Plastid genetic engineering in Solanaceae

Protoplasma

Volumn 249, Issue 4, 2012, Pages 981-999

  Venkatesh, Jelli ^a   Park, Se Won ^a  

^a Konkuk University   (South Korea)

Author keywords

Genetic engineering; Homoplasmic; Plastid; Solanaceae; Transplastome

Indexed keywords

NICOTIANA TABACUM; SOLANACEAE;

EID: 84867142652     PISSN: 0033183X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00709-012-0391-9     Document Type: Review

References (182)

1. Afroz A, Chaudhry Z, Rashid U, Ali GM, Nazir F, Iqbal J, Khan MR (2011) Enhanced resistance against bacterial wilt in transgenic tomato (Lycopersicon esculentum) lines expressing the Xa21 gene. Plant Cell Tiss Organ Cult 104: 227-237.
2. Ahlert D, Ruf S, Bock R (2003) Plastid protein synthesis is required for plant development in tobacco. Proc Natl Acad Sci 100: 15730-15735.
3. Alergand T, Peled-Zehavi H, Katz Y, Danon A (2006) The chloroplast protein disulfide isomerase RB60 reacts with a regulatory disulfide of the RNA-binding protein RB47. Plant Cell Physiol 47: 540-548.
4. Andrews JT, Whitney SM (2003) Manipulating ribulose bisphosphate carboxylase/oxygenase in the chloroplasts of higher plants. Arch Biochem Biophys 414: 159-169.
5. Apel W, Bock R (2009) Enhancement of carotenoid biosynthesis in transplastomic tomatoes by induced lycopene to provitamin A conversion. Plant Physiol 151: 59-66.
6. Apel W, Schulze WX, Bock R (2010) Identification of protein stability determinants in chloroplasts. Plant J 63: 636-650.
7. 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: 1176-1184.
8. Arlen PA, Singleton M, Adamovicz JJ, Ding Y, Davoodi-Semiromi A, Daniell H (2008) Effective plague vaccination via oral delivery of plant cells expressing F1-V antigens in chloroplasts. Infect Immun 76: 3640-3650.
9. 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: 1474-1481.
10. Barone P, Zhang XH, Widholm JM (2009) Tobacco plastid transformation using the feedback-insensitive anthranilate synthase [α]-subunit of tobacco (ASA2) as a new selectable marker. J Exp Bot 60(11): 3195-3202.
11. Barry CS, McQuinn RP, Chung MY, Besuden A, Giovannoni JJ (2008) Amino acid substitutions in homologs of the stay-green protein are responsible for the green-flesh and chlorophyll retainer mutations of tomato and pepper. Plant Physiol 147(1): 179-187.
12. Bellucci M, De Marchis F, Mannucci R, Bock R, Arcioni S (2005) Cytoplasm and chloroplasts are not suitable subcellular locations for β-zein accumulation in transgenic plants. J Exp Bot 56: 1205-1212.
13. Berger IJ, Carraro DM, Bock R, Azevedo RA, Carrer H (2005) Cloning and sequence analysis of tomato cpDNA fragments: towards developing homologous chloroplast transformation vectors. Braz J Plant Physiol 17: 239-245.
14. Biggin P, Sansom M (1999) Interactions of α-helices with lipid bilayers: a review of simulation studies. Biophys Chem 76: 161-183.
15. Birch-Machin I, Newell CA, Hibberd JM, Gray JC (2004) Accumulation of rotavirus VP6 protein in chloroplasts of transplastomic tobacco is limited by protein stability. Plant Biotechnol J 2: 261-270.
16. Bock R (2001) Transgenic plastids in basic research and plant. J Mol Biol 312: 425-438.
17. Bock R (2007) Plastid biotechnology: prospects for herbicide and insect resistance, metabolic engineering and molecular farming. Curr Opin Biotechnol 18: 100-106.
18. Bock R, Khan MS (2004) Taming plastids for a green future. Trends Biotechnol 22: 311-318.
19. Bock R, Maliga P (1995) In vivo testing of a tobacco plastid DNA segment for guide RNA function in psbL editing. Molec Gen Genet 247: 439-443.
20. Bock R, Warzecha H (2010) Solar-powered factories for new vaccines and antibiotics. Trends Biotechnol 28: 246-252.
21. Bohmert-Tatarev K, McAvoy S, Daughtry S, Peoples OP, Snell KD (2011) High levels of bioplastic are produced in fertile transplastomic tobacco plants engineered with a synthetic operon for the production of polyhydroxybutyrate. Plant Physiol 155(4): 1690-1708.
22. Bornke F, Broer I (2010) Tailoring plant metabolism for the production of novel polymers and platform chemicals. Curr Opin Plant Biol 13: 354-362.
23. Boyhan D, Daniell H (2011) Low-cost production of proinsulin in tobacco and lettuce chloroplasts for injectable or oral delivery of functional insulin and C-peptide. Plant Biotechnol J 9: 585-598. doi: 10. 1111/j. 1467-7652. 2010. 00582. x.
