1932

Abstract

The small bacterial-type genome of the plastid (chloroplast) can be engineered by genetic transformation, generating cells and plants with transgenic plastid genomes, also referred to as transplastomic plants. The transformation process relies on homologous recombination, thereby facilitating the site-specific alteration of endogenous plastid genes as well as the precisely targeted insertion of foreign genes into the plastid DNA. The technology has been used extensively to analyze chloroplast gene functions and study plastid gene expression at all levels in vivo. Over the years, a large toolbox has been assembled that is now nearly comparable to the techniques available for plant nuclear transformation and that has enabled new applications of transplastomic technology in basic and applied research. This review describes the state of the art in engineering the plastid genomes of algae and land plants (Embryophyta). It provides an overview of the existing tools for plastid genome engineering, discusses current technological limitations, and highlights selected applications that demonstrate the immense potential of chloroplast transformation in several key areas of plant biotechnology.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-050213-040212
2015-04-29
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/arplant/66/1/annurev-arplant-050213-040212.html?itemId=/content/journals/10.1146/annurev-arplant-050213-040212&mimeType=html&fmt=ahah

Literature Cited

  1. Ahlert D, Ruf S, Bock R. 1.  2003. Plastid protein synthesis is required for plant development in tobacco. PNAS 100:15730–35 [Google Scholar]
  2. Albus C, Ruf S, Schöttler MA, Lein W, Kehr J, Bock R. 2.  2010. Y3IP1, a nucleus-encoded thylakoid protein, co-operates with the plastid-encoded Ycf3 protein in photosystem I assembly. Plant Cell 22:2838–55 [Google Scholar]
  3. Alkatib S, Fleischmann TT, Scharff LB, Bock R. 3.  2012. Evolutionary constraints on the plastid tRNA set decoding methionine and isoleucine. Nucleic Acids Res. 40:6713–24 [Google Scholar]
  4. Alkatib S, Scharff LB, Rogalski M, Fleischmann TT, Matthes A. 4.  et al. 2012. The contributions of wobbling and superwobbling to the reading of the genetic code. PLOS Genet. 8:e1003076 [Google Scholar]
  5. Allison LA, Maliga P. 5.  1995. Light-responsive and transcription-enhancing elements regulate the plastid psbD core promoter. EMBO J. 14:3721–30 [Google Scholar]
  6. Apel W, Bock R. 6.  2009. Enhancement of carotenoid biosynthesis in transplastomic tomatoes by induced lycopene-to-provitamin A conversion. Plant Physiol. 151:59–66 [Google Scholar]
  7. Apel W, Schulze WX, Bock R. 7.  2010. Identification of protein stability determinants in chloroplasts. Plant J. 63:636–50 [Google Scholar]
  8. Arlen PA, Singleton M, Adamovicz JJ, Ding Y, Davoodi-Semiromi A, Daniell H. 8.  2008. Effective plague vaccination via oral delivery of plant cells expressing F1-V antigens in chloroplasts. Infect. Immun. 76:3640–50 [Google Scholar]
  9. Ayliffe MA, Scott NS, Timmis JN. 9.  1998. Analysis of plastid DNA-like sequences within the nuclear genomes of higher plants. Mol. Biol. Evol. 15:738–45 [Google Scholar]
  10. Bally J, Paget E, Droux M, Job C, Job D, Dubald M. 10.  2008. Both the stroma and thylakoid lumen of tobacco chloroplasts are competent for the formation of disulphide bonds in recombinant proteins. Plant Biotechnol. J. 6:46–61 [Google Scholar]
  11. Bateman JM, Purton S. 11.  2000. Tools for chloroplast transformation in Chlamydomonas: expression vectors and a new dominant selectable marker. Mol. Gen. Genet. 263:404–10 [Google Scholar]
  12. Bellucci M, de Marchis F, Mannucci R, Bock R, Arcioni S. 12.  2005. Cytoplasm and chloroplasts are not suitable subcellular locations for β-zein accumulation in transgenic plants. J. Exp. Bot. 56:1205–12 [Google Scholar]
  13. Birch-Machin I, Newell CA, Hibberd JM, Gray JC. 13.  2004. Accumulation of rotavirus VP6 protein in chloroplasts of transplastomic tobacco is limited by protein stability. Plant Biotechnol. J. 2:261–70 [Google Scholar]
  14. Blowers AD, Ellmore GA, Klein U, Bogorad L. 14.  1990. Transcriptional analysis of endogenous and foreign genes in chloroplast transformants of Chlamydomonas. Plant Cell 2:1059–70 [Google Scholar]
  15. Bock R. 15.  2001. Transgenic plastids in basic research and plant biotechnology. J. Mol. Biol. 312:425–38 [Google Scholar]
  16. Bock R. 16.  2007. Structure, function, and inheritance of plastid genomes. Top. Curr. Genet. 19:29–63 [Google Scholar]
  17. Bock R. 17.  2014. Engineering chloroplasts for high-level foreign protein expression. Methods Mol. Biol. 1132:93–106 [Google Scholar]
  18. Bock R. 18.  2014. Genetic engineering of the chloroplast: novel tools and new applications. Curr. Opin. Biotechnol. 26:7–13 [Google Scholar]
  19. Bock R, Hermann M, Fuchs M. 19.  1997. Identification of critical nucleotide positions for plastid RNA editing site recognition. RNA 3:1194–200 [Google Scholar]
