniell H (1993) Foreign gene expression in chloroplasts of higher plants mediated by tungsten particle bombardment. Methods Enzymol 217:536–556PubMedCrossRefGoogle Scholar
  11. Daniell H (1997) Transformation and foreign gene expression in plants by microprojectile bombardment. Methods Mol Biol 62:463–489PubMedGoogle Scholar
  12. Daniell H (2002) Molecular strategies for gene containment in transgenic crops. Nat Biotechnol 20:581–586PubMedPubMedCentralCrossRefGoogle Scholar
  13. Daniell H (2007) Transgene containment by maternal inheritance: effective or elusive? Proc Natl Acad Sci U S A 104(17):6879–6880PubMedPubMedCentralCrossRefGoogle Scholar
  14. Daniell H, Chebolu S, Kumar S, Singleton M, Falconer R (2005) Chloroplast-derived vaccine antigens and other therapeutic proteins. Vaccine 23:1779–1783PubMedCrossRefGoogle Scholar
  15. Daniell H, Dhingra A (2002) Multigene engineering: dawn of an exciting new era in biotechnology. Curr Opin Biotechnol 13:136–141PubMedPubMedCentralCrossRefGoogle Scholar
  16. Daniell H, Lin CS, Yu M, Chang WJ (2016) Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol 17(1):134PubMedPubMedCentralCrossRefGoogle Scholar
  17. Daniell H, Parkinson CL (2003) Jumping genes and containment. Nat Biotechnol 21:374–375PubMedCrossRefGoogle Scholar
  18. Davoodi-Semiromi A, Schreiber M, Nalapalli S, Verma D, Singh ND, Banks RK, Chakrabarti D, Daniell H (2010) Chloroplast-derived vaccine antigens confer dual immunity against cholera and malaria by oral or injectable delivery. Plant Biotechnol J 8:223–242PubMedCrossRefGoogle Scholar
  19. De Block M, Herrera-Estrella L, Van Montagu M, Schell J, Zambryski P (1984) Expression of foreign genes in regenerated plants and in their progeny. EMBO 3(8):1681–1689CrossRefGoogle Scholar
  20. Deng XW, Gruissem W (1987) Control of plastid gene expression during development: the limited role of transcriptional regulation. Cell 49:379–387PubMedCrossRefGoogle Scholar
  21. Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45:616–629PubMedCrossRefGoogle Scholar
  22. Elghabi Z, Ruf S, Bock R (2011) Biolistic co-transformation of the nuclear and plastid genomes. Plant J 67:941–948PubMedCrossRefGoogle Scholar
  23. Francis KE, Spiker S (2005) Identification of Arabidopsis thaliana transformants without selection reveals a high occurrence of silenced T-DNA integrations. Plant J 41(3):464–477PubMedCrossRefGoogle Scholar
  24. Garg R, Tolbert M, Oakes JL, Clemente TE, Bost KL, Piller KJ (2007) Chloroplast targeting of FanC, the major antigenic subunit of Escherichia coli K99 fimbriae, in transgenic soybean. Plant Cell Rep 26(7):1011–1023PubMedCrossRefGoogle Scholar
  25. Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67(1):16–37PubMedPubMedCentralCrossRefGoogle Scholar
  26. Gelvin SB (2010) Finding a way to the nucleus. Curr Opin Microbiol 13(1):53–58PubMedCrossRefGoogle Scholar
  27. Gleba Y, Klimyuk V, Marillonnet S (2005) Magnifection–a new platform for expressing recombinant vaccines in plants. Vaccine 23(17–18):2042–2048PubMedPubMedCentralCrossRefGoogle Scholar
  28. Gleba Y, Klimyuk V, Marillonnet S (2007) Viral vectors for the expression of proteins in plants. Curr Opin Biotechnol 18(2):134–141PubMedCrossRefGoogle Scholar
  29. Gleba Y, Marillonnet S, Klimyuk V (2004) Engineering viral expression vectors for plants: the ‘full virus’ and the ‘deconstructed virus’ strategies. Curr Opin Plant Biol 7(2):182–188PubMedCrossRefGoogle Scholar