24. Boynton JE, Gillham NW, Harris EH, Hosler JP, Johnson AM, Jones AR, Randolph-Anderson BL, Robertson D, Klein TM, Shark KB et al (1988) Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science 240: 1534-1538.
25. Brosch M, Krause K, Falk J, Krupinska K (2007) Analysis of gene expression in amyloplasts of potato tubers. Planta 227: 91-99.
26. Chakrabarti SK, Lutz KA, Lertwiriyawong B, Svab Z, Maliga P (2006) Expression of the cry9Aa2 B. t. gene in tobacco chloroplasts confers resistance to potato tuber moth. Transgenic Res 15: 481-488.
27. Craig W, Lenzi P, Scotti N, De Palma M, Saggese P, Carbone V, McGrath-Curran N, Magee AM, Medgyesy P, Kavanagh TA, Dix PJ, Grillo S, Cardi T (2008) Transplastomic tobacco plants expressing a fatty acid desaturase gene exhibit altered fatty acid profiles and improved cold tolerance. Transgenic Res 17: 769-782.
28. Daniell H (2006) Production of biopharmaceuticals and vaccines in plants via the chloroplast genome. Biotechnol J 1: 1071-1079.
29. Daniell H (2007) Transgene containment by maternal inheritance: effective or elusive? Proc Natl Acad Sci 104(17): 6879-6880.
30. Daniell H, McFadden BA (1987) Uptake and expression of bacterial and cyanobacterial genes by isolated cucumber etioplasts. Proc Natl Acad Sci 84: 6349-6353.
31. Daniell H, Wiebe PO, Fernandez-San Millan A (2001a) Antibiotic-free chloroplast genetic engineering-an environmentally friendly approach. Trends Plant Sci 6(6): 237-239.
32. Daniell H, Lee SB, Panchal T, Wiebe PO (2001b) Expression of cholera toxin B subunit gene and assembly as functional oligomers in transgenic tobacco chloroplasts. J Mol Biol 311: 1001-1009.
33. Daniell H, Singh ND, Mason H, Streatfield SJ (2009) Plant-made vaccine antigens and biopharmaceuticals. Trends Plant Sci 14: 669-679.
34. Dauvillee D, Delhaye S, Gruyer S, Slomianny C, Moretz SE et al (2010) Engineering the chloroplast targeted malarial vaccine antigens in Chlamydomonas starch granules. PLoS One 5(12): e15424. doi: 10. 1371/journal. pone. 0015424.
35. Day A, Goldschmidt-Clermont M (2011) The chloroplast transformation toolbox: selectable markers and marker removal. Plant Biotechnol J 9: 540-553.
36. De Cosa B, Moar W, Lee SB, Miller M, Daniel H (2001) Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat Biotechnol 19: 71-74.
37. DeGray G, Rajasekaran K, Smith F, Sanford J, Daniell H (2001) Expression of an antimicrobial peptide via the chloroplast genome to control phytopathogenic bacteria and fungi. Plant Physiol 127: 852-862.
38. Demanèche S, Sanguin H, Poté J, Navarro E, Bernillon D, Mavingui P, Wildi W et al (2008) Antibiotic-resistant soil bacteria in transgenic plant fields. Proc Natl Acad Sci 105: 3957-3962.
39. 2+ ion. Protein Eng 11: 557-581.
40. Dhingra A, Portis AR, Daniell H (2004) Enhanced translation of a chloroplast-expressed RbcS gene restores the subunit levels and photosynthesis in nuclear RbcS antisense plants. Proc Natl Acad Sci 101: 6315-6320.
41. Dufourmantel N, Dubald M, Matringe M, Canard H, Garcon F, Job C, Kay E, Wisniewski JP, Ferullo JM, Pelissier B, Sailland A, Tissot G (2007) Generation and characterization of soybean and markerfree tobacco plastid transformants over- expressing a bacterial 4- hydroxyphenylpyruvate dioxygenase which provides strong herbicide tolerance. Plant Biotechnol J 5: 118-133.
42. Eibl C, Zou Z, Beck A, Kim M, Mullet J, Koop HU (1999) In vivo analysis of plastid psbA, rbcL and rpl32 UTR elements by chloroplast transformation: tobacco plastid gene expression is controlled by modulation of transcript levels and translation efficiency. Plant J 19: 333-345.
43. Elghabi Z, Ruf S, Bock R (2011a) Biolistic co-transformation of the nuclear and plastid genomes. Plant J 67: 941-948.
44. Elghabi Z, Karcher D, Zhou F, Ruf S, Bock R (2011b) Optimization of the expression of the HIV fusion inhibitor. cyanovirin-N from the tobacco plastid genome. Plant Biotechnol J 9: 599-608.