  20. Bock R, Hermann M, Kössel H. 20.  1996. In vivo dissection of cis-acting determinants for plastid RNA editing. EMBO J. 15:5052–59 [Google Scholar]
  21. Bock R, Koop H-U. 21.  1997. Extraplastidic site-specific factors mediate RNA editing in chloroplasts. EMBO J. 16:3282–88 [Google Scholar]
  22. Bock R, Kössel H, Maliga P. 22.  1994. Introduction of a heterologous editing site into the tobacco plastid genome: the lack of RNA editing leads to a mutant phenotype. EMBO J. 13:4623–28 [Google Scholar]
  23. Bock R, Timmis JN. 23.  2008. Reconstructing evolution: gene transfer from plastids to the nucleus. BioEssays 30:556–66 [Google Scholar]
  24. Bock R, Warzecha H. 24.  2010. Solar-powered factories for new vaccines and antibiotics. Trends Biotechnol. 28:246–52 [Google Scholar]
  25. Bohmert-Tatarev K, McAvoy S, Daughtry S, Peoples OP, Snell KD. 25.  2011. High levels of bioplastic are produced in fertile transplastomic tobacco plants engineered with a synthetic operon for the production of polyhydroxybutyrate. Plant Physiol. 155:1690–708 [Google Scholar]
  26. Boudreau E, Takahashi Y, Lemieux C, Turmel M, Rochaix J-D. 26.  1997. The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. EMBO J. 16:6095–104 [Google Scholar]
  27. Boynton JE, Gillham NW, Harris EH, Hosler JP, Johnson AM. 27.  et al. 1988. Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science 240:1534–38 [Google Scholar]
  28. Buhot L, Horvàth E, Medgyesy P, Lerbs-Mache S. 28.  2006. Hybrid transcription system for controlled plastid transgene expression. Plant J. 46:700–7 [Google Scholar]
  29. Caroca R, Howell KA, Hasse C, Ruf S, Bock R. 29.  2013. Design of chimeric expression elements that confer high-level gene activity in chromoplasts. Plant J. 73:368–79 [Google Scholar]
  30. Carrer H, Hockenberry TN, Svab Z, Maliga P. 30.  1993. Kanamycin resistance as a selectable marker for plastid transformation in tobacco. Mol. Gen. Genet. 241:49–56 [Google Scholar]
  31. Carrer H, Maliga P. 31.  1995. Targeted insertion of foreign genes into the tobacco plastid genome without physical linkage to the selectable marker gene. Bio/Technology 13:791–94 [Google Scholar]
  32. Chakrabarti SK, Lutz KA, Lertwiriyawong B, Svab Z, Maliga P. 32.  2006. Expression of the cry9Aa2 B.t. gene in tobacco chloroplasts confers resistance to potato tuber moth. Transgenic Res. 15:481–88 [Google Scholar]
  33. Chaudhuri S, Carrer H, Maliga P. 33.  1995. Site-specific factor involved in the editing of the psbL mRNA in tobacco plastids. EMBO J. 14:2951–57 [Google Scholar]
  34. Chaudhuri S, Maliga P. 34.  1996. Sequences directing C to U editing of the plastid psbL mRNA are located within a 22 nucleotide segment spanning the editing site. EMBO J. 15:5958–64 [Google Scholar]
  35. Chebolu S, Daniell H. 35.  2007. Stable expression of Gal/GaINAc lectin of Entamoeba histolytica in transgenic chloroplasts and immunogenicity in mice towards vaccine development for amoebiasis. Plant Biotechnol. J. 5:230–39 [Google Scholar]
  36. Chen X, Kindle KL, Stern DB. 36.  1995. The initiation codon determines the efficiency but not the site of translation initiation in Chlamydomonas chloroplasts. Plant Cell 7:1295–305 [Google Scholar]
  37. Chiyoda S, Linley PJ, Yamato KT, Fukuzawa H, Yokota A, Kohchi T. 37.  2007. Simple and efficient plastid transformation system for the liverwort Marchantia polymorpha L. suspension-culture cells. Transgenic Res. 16:41–49 [Google Scholar]
  38. Corneille S, Lutz K, Svab Z, Maliga P. 38.  2001. Efficient elimination of selectable marker genes from the plastid genome by the CRE-lox-site-specific recombination system. Plant J. 27:171–78 [Google Scholar]
  39. Craig W, Lenzi P, Scotti N, De Palma M, Saggese P. 39.  et al. 2008. Transplastomic tobacco plants expressing a fatty acid desaturase gene exhibit altered fatty acid profiles and improved cold tolerance. Transgenic Res. 17:769–82 [Google Scholar]
  40. Daniell H, Lee S-B, Panchal T, Wiebe PO. 40.  2001. Expression of the native cholera toxin B subunit gene and assembly as functional oligomers in transgenic tobacco chloroplasts. J. Mol. Biol. 311:1001–9 [Google Scholar]
  41. Dauvillee D, Hilbig L, Preiss S, Johanningmeier U. 41.  2004. Minimal extent of sequence homology required for homologous recombination at the psbA locus in Chlamydomonas reinhardtii chloroplasts using PCR-generated DNA fragments. Photosynth. Res. 79:219–24 [Google Scholar]
  42. Davoodi-Semiromi A, Schreiber M, Nalapalli S, Verma D, Singh ND. 42.  et al. 2010. Chloroplast-derived vaccine antigens confer dual immunity against cholera and malaria by oral or injectable delivery. Plant Biotechnol. J. 8:223–42 [Google Scholar]
  43. Day A, Goldschmidt-Clermont M. 43.  2011. The chloroplast transformation toolbox: selectable markers and marker removal. Plant Biotechnol. J. 9:540–53 [Google Scholar]