  30. Golczyk H, Greiner S, Wanner G, Weihe A, Bock R, Börner T, Herrmann RG (2014) Chloroplast DNA in mature and senescing leaves: a reappraisal. Plant Cell 26:847–854PubMedPubMedCentralCrossRefGoogle Scholar
  31. Golds T, Maliga P, Koop HU (1993) Stable plastid transformation in PEG-treated protoplasts of Nicotiana tabacum. Nat Biotechnol 11:95–97CrossRefGoogle Scholar
  32. Gómez E, Lucero MS, Chimeno Zoth S, Carballeda JM, Gravisaco MJ, Berinstein A (2013) Transient expression of VP2 in Nicotiana benthamiana and its use as a plant-based vaccine against infectious bursal disease virus. Vaccine 31(23):2623–2627PubMedPubMedCentralCrossRefGoogle Scholar
  33. Gomord V, Faye L (2004) Post-translational modification of therapeutic proteins in plants. Curr Opin Plant Biol 7:171–181PubMedCrossRefGoogle Scholar
  34. Guda C, Lee S-B, Daniell H (2000) Stable expression of a biodegradable protein-based polymer in tobacco chloroplasts. Plant Cell Rep 19:257–262CrossRefGoogle Scholar
  35. He J, Peng L, Lai H, Hurtado J, Stahnke J, Chen Q (2014) A plant-produced antigen elicits potent immune responses against West Nile virus in mice. Biomed Res Int 2014:952865PubMedPubMedCentralGoogle Scholar
  36. Hefferon KL (2012) Plant virus expression vectors set the stage as production platforms for biopharmaceutical proteins. Virology 433(1):1–6PubMedCrossRefGoogle Scholar
  37. Hellens RP, Edward EA, Leyland NR, Bean S, Mullineaux PM (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biol 42:819–832PubMedCrossRefGoogle Scholar
  38. Herrera-Estrella L, Depicker A, Van Montagu M, Schell J (1983) Expression of chimeric genes transferred into plant cells using a Ti-plasmid-derived vector. Nature 303(5914):209–213CrossRefGoogle Scholar
  39. Herz S, Füssl M, Steiger S, Koop HU (2005) Development of novel types of plastid trans formation vectors and evaluation of factors controlling expression. Transgenic Res 14:969–982PubMedCrossRefGoogle Scholar
  40. Hoekema A, Hirsch PR, Hooykaas PJJ, Schilperoort R (1983) A binary plant vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303:179–180CrossRefGoogle Scholar
  41. Jin S, Daniell H (2015) The engineered chloroplast genome just got smarter. Trends Plant Sci 20:622–640PubMedPubMedCentralCrossRefGoogle Scholar
  42. Joensuu JJ, Kotiaho M, Teeri TH, Valmu L, Nuutila AM, Oksman-Caldentey K-M, Niklander-Teeri V (2006) Glycosylated F4 (K88) fimbrial adhesin FaeG expressed in barley endosperm induces ETEC-neutralizing antibodies in mice. Transgenic Res 15:359–373PubMedCrossRefGoogle Scholar
  43. Kanagarajan S, Tolf C, Lundgren A, Waldenström J, Brodelius PE (2012) Transient expression of hemagglutinin antigen from low pathogenic avian influenza a (H7N7) in nicotiana benthamiana. PLoS ONE 7:e33010PubMedPubMedCentralCrossRefGoogle Scholar
  44. Kanagaraj AP, Verma D, Daniell H (2011) Expression of dengue-3 premembrane and envelope polyprotein in lettuce chloroplasts. Plant Mol Biol 76:323–333PubMedPubMedCentralCrossRefGoogle Scholar
  45. Kang TJ, Loc NH, Jang MO, Jang YS, Kim YS, Seo JE, Yang MS (2003) Expression of the B subunit of E. coli heat-labile enterotoxin in the chloroplasts of plants and its characterization. Transgenic Res 12(6):683–691PubMedCrossRefGoogle Scholar