45. Falk J, Brosch M, Schäfer A, Braun S, Krupinska K (2005) Characterization of transplastomic tobacco plants with a plastid localized barley 4-hydroxyphenylpyruvate dioxygenase. J Plant Physiology 162: 738-742.
46. Fernandez-San Millan A, Mingo-Castel A, Miller M, Daniell H (2003) A chloroplast transgenic approach to hyper-express and purify human serum albumin, a protein highly susceptible to proteolytic degradation. Plant Biotechnol J 1: 71-79.
47. Garcia I, Rodgers M, Pepin R, Hsieh TF, Matringe M (1999) Characterization and subcellular compartmentation of recombinant 4-hydroxyphenylpyruvate dioxygenase from Arabidopsis in transgenic tobacco. Plant Physiol 119: 1507-1516.
48. Gargano D, Craig W, Lenzi P, Scotti N, Grillo S, Cardi T (2003) Stable plastid transformation of potato cv. Desiree with a gene involved in fatty acid desaturation. Proceedings of the XLVII Italian Society of Agricultural Genetics- SIGA Annual Congress, Verona, 24-27. September, 2003. ISBN 88-900622-4-X.
49. Gargano D, Valkov V, Lenzi P, Scotti N, Grillo S, Cardi T (2005) Development and application of the plastid transformation technology in potato. Oral Communication Abstract, Proceedings of the XLIX Italian Society of Agricultural Genetics Annual Congress, Potenza, Italy - 12/15 September, 2005, ISBN 88-900622-6-6.
50. Genkov T, Meyer M, Griffiths H, Spreitzer RJ (2010) Functional hybrid Rubisco enzymes with plant small subunits and algal large subunits: engineered rbcS cDNA for expression in Chlamydomonas. J Biol Chem 285: 19833-19841.
51. Girhepuje PV, Shinde GB (2011) Transgenic tomato plants expressing a wheat endochitinase gene demonstrate enhanced resistance to Fusarium oxysporum f. sp. Lycopersici. Plant Cell Tiss Organ Cult 105: 243-251.
52. Glick BR, Pasternak JJ (1998) Molecular biotechnology: principles and applications of recombinant DNA. American Society for Microbiology, Washington, DC.
53. Goldschmidt-Clermont M (1991) Transgenic expression of aminoglycoside adenine transferase in the chloroplast: a selectable marker of site-directed transformation of Chlamydomonas. Nucleic Acids Res 19: 4083-4089.
54. Gorantala J, Grover S, Goel D, Rahi A, Magani SKJ, Chandra S, Bhatnagar R (2011) A plant based protective antigen [PA(dIV)] vaccine expressed in chloroplasts demonstrates protective immunity in mice against anthrax. Vaccine 29(27): 4521-4533.
55. Gray BN, Ahner BA, Hanson MR (2009) Extensive homologous recombination between introduced and native regulatory plastid DNA elements in transplastomic plants. Transgenic Res 18: 559-572.
56. Gray BN, Yang H, Ahner BA, Hanson MR (2011) An efficient downstream box fusion allows high-level accumulation of active bacterial beta-glucosidase in tobacco chloroplasts. Plant Mol Biol 76(3-5): 345-355.
57. Guda C, Lee SB, Daniell H (2000) Stable expression of a biodegradable protein-based polymer in tobacco chloroplasts. Plant Cell Rep 19: 257-262.
58. Hagemann R (2002) Milestones in plastid genetics of higher plants. In: Esser K, Lüttge U, Beyschlag W, Hellwig F (eds) Progress in botany: genetics, physiology, ecology, vol 63. Springer, Heidelberg, pp 5-51.
59. Haseloff J, Siemering KR (1998) The uses of GFP in plants. In: Chalfie M, Kain S (eds) Green fluorescence protein: strategies, applications and protocols. Wiley-Liss, New York, pp 191-220.
60. Hennig A, Bonfig K, Roitsch T, Warzecha H (2007) Expression of the recombinant bacterial outer surface protein A in tobacco chloroplasts leads to thylakoid localization and loss of photosynthesis. FEBS J 274: 5749-5758.
61. Herrin DL, Nickelsen J (2004) Chloroplast RNA processing and stability. Photosynth Res 82: 301-304.
62. Hibberd JM, Linley PJ, Khan MS, Gray JC (1998) Transient expression of green fluorescent protein in various plastid types following microprojectile bombardment. Plant J 16: 627-632.
63. Houston ME Jr, Kondejevski L, Gough M, Fidai S, Hodges RS, Hancock R (1997) Influence of performed α-helix and α-helix induction on the activity of cationic antimicrobial peptides. J Pept Res 52: 81-88.
64. Huang CY, Ayliffe MA, Timmis JN (2003) Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422: 72-76.
65. Huhns M, Neumann K, Hausmann T, Ziegler K, Klemke F, Kahmann U, Staiger D, Lockau W, Pistorius EK, Broer I (2008) Plastid targeting strategies for cyanophycin synthetase to achieve high-level polymer accumulation in Nicotiana tabacum. Plant Biotechnol J 6: 321-336.