  44. De Cosa B, Moar W, Lee S-B, Miller M, Daniell H. 44.  2001. Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat. Biotechnol. 19:71–74 [Google Scholar]
  45. De Marchis F, Pompa A, Bellucci M. 45.  2012. Plastid proteostasis and heterologous protein accumulation in transplastomic plants. Plant Physiol. 160:571–81 [Google Scholar]
  46. Doetsch NA, Favreau MR, Kuscuoglu N, Thompson MD, Hallick RB. 46.  2001. Chloroplast transformation in Euglena gracilis: splicing of a group II twintron transcribed from a transgenic psbK operon. Curr. Genet. 39:49–60 [Google Scholar]
  47. Drechsel O, Bock R. 47.  2010. Selection of Shine-Dalgarno sequences in plastids. Nucleic Acids Res. 39:1427–38 [Google Scholar]
  48. Drescher A, Ruf S, Calsa T Jr, Carrer H, Bock R. 48.  2000. The two largest chloroplast genome-encoded open reading frames of higher plants are essential genes. Plant J. 22:97–104 [Google Scholar]
  49. Drouin G, Daoud H, Xia J. 49.  2008. Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol. Phylogenet. Evol. 49:827–31 [Google Scholar]
  50. Dufourmantel N, Dubald M, Matringe M, Canard H, Garcon F. 50.  et al. 2007. Generation and characterization of soybean and marker-free tobacco plastid transformants over-expressing a bacterial 4-hydroxyphenylpyruvate dioxygenase which provides strong herbicide tolerance. Plant Biotechnol. J. 5:118–33 [Google Scholar]
  51. Dufourmantel N, Pelissier B, Garcon F, Peltier G, Ferullo J-M, Tissot G. 51.  2004. Generation of fertile transplastomic soybean. Plant Mol. Biol. 55:479–89 [Google Scholar]
  52. Dufourmantel N, Tissot G, Goutorbe F, Garcon F, Muhr C. 52.  et al. 2005. Generation and analysis of soybean plastid transformants expressing Bacillus thuringiensis Cry1Ab protoxin. Plant Mol. Biol. 58:659–68 [Google Scholar]
  53. Eberhard S, Drapier D, Wollman F-A. 53.  2002. Searching limiting steps in the expression of chloroplast-encoded proteins: relations between gene copy number, transcription, transcript abundance and translation rate in the chloroplast of Chlamydomonas reinhardtii. Plant J. 31:149–60 [Google Scholar]
  54. Economou C, Wannathong T, Szaub J, Purton S. 54.  2014. A simple, low-cost method for chloroplast transformation of the green alga Chlamydomonas reinhardtii. Methods Mol. Biol. 1132:401–11 [Google Scholar]
  55. Ehrnthaler M, Scharff LB, Fleischmann TT, Hasse C, Ruf S, Bock R. 55.  2014. Synthetic lethality in the tobacco plastid ribosome and its rescue at elevated growth temperatures. Plant Cell 26:765–76 [Google Scholar]
  56. Eibl C, Zou Z, Beck A, Kim M, Mullet J, Koop H-U. 56.  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. 19:333–45 [Google Scholar]
  57. Elghabi Z, Karcher D, Zhou F, Ruf S, Bock R. 57.  2011. Optimization of the expression of the HIV fusion inhibitor cyanovirin-N from the tobacco plastid genome. Plant Biotechnol. J. 9:599–608 [Google Scholar]
  58. Elghabi Z, Ruf S, Bock R. 58.  2011. Biolistic co-transformation of the nuclear and plastid genomes. Plant J. 67:941–48 [Google Scholar]
  59. Esposito D, Hicks AJ, Stern DB. 59.  2001. A role for initiation codon context in chloroplast translation. Plant Cell 13:2373–84 [Google Scholar]
  60. Fargo DC, Boynton JE, Gillham NW. 60.  1999. Mutations altering the predicted secondary structure of a chloroplast 5′ untranslated region affect its physical and biochemical properties as well as its ability to promote translation of reporter mRNAs both in the Chlamydomonas reinhardtii chloroplast and in Escherichia coli. Mol. Cell. Biol. 19:6980–90 [Google Scholar]
  61. Fernández-San Millán A, Ortigosa SM, Hervás-Stubbs S, Corral-Martínez P, Segui-Simarro JM. 61.  et al. 2008. Human papillomavirus L1 protein expressed in tobacco chloroplasts self-assembles into virus-like particles that are highly immunogenic. Plant Biotechnol. J. 6:427–41 [Google Scholar]
  62. Fischer N, Stampacchia O, Redding K, Rochaix J-D. 62.  1996. Selectable marker recycling in the chloroplast. Mol. Gen. Genet. 251:373–80 [Google Scholar]
  63. Fleischmann TT, Scharff LB, Alkatib S, Hasdorf S, Schöttler MA, Bock R. 63.  2011. Nonessential plastid-encoded ribosomal proteins in tobacco: a developmental role for plastid translation and implications for reductive genome evolution. Plant Cell 23:3137–55 [Google Scholar]
  64. Fuentes I, Karcher D, Bock R. 64.  2012. Experimental reconstruction of the functional transfer of intron-containing plastid genes to the nucleus. Curr. Biol. 22:763–71 [Google Scholar]
  65. Fuentes I, Stegemann S, Golczyk H, Karcher D, Bock R. 65.  2014. Horizontal genome transfer as an asexual path to the formation of new species. Nature 511:232–35 [Google Scholar]
  66. Gisby MF, Mudd EA, Day A. 66.  2012. Growth of transplastomics cells expressing d-amino acid oxidase in chloroplasts is tolerant to d-alanine and inhibited by d-valine. Plant Physiol. 160:2219–26 [Google Scholar]