  46. Karimi M, Inze D, Depicker A (2002) GATEWAY™ vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195PubMedCrossRefGoogle Scholar
  47. Kikkert JR, Vidal JR, Reisch BI (2005) Stable transformation of plant cells by particle bombardment/biolistics. Meth Mol Biol 286:61–78Google Scholar
  48. Kim MY, Kim BY, Oh SM, Reljic R, Jang YS, Yang MS (2016) Oral immunisation of mice with transgenic rice calli expressing cholera toxin B subunit fused to consensus dengue cEDIII antigen induces antibodies to all four dengue serotypes. Plant Mol Biol 92:347–356PubMedPubMedCentralCrossRefGoogle Scholar
  49. Klaus SM, Huang FC, Golds TJ, Koop HU (2004) Generation of marker-free plastid transformants using a transiently cointegrated selection gene. Nat Biotechnol 22:225–229PubMedCrossRefGoogle Scholar
  50. Koop HU, Steinmuller K, Wagner H, Rossler C, Eibl C, Sacher L (1996) Integration of foreign sequences into the tobacco plastome via polyethylene glycol-mediated protoplast transformation. Planta 199:193–201PubMedCrossRefGoogle Scholar
  51. Krenek P, Samajova O, Luptovciak I, Doskocilova A, Komis G, Samaj J (2015) Transient plant transformation mediated by Agrobacterium tumefaciens: Principles, methods and applications. Biotechnol Adv 1(33):1024–1042CrossRefGoogle Scholar
  52. Laguía-Becher M, Martín V, Kraemer M, Corigliano M, Yacono ML, Goldman A, Clemente M (2010) Effect of codon optimization and subcellular targeting on Toxoplasma gondii antigen SAG1 expression in tobacco leaves to use in subcutaneous and oral immunization in mice. BMC Biotechnol 10:52PubMedPubMedCentralCrossRefGoogle Scholar
  53. Lakshmi PS, Verma D, Yang X, Lloyd B, Daniell H (2013) Low cost tuberculosis vaccine antigens in capsules: expression in chloroplasts, bio-encapsulation, stability and functional evaluation in vitro. PLoS ONE 8(1):e54708PubMedPubMedCentralCrossRefGoogle Scholar
  54. Lee G, Na YJ, Yang B-G, Choi J-P, Seo YB, Hong C-P, Yun CH, Kim DH, Sohn EJ, Kim JH, Sung YC, Kim Y-K, Jang MH, Hwang I (2015a) Oral immunization of haemaggulutinin H5 expressed in plant endoplasmic reticulum with adjuvant saponin protects mice against highly pathogenic avian influenza A virus infection. Plant Biotechnol J 13:62–72PubMedCrossRefGoogle Scholar
  55. Lee JS, Kallehauge TB, Pedersen LE, Kildegaarda HF (2015b) Site-specific integration in CHO cells mediated by CRISPR/Cas9 and homology-directed DNA repair pathway. Sci Rep 5:8572PubMedPubMedCentralCrossRefGoogle Scholar
  56. Lee SM, Kang K, Chung H, Yoo SH, Xu XM, Lee SB, Cheong JJ, Daniell H, Kim M (2006) Plastid transformation in the monocotyledonous cereal crop, rice (Oryza sativa) and transmission of transgenes to their progeny. Mol Cells 21(3):401–410PubMedPubMedCentralGoogle Scholar
  57. Leister D (2003) Chloroplast research in the genomic age. Trends Genet 19:47–56PubMedCrossRefGoogle Scholar
  58. Lelivelt CL, McCabe MS, Newell CA, Desnoo CB, van Dun KM, Birch-Machin I, Gray JC, Mills KH, Nugent JM (2005) Stable plastid transformation in lettuce (Lactuca sativa L.). Plant Mol Biol 58:763–774PubMedCrossRefGoogle Scholar
  59. Lelivelt CL, van Dun KM, de Snoo CB, McCabe MS, Hogg BV, Nugent JM (2014) Plastid transformation in lettuce (Lactuca sativa L.) by polyethylene glycol treatment of protoplasts. Methods Mol Biol 1132:317–330PubMedCrossRefGoogle Scholar