66. Huhns M, Neumann K, Hausmann T, Klemke F, Lockau W, Kahmann U et al (2009) Tuber-specific cphA expression to enhance cyanophycin production in potatoes. Plant Biotechnol J 7(9): 883-898.
67. Iamtham S, Day A (2000) Removal of antibiotic resistance genes from transgenic tobacco plastids. Nat Biotechnol 18: 1172-1176.
68. Kahlau S, Bock R (2008) Plastid transcriptomics and translatomics of tomato fruit development and chloroplast-to-chromoplast differentiation: chromoplast gene expression largely serves the production of a single protein. Plant Cell 20: 856-874.
69. Kanevski I, Maliga P, Rhoades DF, Gutteridge S (1999) Plastome engineering of ribulose-1, 5-bisphosphatecarboxylase/oxygenase in tobacco to form a sunflower large subunit and tobacco small subunit hybrid. Plant Physiol 119: 133-141.
70. Kim J, Mayfield SP (2002) The active site of the thioredoxin-like domain of chloroplast protein disulfide isomerase, RB60, catalyzes the redox-regulated binding of chloroplast poly(A)-binding protein, RB47, to the 5' untranslated region of psbA mRNA. Plant Cell Physiol 43(10): 1238-1243.
71. Kinney AJ (2006) Metabolic engineering in plants for human health and nutrition. Curr Opin Biotechnol 17: 130-138.
72. Klaus SMJ, Huang FC, Eibl C, Koop HU, Golds TJ (2003) Rapid and proven production of transplastomic tobacco plants by restoration of pigmentation and photosynthesis. Plant J 35(6): 811-821.
73. Klaus SM, Huang FC, Golds TJ, Koop HU (2004) Generation of marker-free plastid transformants using a transiently cointegrated selection gene. Nat Biotechnol 22: 225-229.
74. Knoblauch M, Hibberd JM, Gray JC, van Bel AJE (1999) A galinstan expansion femtosyringe for microinjection of eukaryotic organelles and prokaryotes. Nat Biotechnol 17: 906-909.
75. Kode V, Mudd EA, Iamtham S, Day A (2006) Isolation of precise plastid deletion mutants by homology-based excision: a resource for site-directed mutagenesis, multi-gene changes and high-throughput plastid transformation. Plant J 46: 901-909.
76. Koehler RH, Zipfel WR, Webb WW, Hanson MR (1997) The green fluorescent protein as a marker to visualize plant mitochondria in vivo. Plant J 11: 613-621.
77. Koop HU, Steinmüller K, Wagner H, Rössler C, Eibl C, Sacher L (1996) Integration of foreign sequences into the tobacco plastome via polyethylene glycol-mediated protoplast transformation. Planta 199: 193-201.
78. Kooter JM, Matzke MA, Meyer P (1999) Listening to the silent genes: transgene silencing, gene regulation and pathogen control. Trends Plant Sci 4: 340-347.
79. Koya V, Moayeri M, Leppla SH, Daniell H (2005) Plant-based vaccine: mice immunized with chloroplast-derived anthrax protective antigen survive anthrax lethal toxin challenge. Infect Immun 73: 8266-8274.
80. Kuchuk N, Sytnyk K, Vasylenko M, Shakhovsky A, Komarnytsky I, Kushnir S, Gleba Y (2006) Genetic transformation of plastids of different Solanaceae species using tobacco cells as organelle hosts. Theor Appl Genet 113: 519-527.
81. Lee SB, Kwon HB, Kwon SJ, Park SC, Jeong MJ, Han SE, Byun MO, Daniell H (2003) Accumulation of trehalose within transgenic chloroplasts confers drought tolerance. Mol Breed 11: 1-13.
82. Lee M, Zhou Y, Lung R, Chye ML, Yip WK, Zee SY, Lam E (2006) Expression of viral capsid protein antigen against Epstein-Barr virus in plastids of Nicotiana tabacum cv. SR1. Biotechnol Bioeng 20: 1129-1137.
83. Lee SB, Li B, Jin S, Daniell H (2011) Expression and characterization of antimicrobial peptides Retrocyclin-101 and Protegrin-1 in chloroplasts to control viral and bacterial infections. Plant Biotechnol J 9: 100-115.
84. Lenzi P, Scotti N, Alagna F, Tornesello ML, Pompa A, Vitale A, De Stradis A, Monti L, Grillo S, Buonaguro FM, Maliga P, Cardi (2008) Translational fusion of chloroplast-expressed human papillomavirus type 16 L1 capsid protein enhances antigen accumulation in transplastomic tobacco. Transgenic Res 17(6): 1091-1102.
85. Li W, Ruf S, Bock R (2011) Chloramphenicol acetyltransferase as selectable marker for plastid transformation. Plant Mol Biol 76: 443-451.