  67. Glenz K, Bouchon B, Stehle T, Wallich R, Simon MM, Warzecha H. 67.  2006. Production of a recombinant bacterial lipoprotein in higher plant chloroplasts. Nat. Biotechnol. 24:76–77 [Google Scholar]
  68. Golczyk H, Greiner S, Wanner G, Weihe A, Bock R. 68.  et al. 2014. Chloroplast DNA in mature and senescing leaves: a reappraisal. Plant Cell 26:847–54 [Google Scholar]
  69. Golds T, Maliga P, Koop H-U. 69.  1993. Stable plastid transformation in PEG-treated protoplasts of Nicotiana tabacum. Bio/Technology 11:95–97 [Google Scholar]
  70. Goldschmidt-Clermont M. 70.  1991. Transgenic expression of aminoglycoside adenyl transferase in the chloroplast: a selectable marker for site-directed transformation of Chlamydomonas. Nucleic Acids Res. 19:4083–89 [Google Scholar]
  71. Gonzalez-Rabade N, McGowan EG, Zhou F, McCabe MS, Bock R. 71.  et al. 2011. Immunogenicity of chloroplast-derived HIV-1 p24 and a p24-Nef fusion protein following subcutaneous and oral administration in mice. Plant Biotechnol. J. 9:629–38 [Google Scholar]
  72. Greiner S, Bock R. 72.  2013. Tuning a ménage à trois: co-evolution and co-adaptation of nuclear and organellar genomes in plants. BioEssays 35:354–65 [Google Scholar]
  73. Hager M, Biehler K, Illerhaus J, Ruf S, Bock R. 73.  1999. Targeted inactivation of the smallest plastid genome-encoded open reading frame reveals a novel and essential subunit of the cytochrome b6f complex. EMBO J. 18:5834–42 [Google Scholar]
  74. Hajdukiewicz PTJ, Allison LA, Maliga P. 74.  1997. The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J. 16:4041–48 [Google Scholar]
  75. Hasunuma T, Miyazawa S-I, Yoshimura S, Shinzaki Y, Tomizawa K-I. 75.  et al. 2008. Biosynthesis of astaxanthin in tobacco leaves by transplastomic engineering. Plant J. 55:857–68 [Google Scholar]
  76. Hennig A, Bonfig K, Roitsch T, Warzecha H. 76.  2007. Expression of the recombinant bacterial outer surface protein A in tobacco chloroplasts leads to thylakoid localization and loss of photosynthesis. FEBS J. 274:5749–58 [Google Scholar]
  77. Hermann M, Bock R. 77.  1999. Transfer of plastid RNA-editing activity to novel sites suggests a critical role for spacing in editing-site recognition. PNAS 96:4856–61 [Google Scholar]
  78. Herz S, Füßl M, Steiger S, Koop H-U. 78.  2005. Development of novel types of plastid transformation vectors and evaluation of factors controlling expression. Transgenic Res. 14:969–82 [Google Scholar]
  79. Higgs DC, Shapiro RS, Kindle KL, Stern DB. 79.  1999. Small cis-acting sequences that specify secondary structures in a chloroplast mRNA are essential for RNA stability and translation. Mol. Cell. Biol. 19:8479–91 [Google Scholar]
  80. Hirose T, Sugiura M. 80.  1997. Both RNA editing and RNA cleavage are required for translation of tobacco chloroplast ndhD mRNA: a possible regulatory mechanism for the expression of a chloroplast operon consisting of functionally unrelated genes. EMBO J. 16:6804–11 [Google Scholar]
  81. Huang CY, Ayliffe MA, Timmis JN. 81.  2003. Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422:72–76 [Google Scholar]
  82. Huang CY, Ayliffe MA, Timmis JN. 82.  2004. Simple and complex nuclear loci created by newly transferred chloroplast DNA in tobacco. PNAS 101:9710–15 [Google Scholar]
  83. Huang F-C, Klaus SMJ, Herz S, Zou Z, Koop H-U, Golds TJ. 83.  2002. Efficient plastid transformation in tobacco using the aphA-6 gene and kanamycin selection. Mol. Genet. Genomics 268:19–27 [Google Scholar]
  84. Iamtham S, Day A. 84.  2000. Removal of antibiotic resistance genes from transgenic tobacco plastids. Nat. Biotechnol. 18:1172–76 [Google Scholar]
  85. Kahlau S, Aspinall S, Gray JC, Bock R. 85.  2006. Sequence of the tomato chloroplast DNA and evolutionary comparison of solanaceous plastid genomes. J. Mol. Evol. 63:194–207 [Google Scholar]
  86. Kahlau S, Bock R. 86.  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 20:856–74 [Google Scholar]
  87. Kanamoto H, Yamashita A, Asao H, Okumura S, Takase H. 87.  et al. 2006. Efficient and stable transformation of Lactuca sativa L. cv. Cisco (lettuce) plastids. Transgenic Res. 15:205–17 [Google Scholar]
  88. Kavanagh TA, Thanh ND, Lao NT, McGrath N, Peter SO. 88.  et al. 1999. Homeologous plastid DNA transformation in tobacco is mediated by multiple recombination events. Genetics 152:1111–22 [Google Scholar]
  89. Khakhlova O, Bock R. 89.  2006. Elimination of deleterious mutations in plastid genomes by gene conversion. Plant J. 46:85–94 [Google Scholar]
  90. Kim JY, Kavas M, Fouad WM, Nong G, Preston JF, Altpeter F. 90.  2011. Production of hyperthermostable GH10 xylanase Xyl10B from Thermotoga maritima in transplastomic plants enables complete hydrolysis of methylglucuronoxylan to fermentable sugars for biofuel production. Plant Mol. Biol. 76:357–69 [Google Scholar]
  91. Kindle KL, Richards KL, Stern DB. 91.  1991. Engineering the chloroplast genome: Techniques and capabilities for chloroplast transformation in Chlamydomonas reinhardtii. PNAS 88:1721–25 [Google Scholar]