  60. Lerouge P, Cabanes-Macheteau M, Rayon C, Fischette-Laine AC, Gomord V, Faye L (1998) N-Glycoprotein biosynthesis in plants: recent developments and future trends. Plant Mol Biol 38:31–48PubMedCrossRefGoogle Scholar
  61. Li D, O’Leary J, Huang Y, Huner NP, Jevnikar AM, Ma S (2006) Expression of cholera toxin B subunit and the B chain of human insulin as a fusion protein in transgenic tobacco plants. Plant Cell Rep 25(5):417–424PubMedCrossRefGoogle Scholar
  62. Lu Y, Rijzaani H, Karcher D, Ruf S, Bock R (2013) Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons. Proc Natl Acad Sci U S A 110(8):E623–E632PubMedPubMedCentralCrossRefGoogle Scholar
  63. Ma C, Wang L, Webster DE, Campbell AE, Coppel RL (2012) Production, characterisation and immunogenicity of a plant-made Plasmodium antigen–the 19 kDa C-terminal fragment of Plasmodium yoelii merozoite surface protein 1. Appl Microbiol Biotechnol 94(1):151–161PubMedCrossRefGoogle Scholar
  64. Maliga P (1993) Towards plastid transformation in flowering plants. Trends Biotechnol 11:101–106CrossRefGoogle Scholar
  65. Maliga P (2004) Plastid transformation in higher plants. Annu Rev Plant Biol 55:289–313PubMedCrossRefGoogle Scholar
  66. Maliga P, Carrer H, Kanevski I, Staub J, Svab Z (1993) Plastid engineering in land plants: a conservative genome is open to change. Phil Trans R Soc Lond B 341:449–454CrossRefGoogle Scholar
  67. Matsui T, Asao H, Ki M, Sawada K, Kato K (2009) Transgenic lettuce producing a candidate protein for vaccine against edema disease. Biosci Biotechnol Biochem 73:1628–1634PubMedCrossRefGoogle Scholar
  68. Moloney MM, Van-Rooijen G, Sembiosys Genetics Inc (2006) Expression of epidermal growth factor in plant seeds. United States patent US 7091401Google Scholar
  69. Monreal-Escalante E, Bañuelos-Hernández B, Hernández M, Fragoso G, Garate T, Sciutto E, Rosales-Mendoza S (2015) Expression of multiple taenia solium immunogens in plant cells through a ribosomal skip mechanism. Mol Biotechnol 57(7):635–643PubMedPubMedCentralCrossRefGoogle Scholar
  70. Nakashita H, Arai Y, Shikanai T, Doi Y, Yamaguchi I (2001) Introduction of bacterial metabolism into higher plants by polycistronic transgene expression. Biosci Biotechnol Biochem 65:1688–1691PubMedCrossRefGoogle Scholar
  71. Nelson G, Marconi P, Periolo O, La Torre J, Alvarez MA (2012) Immunocompetent truncated E2 glycoprotein of bovine viral diarrhea virus (BVDV) expressed in Nicotiana tabacum plants: a candidate antigen for new generation of veterinary vaccines. Vaccine 30:4499–4504PubMedCrossRefGoogle Scholar
  72. Neuhaus JM, Rogers JC (1988) Sorting of proteins to vacuoles in plant cells. Plant Mol Biol 38:127–144CrossRefGoogle Scholar
  73. Neuhaus JM, Sticher L, Meins FJ, Boller T (1991) A short C-terminal sequence is necessary and sufficient for the targeting of chitinases to the plant vacuole. Proc Natl Acad Sci U S A 88(22):10362–10366PubMedPubMedCentralCrossRefGoogle Scholar
  74. Noris E, Poli A, Cojoca R, Rittà M, Cavallo F, Vaglio S, Matic S, Landolfo S (2011) A human papillomavirus 8 E7 protein produced in plants is able to trigger the mouse immune system and delay the development of skin lesions. Arch Virol 156(4):587–595PubMedCrossRefGoogle Scholar
  75. Nugent GD, Coyne S, Nguyen TH, Kavanagh TA, Dix PJ (2005a) Nuclear and plastid transformation of Brassica oleracea var. botrytis (cauliflower) using PEG-mediated uptake of DNA into protoplasts. Plant Sci 170:135–142CrossRefGoogle Scholar