86. Lloyd AH, Timmis JN (2011) The origin and characterization of new nuclear genes originating from a cytoplasmic organellar genome. Mol Biol Evol 28(7): 2019-2028.
87. Lopez AB, van Eck J, Conlin BJ, Paolillo DJ, O'Neill J, Li L (2008) Effect of the cauliflower Or transgene on carotenoid accumulation and chromoplast formation in transgenic potato tubers. J Exp Bot 59: 213-223.
88. Lössl AG, Waheed MT (2011) Chloroplast-derived vaccines against human diseases: achievements, challenges and scopes. Plant Biotechnol J 9: 527-539.
89. Lossl A, Eibl C, Harloff HJ, Jung C, Koop HU (2003) Polyester synthesis in transplastomic tobacco (Nicotiana tabacum L.): significant contents of polyhydroxybutyrate are associated with growth reduction. Plant Cell Rep 21: 891-899.
90. Lossl A, Bohmert K, Harloff H, Eibl C, Mühlbauer S, Koop HU (2005) Inducible trans-activation of plastid transgenes: expression of the Reutropha phb operon in transplastomic tobacco. Plant Cell Physiol 46(9): 1462-1471.
91. Lu S, Li L (2008) Carotenoid metabolism: biosynthesis, regulation, and beyond. J Integr Plant Biol 50: 778-785.
92. Ludwig DS, Holmes RK, Schoolnik GK (1985) Chemical and immunochemical studies on the receptor binding domain of cholera toxin B subunit. J Biol Chem 260: 12528-12534.
93. Lutz KA, Maliga P (2007) Construction of marker-free transplastomic plants. Curr Opin Biotechnol 18: 107-114.
94. Lutz KA, Knapp JE, Maliga P (2001) Expression of bar in the plastid genome confers herbicide resistance. Plant Physiol 125: 1585-1590.
95. Lutz KA, Azhagiri AK, Tungsuchat-Huang T, Maliga P (2007) A guide to choosing vectors for transformation of the plastid genome of higher plants. Plant Physiol 145: 1201-1210.
96. Madoka Y, Tomizawa KI, Miozoi J, Nishida I, Nagano Y, Sasaki Y (2002) Chloroplast transformation with modified accD operon increases acetyl-CoA carboxylase and causes extension of leaf longevity and increase in seed yield in tobacco. Plant Cell Physiol 43: 1518-1525.
97. Magee AM, Coyne S, Murphy D, Horvath EM, Medgyesy P, Kavanagh TA (2004) T7 RNA polymerase-directed expression of an antibody fragment transgene in plastids causes a semi-lethal pale-green seedling phenotype. Transgenic Res 13: 325-337.
98. Maliga P (2004) Plastid transformation in higher plants. Annu Rev Plant Physiology Plant Mol Biol 55: 289-313.
99. Maliga P, Bock R (2011) Plastid biotechnology: food, fuel, and medicine for the 21st century. Plant Physiol 155(4): 1501-1510.
100. Matsushima R, Hu Y, Toyoda K, Sodmergen SW (2008) The model plant Medicago truncatula exhibits biparental plastid inheritance. Plant Cell Physiol 49(1): 81-91.
101. McBride KE, Svab Z, Schaaf DJ, Hogan PS, Stalker DM, Maliga P (1995) Amplification of a chimeric Bacillus gene in chloroplasts leads to an extraordinary level of an insecticidal protein in tobacco. Bio/Technology 13: 362-365.
102. McCabe MS, Klaas M, Gonzalez-Rabade N, Poage M, Badillo-Corona JA, Zhou F, Karcher D, Bock R, Gray JC, Dix PJ (2008) Plastid transformation of high-biomass tobacco variety Maryland Mammoth for production of human immunodeficiency virus type 1 (HIV-1) p24 antigen. Plant Biotechnol J 6: 914-929.
103. Meiyalaghan S, Pringle JM, Barrell PJ, Jacobs JME, Conner AJ (2010) Pyramiding transgenes for potato tuber moth resistance in potato. Plant Biotechnol Rep 4: 293-301.
104. Meyer L, Serek M, Winkelmann T (2009) Protoplast isolation and plant regeneration of different genotypes of Petunia and Calibrachoa. Plant Cell Tiss Organ Cult 99: 27-34.
105. Molina A, Veramendi J (2009) High stability of recombinant proteins expressed in tobacco chloroplasts. Open Biotechnol J 3: 67-72.
106. Morgenfeld M, Segretin ME, Wirth S, Lentz E, Zelada A, Mentaberry A, Gissmann L, Bravo-Almonacid F (2009) Potato virus X coat protein fusion to human papillomavirus 16 E7 oncoprotein enhance antigen stability and accumulation in tobacco chloroplast. Mol Biotechnol 43: 243-249.
107. 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: 1688-1691.
108. Neumann K, Stephan DP, Ziegler K, Hühns M, Broer I, Lockau W, Pistorius EK (2005) Production of cyanophycin, a suitable source for the biodegradable polymer polyaspartate, in transgenic plants. Plant Biotechnol J 3: 249-258.