  92. Klaus SMJ, Huang F-C, Golds TJ, Koop H-U. 92.  2004. Generation of marker-free plastid transformants using a transiently cointegrated selection gene. Nat. Biotechnol. 22:225–29 [Google Scholar]
  93. Klein U, Salvador ML, Bogorad L. 93.  1994. Activity of the Chlamydomonas chloroplast rbcL gene promoter is enhanced by a remote sequence element. PNAS 91:10819–23 [Google Scholar]
  94. Kode V, Mudd EA, Iamtham S, Day A. 94.  2005. The tobacco plastid accD gene is essential and is required for leaf development. Plant J. 44:237–44 [Google Scholar]
  95. Krech K, Fu H-Y, Thiele W, Ruf S, Schöttler MA, Bock R. 95.  2013. Reverse genetics in complex multigene operons by co-transformation of the plastid genome and its application to the open reading frame previously designated psbN. Plant J. 75:1062–74 [Google Scholar]
  96. Krech K, Ruf S, Masduki FF, Thiele W, Bednarczyk D. 96.  et al. 2012. The plastid genome-encoded Ycf4 protein functions as a nonessential assembly factor for photosystem I in higher plants. Plant Physiol. 159:579–91 [Google Scholar]
  97. Kuchuk N, Sytnyk K, Vasylenko M, Shakhovsky A, Komarnytsky I. 97.  et al. 2006. Genetic transformation of plastids of different Solanaceae species using tobacco cells as organelle hosts. Theor. Appl. Genet. 113:519–27 [Google Scholar]
  98. Kuroda H, Maliga P. 98.  2001. Complementarity of the 16S rRNA penultimate stem with sequences downstream of the AUG destabilizes the plastid mRNAs. Nucleic Acids Res. 29:970–75 [Google Scholar]
  99. Kuroda H, Maliga P. 99.  2003. The plastid clpP1 protease gene is essential for plant development. Nature 425:86–89 [Google Scholar]
  100. Langbecker CL, Ye G-N, Broyles DL, Duggan LL, Xu CW. 100.  et al. 2004. High-frequency transformation of undeveloped plastids in tobacco suspension cells. Plant Physiol. 135:39–46 [Google Scholar]
  101. Lelivelt CLC, McCabe MS, Newell CA, de Snoo CB, van Dun KMP. 101.  et al. 2005. Stable plastid transformation in lettuce (Lactuca sativa L.). Plant Mol. Biol. 58:763–74 [Google Scholar]
  102. Lentz EM, Garaicoechea L, Alfano EF, Parreno V, Wigdorovitz A, Bravo-Almonacid FF. 102.  2012. Translational fusion and redirection to thylakoid lumen as strategies to improve the accumulation of a camelid antibody fragment in transplastomic tobacco. Planta 236:703–14 [Google Scholar]
  103. Lentz EM, Mozgovoj MV, Bellido D, Dus Santos MJ, Wigdorovitz A, Bravo-Almonacid FF. 103.  2011. VP8 antigen produced in tobacco transplastomic plants confers protection against bovine rotavirus infection in a suckling mouse model. J. Biotechnol. 156:100–7 [Google Scholar]
  104. Li W, Ruf S, Bock R. 104.  2011. Chloramphenicol acetyltransferase as selectable marker for plastid transformation. Plant Mol. Biol. 76:443–51 [Google Scholar]
  105. Liu C-W, Lin C-C, Chen JJW, Tseng M-J. 105.  2007. Stable chloroplast transformation in cabbage (Brassica oleracea L. var. capitata L.) by particle bombardment. Plant Cell Rep. 26:1733–44 [Google Scholar]
  106. Lohse M, Drechsel O, Bock R. 106.  2007. OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr. Genet. 52:267–74 [Google Scholar]
  107. Lohse M, Drechsel O, Kahlau S, Bock R. 107.  2013. OrganellarGenomeDRAW—a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res. 41:W575–81 [Google Scholar]
  108. Lössl A, Bohmert K, Harloff H, Eibl C, Mühlbauer S, Koop H-U. 108.  2005. Inducible trans-activation of plastid transgenes: expression of the R. eutropha phb operon in transplastomic tobacco. Plant Cell Physiol. 46:1462–71 [Google Scholar]
  109. Lu Y, Rijzaani H, Karcher D, Ruf S, Bock R. 109.  2013. Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons. PNAS 110:E623–32 [Google Scholar]
  110. Lutz KA, Azhagiri AK, Tungsuchat-Huang T, Maliga P. 110.  2007. A guide to choosing vectors for transformation of the plastid genome of higher plants. Plant Physiol. 145:1201–10 [Google Scholar]
  111. Lutz KA, Knapp JE, Maliga P. 111.  2001. Expression of bar in the plastid genome confers herbicide resistance. Plant Physiol. 125:1585–91 [Google Scholar]
  112. Lutz KA, Maliga P. 112.  2007. Construction of marker-free transplastomic plants. Curr. Opin. Biotechnol. 18:107–14 [Google Scholar]
  113. Madoka Y, Tomizawa K-I, Mizoi J, Nishida I, Nagano Y, Sasaki Y. 113.  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. 43:1518–25 [Google Scholar]
  114. Majeran W, Wollman F-A, Vallon O. 114.  2000. Evidence for a role of ClpP in the degradation of the chloroplast cytochrome b6f complex. Plant Cell 12:137–49 [Google Scholar]
  115. Maliga P. 115.  2004. Plastid transformation in higher plants. Annu. Rev. Plant Biol. 55:289–313 [Google Scholar]
  116. Maliga P, Bock R. 116.  2011. Plastid biotechnology: food, fuel, and medicine for the 21st century. Plant Physiol. 155:1501–10 [Google Scholar]