  76. Nugent GD, ten Have M, van der Gulik A, Dix PJ, Uijtewaal BA, Mordhorst AP (2005b) Plastid transformants of tomato selected using mutations affecting ribosome structure. Plant Cell Rep 24:341–349PubMedCrossRefGoogle Scholar
  77. Nykiforuk CL, Boothe JG, Murray EW, Keon RG, Goren J, Markley NA, Moloney MM (2005) Transgenic expression and recovery of biologically active recombinant human insulin from Arabidopsis thaliana seeds. Plant Biotechnol J 4:77–85CrossRefGoogle Scholar
  78. O’Neill C, Horvath GV, Horvath E, Dix PJ, Medgyesy P (1993) Chloroplast transformation in plants: polyethylene glycol (PEG) treatment of protoplasts is an alternative to biolistic delivery systems. Plant J 3:729–738PubMedCrossRefGoogle Scholar
  79. Păcurar DI, Thordal-Christensen H, Păcurar ML, Pamfil D, Botez C, Bellini C (2011) Agrobacterium tumefaciens: from crown gall tumors to genetic transformation. Physiol Mol Plant Pathol 76:76–81CrossRefGoogle Scholar
  80. Parmenter DL, Boothe JG, Van Rooijen GJH, Yeung EC, Moloney MM (1995) Production of biologically active hirudin in plants seeds using oleosin partitioning. Plant Mol Biol 29:1167–1180PubMedCrossRefGoogle Scholar
  81. Paul M, Ma JK (2011) Plant-made pharmaceuticals: leading products and production platforms. Biotechnol Appl Biochem 58(1):58–67PubMedCrossRefGoogle Scholar
  82. Piron R, De Koker S, De Paepe A, Goossens J, Grooten J, Nauwynck H, Depicker A (2014) Boosting in planta production of antigens derived from the porcine reproductive and respiratory syndrome virus (PRRSV) and subsequent evaluation of their immunogenicity. PLoS ONE 9:e91386PubMedPubMedCentralCrossRefGoogle Scholar
  83. Rivera AL, Gómez-Lim M, Fernández F, Loske AM (2012) Physical methods for genetic plant transformation. Phys Life Rev 9(3):308–345PubMedCrossRefGoogle Scholar
  84. Ruf S, Hermann M, Berger IJ, Carrer H, Bock R (2001) Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nat Biotechnol 19:870–875PubMedCrossRefGoogle Scholar
  85. Ruf S, Karcher D, Bock R (2007) Determining the transgene containment level provided by chloroplast transformation. Proc Natl Acad Sci U S A 104(17):6998–7002PubMedPubMedCentralCrossRefGoogle Scholar
  86. Ruhlman T, Ahangari R, Devine A, Samsam M, Daniell H (2007) Expression of cholera toxin B-proinsulin fusion protein in lettuce and tobacco chloroplasts-oral administration protects against development of insulitis in non-obese diabetic mice. Plant Biotechnol J 5(4):495–510PubMedPubMedCentralCrossRefGoogle Scholar
  87. Ruhlman TA (2014) Plastid transformation in lettuce (Lactuca sativa L.) by biolistic DNA delivery. Methods Mol Biol 1132:331–343PubMedCrossRefGoogle Scholar
  88. Sainsbury F, Lomonossoff GP (2008) Extremely high-level and rapid transient protein production in plants without the use of viral replication. Plant Physiol 148(3):1212–1218PubMedPubMedCentralCrossRefGoogle Scholar
  89. Sanford JC, Smith FD, Russell JA (1993) Optimizing the biolistic process for different biological applications. Methods Enzymol 217:483–509PubMedCrossRefGoogle Scholar
  90. Schnell J, Steele M, Bean J, Neuspiel M, Girard C, Dormann N, Pearson C, Savoie A, Bourbonnière L, Macdonald P (2015) A comparative analysis of insertional effects in genetically engineered plants: considerations for pre-market assessments. Transgenic Res 24(1):1–17PubMedCrossRefGoogle Scholar