109. Nguyen TT, Nugent G, Cardi T, Dix PJ (2005) Generation of homoplasmic plastid transformants of a commercial cultivar of potato (Solanum tuberosum L.). Plant Sci 168: 1495-1500.
110. Nugent JM, Joyce SM (2005) Producing human therapeutic proteins in plastids. Curr Pharm Des 11: 2459-2470.
111. Nugent GD, Ten Have M, van der Gulik A, Dix PJ, Uijtewaal BA, Mordhorst AP (2005) Plastid transformants of tomato selected using mutations affecting ribosome structure. Plant Cell Rep 24: 341-349.
112. 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: 729-738.
113. Oey M, Lohse M, Kreikemeyer B, Bock R (2009) Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. Plant J 57: 436-445.
114. Parry MAJ, Madgwick PJ, Carvalho JFC, Andralojc PJ (2007) Prospects for increasing photosynthesis by overcoming the limitations of Rubisco. J Agric Sci 145: 31-43.
115. Penna S, Sagi L, Swennen R (2002) Positive selectable marker genes for routine plant transformation. In Vitro Cell Dev Biol-Plant 38: 125-128.
116. Petersen K, Bock R (2011) High-level expression of a suite of thermostable cell wall-degrading enzymes from the chloroplast genome. Plant Mol Biol 76: 311-321.
117. Petersen K, Schöttler MA, Karcher D, Thiele W, Bock R (2011) Elimination of a group II intron from a plastid gene causes a mutant phenotype. Nucl Acids Res 39(12): 5181-5192.
118. Poage M, Martret L, Jansen MAK, Nugent GD, Dix PJ (2011) Modification of reactive oxygen species scavenging capacity of chloroplasts through plastid transformation. Plant Mol Biol 76: 371-384.
119. Pogson BJ, Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development: an overview. Plant Physiol 155(4): 1545-1551.
120. Quesada-Vargas T, Ruiz ON, Daniell H (2005) Characterization of heterologous multigene operons in transgenic chloroplasts. Transcription, processing, and translation. Plant Physiol 138: 1746-1762.
121. Raines CA (2006) Transgenic approaches to manipulate the environmental responses of the C3 carbon fixation cycle. Plant Cell Environ 29: 331-339.
122. Rathinasabapathi B, McCue KF, Gage DA, Hanson AD (1994) Metabolic engineering of glycine betaine synthesis: plant betaine aldehyde dehydrogenases lacking typical transit peptides are targeted to tobacco chloroplasts where they confer betaine aldehyde resistance. Planta 193: 155-162.
123. Robinson SP, Jones GP (1986) Accumulation of glycine betaine in chloroplasts provides osmotic adjustment during salt stress. Aust J Plant Physiology 13: 659-668.
124. Roca M, Hornero-Méndez D, Gandul-Rojas B, Mínguez-Mosquera MI (2006) Stay-Green phenotype slows the carotenogenic process in Capsicum annuum (L.) Fruits. J Agric Food Chem 54(23): 8782-8787.
125. Rogalski M, Carrer H (2011) Engineering plastid fatty acid biosynthesis to improve food quality and biofuel production in higher plants. Plant Biotechnol J 9(5): 554-564.
126. Rogalski M, Ruf S, Bock R (2006) Tobacco plastid ribosomal protein S18 is essential for cell survival. Nucleic Acids Res 34: 4537-4545.
127. Ruf S, Hermann M, Berger I, Carrer H, Bock R (2001) Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nat Biotechnol 19: 870-875.
128. Ruf S, Karcher D, Bock R (2007) Determining the transgene containment level provided by chloroplast transformation. Proc Natl Acad Sci 104(17): 6998-7002.
129. 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: 495-510.
130. Ruhlman T, Verma D, Samson N, Daniell H (2010) The role of heterologous chloroplast sequence elements in transgene integration and expression. Plant Physiol 152: 2088-2104.
131. Ruiz ON, Daniell H (2005) Engineering cytoplasmic male sterility via the chloroplast genome by expression of β-ketothiolase. Plant Physiol 138(3): 1232-1246.
132. Sanford JC, Smith FD, Russell JA (1993) Optimizing the biolistic process for different biological applications. Methods Enzymol 217: 483-509.
133. Schädlich L, Senger T, Gerlach B, Mücke N, Klein C, Bravo IG, Müller M, Gissmann L (2009) Analysis of modified human papillomavirus type 16 L1 capsomeres: the ability to assemble into larger particles correlates with higher immunogenicity. J Virol 83: 7690-7705.
134. Scheller J, Conrad U (2005) Plant-based material, protein and biodegradable plastic. Curr Opin Plant Biol 8: 188-196.
135. Schiraldi C, DiLernia I, DeRosa M (2002) Trehalose production: exploiting novel approaches. Trends Biotechnol 20: 420-425.