  117. Manuell AL, Beligni MV, Elder JH, Siefker DT, Tran M. 117.  et al. 2007. Robust expression of a bioactive mammalian protein in Chlamydomonas chloroplast. Plant Biotechnol. J. 5:402–12 [Google Scholar]
  118. Mayfield SP, Schultz J. 118.  2004. Development of a luciferase reporter gene, luxCt, for Chlamydomonas reinhardtii chloroplast. Plant J. 37:449–58 [Google Scholar]
  119. McBride KE, Schaaf DJ, Daley M, Stalker DM. 119.  1994. Controlled expression of plastid transgenes in plants based on a nuclear DNA-encoded and plastid-targeted T7 RNA polymerase. PNAS 91:7301–5 [Google Scholar]
  120. McBride KE, Svab Z, Schaaf DJ, Hogan PS, Stalker DM, Maliga P. 120.  1995. Amplification of a chimeric Bacillus gene in chloroplasts leads to an extraordinary level of an insecticidal protein in tobacco. Bio/Technology 13:362–65 [Google Scholar]
  121. Millen RS, Olmstead RG, Adams KL, Palmer JD, Lao NT. 121.  et al. 2001. Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell 13:645–58 [Google Scholar]
  122. Minko I, Holloway SP, Nikaido S, Carter M, Odom OW. 122.  et al. 1999. Renilla luciferase as a vital reporter for chloroplast gene expression in Chlamydomonas. Mol. Gen. Genet. 262:421–25 [Google Scholar]
  123. Molina A, Hervás-Stubbs S, Daniell H, Mingo-Castel AM, Veramendi J. 123.  2004. High-yield expression of a viral peptide animal vaccine in transgenic tobacco chloroplasts. Plant Biotechnol. J. 2:141–53 [Google Scholar]
  124. Monde R-A, Greene JC, Stern DB. 124.  2000. The sequence and secondary structure of the 3′-UTR affect 3′-end maturation, RNA accumulation, and translation in tobacco chloroplasts. Plant Mol. Biol. 44:529–42 [Google Scholar]
  125. Mühlbauer SK, Koop H-U. 125.  2005. External control of transgene expression in tobacco plastids using the bacterial lac repressor. Plant J. 43:941–46 [Google Scholar]
  126. Newell CA, Birch-Machin I, Hibberd JM, Gray JC. 126.  2003. Expression of green fluorescent protein from bacterial and plastid promoters in tobacco chloroplasts. Transgenic Res. 12:631–34 [Google Scholar]
  127. Newman SM, Boynton JE, Gillham NW, Randolph-Anderson BL, Johnson AM, Harris EH. 127.  1990. Transformation of chloroplast ribosomal RNA genes in Chlamydomonas: molecular and genetic characterization of integration event. Genetics 126:875–88 [Google Scholar]
  128. Newman SM, Harris EH, Johnson AM, Boynton JE, Gillham NW. 128.  1992. Nonrandom distribution of chloroplast recombination events in Chlamydomonas reinhardtii: evidence for a hotspot and an adjacent cold region. Genetics 132:413–29 [Google Scholar]
  129. Nickelsen J, Fleischmann M, Boudreau E, Rahire M, Rochaix J-D. 129.  1999. Identification of cis-acting RNA leader elements required for chloroplast psbD gene expression in Chlamydomonas. Plant Cell 11:957–70 [Google Scholar]
  130. Nugent GD, Coyne S, Nguyen TT, Kavanagh TA, Dix PJ. 130.  2006. Nuclear and plastid transformation of Brassica oleracea var. botrytis (cauliflower) using PEG-mediated uptake of DNA into protoplasts. Plant Sci. 170:135–42 [Google Scholar]
  131. Nugent GD, ten Have M, van der Gulik A, Dix PJ, Uijtewaal BA, Mordhorst AP. 131.  2005. Plastid transformants of tomato selected using mutations affecting ribosome structure. Plant Cell Rep. 24:341–49 [Google Scholar]
  132. Oey M, Lohse M, Kreikemeyer B, Bock R. 132.  2009. Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. Plant J. 57:436–45 [Google Scholar]
  133. Oey M, Lohse M, Scharff LB, Kreikemeyer B, Bock R. 133.  2009. Plastid production of protein antibiotics against pneumonia via a new strategy for high-level expression of antimicrobial proteins. PNAS 106:6579–84 [Google Scholar]
  134. O'Neill C, Horvath GV, Horvath E, Dix PJ, Medgyesy P. 134.  1993. Chloroplast transformation in plants: polyethylene glycol (PEG) treatment of protoplasts is an alternative to biolistic delivery systems. Plant J. 3:729–38 [Google Scholar]
  135. Ovcharenko O, Momot V, Cherep N, Sheludko Y, Komarnitsky I. 135.  et al. 2011. Transfer of transformed Lesquerella fendleri (Gray) Wats. chloroplasts into Orychophragmus violaceus (L.) O.E. Schulz by protoplast fusion. Plant Cell Tissue Organ Cult. 105:21–27 [Google Scholar]
  136. Ozawa S-I, Nield J, Terao A, Stauber EJ, Hippler M. 136.  et al. 2009. Biochemical and structural studies of the large Ycf4-photosystem I assembly complex of the green alga Chlamydomonas reinhardtii. Plant Cell 21:2424–42 [Google Scholar]
  137. Petersen K, Bock R. 137.  2011. High-level expression of a suite of thermostable cell wall-degrading enzymes from the chloroplast genome. Plant Mol. Biol. 76:311–21 [Google Scholar]
  138. Przibilla E, Heiss S, Johanningmeier U, Trebst A. 138.  1991. Site-specific mutagenesis of the D1 subunit of photosystem II in wild-type Chlamydomonas. Plant Cell 3:169–74 [Google Scholar]
  139. Qiu H, Price DC, Weber APM, Facchinelli F, Yoon HS, Bhattacharya D. 139.  2013. Assessing the bacterial contribution to the plastid proteome. Trends Plant Sci. 18:680–87 [Google Scholar]