  91. Shaaltiel Y, Bartfeld D, Hashmueli S, Baum G, Brill-Almon E, Galili G, Dym O, Boldin-Adamsky SA, Silman I, Sussman JL, Futerman AH, Aviezer D (2007) Production of glucocerebrosidase with terminal mannose glycans for enzyme replacement therapy of Gaucher’s disease using a plant cell system. Plant Biotechnol J 5(5):579–590PubMedCrossRefGoogle Scholar
  92. Shaaltiel Y, Yl Tekoah (2016) Plant specific N-glycans do not have proven adverse effects in humans. Nat Biotechnol 34(7):706–708PubMedCrossRefGoogle Scholar
  93. Shen BR, Zhu CH, Yao Z, Cui LL, Zhang JJ, Yang CW, He ZH, Peng XX (2017) An optimized transit peptide for effective targeting of diverse foreign proteins into chloroplasts in rice. Sci Rep 11(7):46231CrossRefGoogle Scholar
  94. Sidorov VA, Kasten D, Pang SZ, Hajdukiewicz PTJ, Staub JM, Nehra NS (1999) Stable plastid transformation in potato: use of green fluorescent protein as a plastid marker. Plant J 19:209–216PubMedCrossRefGoogle Scholar
  95. Smith EF, Townsend CO (1907) A plant tumor of bacterial origin. Science 25:671–673PubMedCrossRefGoogle Scholar
  96. Sojikul P, Buehner N, Mason HS (2003) A plant signal peptide-hepatitis B surface antigen fusion protein with enhanced stability and immunogenicity expressed in plant cells. Proc Natl Acad Sci U S A 100(5):2209–2214PubMedPubMedCentralCrossRefGoogle Scholar
  97. Staub JM, Garcia B, Graves J, Hajdukiewicz PT, Hunter P, Nehra N, Paradkar V, Schlittler M, Carroll JA, Spatola L, Ward D, Ye G, Russell DA (2000) High-yield production of a human therapeutic protein in tobacco chloroplasts. Nat Biotechnol 18(3):333–338PubMedCrossRefGoogle Scholar
  98. Staub JM, Maliga P (1992) Long regions of homologous DNA are incorporated into the tobacco plastid genome by transformation. Plant Cell 4:39–45PubMedPubMedCentralCrossRefGoogle Scholar
  99. Staub JM, Maliga P (1994) Extrachromosomal elements in tobacco plastids. Proc Natl Acad Sci U S A 91:7468–7472PubMedPubMedCentralCrossRefGoogle Scholar
  100. Svab Z, Hajdukiewicz P, Maliga P (1990) Stable transformation of plastids in higher plants. Proc Natl Acad Sci U S A 87:8526–8530PubMedPubMedCentralCrossRefGoogle Scholar
  101. Svab Z, Maliga P (1993) High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc Natl Acad Sci U S A 90:913–917PubMedPubMedCentralCrossRefGoogle Scholar
  102. Thomas TJ, Kulkarni GD, Greenfield NJ, Shirahata A, Thomas T (1996) Structural specificity effects of trivalent polyamine analogues on the stabilization and conformational plasticity of triplex DNA. Biochem J 319:591–599PubMedPubMedCentralCrossRefGoogle Scholar
  103. Thuenemann EC, Meyers AE, Verwey J, Rybicki EP, Lomonossoff GP (2013) A method for rapid production of heteromultimeric protein complexes in plants: assembly of protective bluetongue virus-like particles. Plant Biotechnol J 11(7):839–846PubMedCrossRefGoogle Scholar
  104. To KY, Cheng MC, Chen LF, Chen SC (1996) Introduction and expression of foreign DNA in isolated spinach chloroplasts by electroporation. Plant J 10(4):737–743PubMedCrossRefGoogle Scholar
  105. Tregoning JS, Clare S, Bowe F, Edwards L, Fairweather N, Qazi O, Nixon PJ, Maliga P, Dougan G, Hussell T (2005) Protection against tetanus toxin using a plant-based vaccine. Eur J Biotechnol 35(4):1320–1326Google Scholar