136. Scotti N, Valkov VT, Cardi T (2011) Improvement of plastid transformation efficiency in potato by using vectors with homologous flanking sequences. GM Crops 2(2): 89-91.
137. Segretin ME, Lentz EM, Wirth SA, Morgenfeld MM, Bravo-Almonacid FF (2011) Transformation of Solanum tuberosum plastids allows high expression levels of β-glucuronidase both in leaves and microtubers developed in vitro. Planta. doi: 10. 1007/s00425-011-1541-6.
138. Sheppard AE, Madesis P, Lloyd AH, Day A, Ayliffe MA, Timmis JN (2011) Introducing an RNA editing requirement into a plastid-localised transgene reduces but does not eliminate functional gene transfer to the nucleus. Plant Mol Bio l 76: 299-309.
139. Sidorov VA, Kasten D, Pang SZ, Hajdukiewicz PTJ, Staub JM, Nehra NS (1999) Stable chloroplast transformation in potato: use of green fluorescent protein as a plastid marker. Plant J 19: 209-216.
140. Sigeno A, Hayashi S, Terachi T, Yamagishi H (2009) Introduction of transformed chloroplasts from tobacco into petunia by asymmetric cell fusion. Plant Cell Rep 28: 1633-1640.
141. Sim JS, Pak HK, Kim DS, Lee SB, Kim YH, Hahn BS (2009) Expression and characterization of synthetic heat-labile enterotoxin b subunit and hemagglutinin-neuraminidase-neutralizing epitope fusion protein in Escherichia coli and tobacco chloroplasts. Plant Mol Biol Rep 27: 388-399.
142. Singh AK, Verma SS, Bansal KC (2010) Plastid transformation in eggplant (Solanum melongena L.). Transgenic Res 19: 113-119.
143. Soria-Guerra RE, Alpuche-Solis AG, Rosales-Mendoza S, Moreno-Fierros L, Bendik EM, Martinez-Gonzalez L, Korban SS (2009) Expression of a multi-epitope DPT fusion protein in transplastomic tobacco plants retains both antigenicity and immunogenicity of all three components of the functional oligomer. Planta 229: 1293-1302.
144. Spreitzer RJ, Salvucci ME (2002) Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53: 449-475.
145. Staub JM, Maliga P (1995) Expression of a chimeric uidA gene indicates that polycistronic mRNAs are efficiently translated in tobacco plastids. Plant J 7: 845-848.
146. 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: 333-338.
147. Stegemann S, Bock R (2006) Experimental reconstruction of functional gene transfer from the tobacco plastid genome to the nucleus. Plant Cell 18: 2869-2878.
148. Stegemann S, Hartmann S, Ruf S, Bock R (2003) High-frequency gene transfer from the chloroplast genome to the nucleus. Proc Natl Acad Sci 100(15): 8828-8833.
149. Svab Z, Maliga P (1991) Mutation proximal to the tRNA binding region of the Nicotiana plastid 16S rRNA confers resistance to spectinomycin. Mol Gen Genet 228: 316-319.
150. Svab Z, Maliga P (1993) High frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc Natl Acad Sci 90: 913-917.
151. Svab Z, Maliga P (2007) Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment. Proc Natl Acad Sci 104: 7003-7008.
152. Svab Z, Hajdukiewicz P, Maliga P (1990) Stable transformation of plastids in higher plants. Proc Natl Acad Sci 87: 8526-8530.
153. Talianova M, Janousek B (2011) What can we learn from tobacco and other Solanaceae about horizontal DNA transfer? Am J Bot 98(8): 1231-1242.
154. Tregoning JS, Nixon P, Kuroda H, Svab Z, Clare S, Bowe F, Fairweather N, Ytterberg J, van Wijk KJ, Dougan G, Maliga P (2003) Expression of tetanus toxin fragment C in tobacco chloroplasts. Nucleic Acids Res 31: 1174-1179.
155. Upadhyaya CP, Nookaraju A, Gururani MA, Upadhyaya DC, Kim DH, Chun SC, Park SW (2010) An update on the progress towards the development of marker-free transgenic plants. Botanical Studies 51(3): 277-292.
156. Valkov T, Scotti N, Kahlau S, MacLean D, Grillo S, Gray JC, Bock R, Cardi T (2009) Genome-wide analysis of plastid gene expression in potato leaf chloroplasts and tuber amyloplasts: transcriptional and posttranscriptional control. Plant Physiol 150: 2030-2044.
157. Valkov VT, Gargano D, Manna C, Formisano G, Dix PJ, Gray JC, Scotti N, Cardi T (2011) High efficiency plastid transformation in potato and regulation of transgene expression in leaves and tubers by alternative 5' and 3' regulatory sequences. Transgenic Res 20: 137-151.
158. van Beilen JB (2008) Transgenic plant factories for the production of biopolymers and platform chemicals. Biofuels Bioprod Biorefining 2(3): 215-228.