  140. Ramundo S, Rahire M, Schaad O, Rochaix J-D. 140.  2013. Repression of essential chloroplast genes reveals new signaling pathways and regulatory feedback loops in Chlamydomonas. Plant Cell 25:167–86 [Google Scholar]
  141. Rasala BA, Muto M, Lee PA, Jager M, Cardoso RMF. 141.  et al. 2010. Production of therapeutic proteins in algae, analysis of expression of seven human proteins in the chloroplast of Chlamydomonas reinhardtii. Plant Biotechnol. J. 8:719–33 [Google Scholar]
  142. Reed ML, Wilson SK, Sutton CA, Hanson MR. 142.  2001. High-level expression of a synthetic red-shifted GFP coding region incorporated into transgenic chloroplasts. Plant J. 27:257–65 [Google Scholar]
  143. Rogalski M, Karcher D, Bock R. 143.  2008. Superwobbling facilitates translation with reduced tRNA sets. Nat. Struct. Mol. Biol. 15:192–98 [Google Scholar]
  144. Rogalski M, Ruf S, Bock R. 144.  2006. Tobacco plastid ribosomal protein S18 is essential for cell survival. Nucleic Acids Res. 34:4537–45 [Google Scholar]
  145. Rogalski M, Schöttler MA, Thiele W, Schulze WX, Bock R. 145.  2008. Rpl33, a nonessential plastid-encoded ribosomal protein in tobacco, is required under cold stress conditions. Plant Cell 20:2221–37 [Google Scholar]
  146. Ruf S, Hermann M, Berger IJ, Carrer H, Bock R. 146.  2001. Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nat. Biotechnol. 19:870–75 [Google Scholar]
  147. Ruf S, Karcher D, Bock R. 147.  2007. Determining the transgene containment level provided by chloroplast transformation. PNAS 104:6998–7002 [Google Scholar]
  148. Ruf S, Kössel H, Bock R. 148.  1997. Targeted inactivation of a tobacco intron-containing open reading frame reveals a novel chloroplast-encoded photosystem I-related gene. J. Cell Biol. 139:95–102 [Google Scholar]
  149. Scharff LB, Bock R. 149.  2014. Synthetic biology in plastids. Plant J. 78:783–98 [Google Scholar]
  150. Schmitz-Linneweber C, Kushnir S, Babiychuk E, Poltnigg P, Herrmann RG, Maier RM. 150.  2005. Pigment deficiency in nightshade/tobacco cybrids is caused by the failure to edit the plastid ATPase α-subunit mRNA. Plant Cell 17:1815–28 [Google Scholar]
  151. Serino G, Maliga P. 151.  1997. A negative selection scheme based on the expression of cytosine deaminase in plastids. Plant J. 12:697–701 [Google Scholar]
  152. Sheppard AE, Timmis JN. 152.  2009. Instability of plastid DNA in the nuclear genome. PLOS Genet. 5:e1000323 [Google Scholar]
  153. Shikanai T, Shimizu K, Ueda K, Nishimura Y, Kuroiwa T, Hashimoto T. 153.  2001. The chloroplast cplP gene, encoding a proteolytic subunit of ATP-dependent protease, is indispensable for chloroplast development in tobacco. Plant Cell Physiol. 42:264–73 [Google Scholar]
  154. Shimizu M, Goto M, Hanai M, Shimizu T, Izawa N. 154.  et al. 2008. Selectable tolerance to herbicides by mutated acetolactate synthase genes integrated into the chloroplast genome of tobacco. Plant Physiol. 147:1976–83 [Google Scholar]
  155. Sidorov VA, Kasten D, Pang S-Z, Hajdukiewicz PTJ, Staub JM, Nehra NS. 155.  1999. Stable chloroplast transformation in potato: use of green fluorescent protein as a plastid marker. Plant J. 19:209–16 [Google Scholar]
  156. Sigeno A, Hayashi S, Terachi T, Yamagishi H. 156.  2009. Introduction of transformed chloroplasts from tobacco into petunia by asymmetric cell fusion. Plant Cell Rep. 28:1633–40 [Google Scholar]
  157. Sikdar SR, Serino G, Chaudhuri S, Maliga P. 157.  1998. Plastid transformation in Arabidopsis thaliana. Plant Cell Rep. 18:20–24 [Google Scholar]
  158. Staub JM, Garcia B, Graves J, Hajdukiewicz PTJ, Hunter P. 158.  et al. 2000. High yield production of a human therapeutic protein in tobacco chloroplasts. Nat. Biotechnol. 18:333–38 [Google Scholar]
  159. Staub JM, Maliga P. 159.  1993. Accumulation of D1 polypeptide in tobacco plastids is regulated via the untranslated region of the psbA mRNA. EMBO J. 12:601–6 [Google Scholar]
  160. Staub JM, Maliga P. 160.  1994. Translation of the psbA mRNA is regulated by light via the 5′-untranslated region in tobacco plastids. Plant J. 6:547–53 [Google Scholar]
  161. Stegemann S, Bock R. 161.  2006. Experimental reconstruction of functional gene transfer from the tobacco plastid genome to the nucleus. Plant Cell 18:2869–78 [Google Scholar]
  162. Stegemann S, Bock R. 162.  2009. Exchange of genetic material between cells in plant tissue grafts. Science 324:649–51 [Google Scholar]
  163. Stegemann S, Hartmann S, Ruf S, Bock R. 163.  2003. High-frequency gene transfer from the chloroplast genome to the nucleus. PNAS 100:8828–33 [Google Scholar]
  164. Stegemann S, Keuthe M, Greiner S, Bock R. 164.  2012. Horizontal transfer of chloroplast genomes between plant species. PNAS 109:2434–38 [Google Scholar]