  106. Tzfira T, Citovsky V (2002) Partners-in-infection: host proteins involved in the transformation of plant cells by Agrobacterium. Trends Cell Biol 12(3):121–129PubMedCrossRefGoogle Scholar
  107. Tzfira T, Citovsky V (2006) Agrobacterium-mediated genetic transformation of plants: biology and biotechnology. Curr Opin Biotechnol 17(2):147–154PubMedCrossRefGoogle Scholar
  108. Tzfira T, Li J, Lacroix B, Citovsky V (2004) Agrobacterium T-DNA integration: molecules and models. Trends Genet 20(8):375–383PubMedCrossRefGoogle Scholar
  109. Valkov VT, Gargano D, Scotti N, Cardi T (2014) Plastid transformation in potato: solanum tuberosum. Methods Mol Biol 1132:295–303PubMedCrossRefGoogle Scholar
  110. van Wordragen MF, Dons HJM (1992) Agrobacterium tumefaciens-mediated transformation of recalcitrant crops. Plant Mol Biol Rep 10:12–36CrossRefGoogle Scholar
  111. Verma D, Daniell H (2007) Chloroplast vector systems for biotechnology applications. Plant Physiol 145:1129–1143PubMedPubMedCentralCrossRefGoogle Scholar
  112. Wakasugi T, Tsudzuki T, Sugiura M (2001) The genomics of land plant chloroplasts: gene content and alteration of genomic information by RNA editing. Photosynth Res 70:107–118PubMedCrossRefGoogle Scholar
  113. Wani SH, Haider N, Kumar H, Singh NB (2010) Plant plastid engineering. Curr Genomics 11:510–512CrossRefGoogle Scholar
  114. Watson J, Koya V, Leppla SH, Daniell H (2004) Expression of Bacillus anthracis protective antigen in transgenic chloroplasts of tobacco, a non-food/feed crop. Vaccine 22:4374–4384PubMedPubMedCentralCrossRefGoogle Scholar
  115. Werner S, Breus O, Symonenko Y, Marillonnet S, Gleba Y (2011) High-level recombinant protein expression in transgenic plants by using a double-inducible viral vector. Proc Natl Acad Sci U S A. 108(34):14061–14066PubMedPubMedCentralCrossRefGoogle Scholar
  116. Wirth S, Calamante G, Mentaberry A, Bussmann L, Lattanzi M, Barañao L, Bravo-Almonacid F (2004) Expression of active human epidermal growth factor (hEGF) in tobacco plants by integrative and non-integrative systems. Mol Breed 13:23CrossRefGoogle Scholar
  117. Yang J, Barr LA, Fahnestock SR, Liu ZB (2005) High yield recombinant silk-like protein production in transgenic plants through protein targeting. Transgenic Res 14(3):313–324PubMedCrossRefGoogle Scholar
  118. Zhou B, Zhang Y, Wang X, Dong J, Wang B, Han C, Yu J, Li D (2010) Oral administration of plant-based rotavirus VP6 induces antigen-specific IgAs, IgGs and passive protection in mice. Vaccine 28(37):6021–6027PubMedCrossRefGoogle Scholar
  119. Zoubenko OV, Allison LA, Svab Z, Maliga P (1994) Efficient targeting of foreign genes into the tobacco plastid genome. Nucleic Acids Res 22:3819–3824PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Verónica Araceli Márquez-Escobar
    • 1
    • 2
  • Omar González-Ortega
    • 3
  • Sergio Rosales-Mendoza
    • 1
    • 2
    Email author
  1. 1.Laboratorio de Biofarmacéuticos Recombinantes, Facultad de Ciencias QuímicasUniversidad Autónoma de San Luis PotosíSan Luis PotosíMexico
  2. 2.Sección de Biotecnología, Centro de Investigación En Ciencias de La Salud Y BiomedicinaUniversidad Autónoma de San Luis PotosíSan Luis PotosíMexico
  3. 3.Laboratorio de Bioseparaciones, Facultad de Ciencias QuímicasUniversidad Autónoma de San Luis PotosíSan Luis PotosíMexico

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