159. van Bel AJE, Hibberd J, Prüfer D, Knoblauch M (2001) Novel approach in plastid transformation. Curr Opin Biotechnol 12: 144-149.
160. van Wijk KJ, Baginsky S (2011) Plastid proteomics in higher plants: current state and future goals. Plant Physiol 155(4): 1578-1588.
161. Verhounig A, Karcher D, Bock R (2010) Inducible gene expression from the plastid genome by a synthetic riboswitch. Proc Natl Acad Sci 107: 6204-6209.
162. Verma D, Daniell H (2007) Chloroplast vector systems for biotechnology applications. Plant Physiol 145: 1129-1143.
163. Verma D, Samson NP, Koya V, Daniell H (2008) A protocol for expression of foreign genes in chloroplasts. Nat Protoc 3: 739-758.
164. Von Caemmerer S, Evans JR (2010) Enhancing C3 photosynthesis. Plant Physiol 154: 589-592.
165. Waheed MT, Thönes N, Müller M, Hassan SW, Razavi NM, Lössl E, Kaul HP, Lössl AG (2011) Transplastomic expression of a modified human papillomavirus L1 protein leading to the assembly of capsomeres in tobacco: a step towards cost-effective second-generation vaccines. Transgenic Res 20: 271-282.
166. Waterer D, Benning NT, Wu G, Luo X, Liu X, Gusta M, McHughen A, Gusta LV (2010) Evaluation of abiotic stress tolerance of genetically modified potatoes (Solanum tuberosum cv. Desiree). Mol Breed 25: 527-540.
167. 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: 4374-4384.
168. Weeda SM, Kumar GNM, Knowles NR (2009) Developmentally linked changes in proteases and protease inhibitors suggest a role for potato multicystatin in regulating protein content of potato tubers. Planta 230: 73-84.
169. Wei Z, Liu Y, Lin C, Wang Y, Cai Q, Dong Y, Xing S (2011) Transformation of alfalfa chloroplasts and expression of green fluorescent protein in a forage crop. Biotechnol Lett 33: 2487-2494. doi: 10. 1007/s10529-011-0709-2.
170. Whitney SM, Andrews TJ (2001) The gene for the ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco) small subunit relocated to the plastid genome of tobacco directs the synthesis of small subunits that assemble into Rubisco. Plant Cell 13: 193-205.
171. Whitney SM, Sharwood RE (2008) Construction of a tobacco master line to improve Rubisco engineering in chloroplasts. J Exp Bot 59: 1909-1921.
172. 2-sequestering enzyme, Rubisco. Plant Physiol 155(1): 27-35.
173. Wurbs D, Ruf S, Bock R (2007) Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome. Plant J 49: 276-288.
174. Xia XX, Qiana ZG, Kib CS, Park YH, Kaplan DL, Lee SY (2010) Native-sized recombinant spider silk protein produced in metabolically engineered Escherichia coli results in a strong fiber. Proc Natl Acad Sci 107: 14059-14063.
175. Ye GN, Hajdukiewicz PT, Broyles D, Rodriguez D, Xu CW, Nehra N, Staub JM (2001) Plastid-expressed 5-enolpyruvylshikimate-3-phosphate synthase genes provide high level glyphosate tolerance in tobacco. Plant J 25: 261-270.
176. Ye GN, Colburn SM, Xu CW, Hajdukiewicz PTJ, Staub JM (2003) Persistence of unselected transgenic DNA during a plastid transformation and segregation approach to herbicide resistance. Plant Physiol 133: 402-410.
177. Zhang XH, Ewy RG, Widholm JM, Portis AR Jr (2002) Complementation of the nuclear antisense rbcS-induced photosynthesis deficiency by introducing an rbcS gene into the tobacco plastid genome. Plant Cell Physiol 43: 1302-1313.
178. Zhang J, Tan W, Yang XH, Zhang HX (2008) Plastid-expressed choline monooxygenase gene improves salt and drought tolerance through accumulation of glycine betaine in tobacco. Plant Cell Rep 27: 1113-1124.
179. Zhang XH, Webb J, Huang YH, Lin L, Tang RS, Liu A (2011) Hybrid Rubisco of tomato large subunits and tobacco small subunits is functional in tobacco plants. Plant Sci 180: 480-488.
180. Zhou F, Karcher D, Bock R (2007) Identification of a plastid intercistronic expression element (IEE) facilitating the expression of stable translatable monocistronic mRNAs from operons. Plant J 52: 961-972.
181. Zhou F, Badillo-Corona JA, Karcher D, Gonzalez-Rabade N, Piepenburg K, Borchers AMI, Maloney AP, Kavanagh TA, Gray JC, Bock R (2008) High-level expression of human immunodeficiency virus antigens from the tobacco and tomato plastid genomes. Plant Biotechnol J 6: 897-913.
182. Zubko MK, Zubko EI, Zuilen K, Meyer P, Day A (2004) Stable transformation of petunia plastids. Transgenic Res 13: 523-530.