  165. Stern DB, Gruissem W. 165.  1987. Control of plastid gene expression: 3′ inverted repeats act as mRNA processing and stabilizing elements but do not terminate transcription. Cell 51:1145–57 [Google Scholar]
  166. Sugiura C, Sugita M. 166.  2004. Plastid transformation reveals that moss tRNAArg-CCG is not essential for plastid function. Plant J. 40:314–21 [Google Scholar]
  167. Surzycki R, Cournac L, Peltier G, Rochaix J-D. 167.  2007. Potential for hydrogen production with inducible chloroplast gene expression in Chlamydomonas. PNAS 104:17548–53 [Google Scholar]
  168. Sutton CA, Zoubenko OV, Hanson MR, Maliga P. 168.  1995. A plant mitochondrial sequence transcribed in transgenic tobacco chloroplasts is not edited. Mol. Cell. Biol. 15:1377–81 [Google Scholar]
  169. Svab Z, Hajdukiewicz P, Maliga P. 169.  1990. Stable transformation of plastids in higher plants. PNAS 87:8526–30 [Google Scholar]
  170. Svab Z, Maliga P. 170.  1993. High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. PNAS 90:913–17 [Google Scholar]
  171. Svab Z, Maliga P. 171.  2007. Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment. PNAS 104:7003–8 [Google Scholar]
  172. Tangphatsornruang S, Birch-Machin I, Newell CA, Gray JC. 172.  2011. The effect of different 3′ untranslated regions on the accumulation and stability of transcripts of a gfp transgene in chloroplasts of transplastomic tobacco. Plant Mol. Biol. 76:385–96 [Google Scholar]
  173. Thyssen G, Svab Z, Maliga P. 173.  2012. Cell-to-cell movement of plastids in plants. PNAS 109:2439–43 [Google Scholar]
  174. Tissot G, Canard H, Nadai M, Martone A, Botterman J, Dubald M. 174.  2008. Translocation of aprotinin, a therapeutic protease inhibitor, into the thylakoid lumen of genetically engineered tobacco chloroplasts. Plant Biotechnol. J. 6:309–20 [Google Scholar]
  175. Tregoning JS, Nixon P, Kuroda H, Svab Z, Clare S. 175.  et al. 2003. Expression of tetanus toxin fragment C in tobacco chloroplasts. Nucleic Acids Res. 31:1174–79 [Google Scholar]
  176. Ueda M, Kuniyoshi T, Yamamoto H, Sugimoto K, Ishizaki K. 176.  et al. 2012. Composition and physiological function of the chloroplast NADH dehydrogenase-like complex in Marchantia polymorpha. Plant J. 72:683–93 [Google Scholar]
  177. Valkov VT, Gargano D, Manna C, Formisano G, Dix PJ. 177.  et al. 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. 20:137–51 [Google Scholar]
  178. Valkov VT, Scotti N, Kahlau S, MacLean D, Grillo S. 178.  et al. 2009. Genome-wide analysis of plastid gene expression in potato leaf chloroplasts and tuber amyloplasts: transcriptional and posttranscriptional control. Plant Physiol. 150:2030–44 [Google Scholar]
  179. Verhounig A, Karcher D, Bock R. 179.  2010. Inducible gene expression from the plastid genome by a synthetic riboswitch. PNAS 107:6204–9 [Google Scholar]
  180. Verma D, Jin S, Kanagaraj A, Singh ND, Daniel J. 180.  et al. 2013. Expression of fungal cutinase and swollenin in tobacco chloroplasts reveals novel enzyme functions and/or substrates. PLOS ONE 8:e57187 [Google Scholar]
  181. Verma D, Kanagaraj A, Jin S, Singh ND, Kolattukudy PE, Daniell H. 181.  2010. Chloroplast-derived enzyme cocktails hydrolyse lignocellulosic biomass and release fermentable sugars. Plant Biotechnol. J. 8:332–50 [Google Scholar]
  182. Verma D, Moghimi B, LoDuca PA, Singh HD, Hoffman BE. 182.  et al. 2010. Oral delivery of bioencapsulated coagulation factor IX prevents inhibitor formation and fatal anaphylaxis in hemophilia B mice. PNAS 107:7101–6 [Google Scholar]
  183. Wakasugi T, Tsudzuki T, Sugiura M. 183.  2001. The genomics of land plant chloroplasts: gene content and alteration of genomic information by RNA editing. Photosynth. Res. 70:107–18 [Google Scholar]
  184. Wurbs D, Ruf S, Bock R. 184.  2007. Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome. Plant J. 49:276–88 [Google Scholar]
  185. Ye G-N, Colburn SM, Xu CW, Hajdukiewicz PTJ, Staub JM. 185.  2003. Persistence of unselected transgenic DNA during a plastid transformation and segregation approach to herbicide resistance. Plant Physiol. 133:402–10 [Google Scholar]
  186. Ye G-N, Hajdukiewicz PTJ, Broyles D, Rodriguez D, Xu CW. 186.  et al. 2001. Plastid-expressed 5-enolpyruvylshikimate-3-phosphate synthase genes provide high level glyphosate tolerance in tobacco. Plant J. 25:261–70 [Google Scholar]
  187. Yu L-X, Gray BN, Rutzke CJ, Walker LP, Wilson DB, Hanson MR. 187.  2007. Expression of thermostable microbial cellulases in the chloroplasts of nicotine-free tobacco. J. Biotechnol. 131:362–69 [Google Scholar]
  188. Zhang J, Ruf S, Hasse C, Childs L, Scharff LB, Bock R. 188.  2012. Identification of cis-elements conferring high levels of gene expression in non-green plastids. Plant J. 72:115–28 [Google Scholar]
  189. Zhou F, Badillo-Corona JA, Karcher D, Gonzalez-Rabade N, Piepenburg K. 189.  et al. 2008. High-level expression of human immunodeficiency virus antigens from the tobacco and tomato plastid genomes. Plant Biotechnol. J. 6:897–913 [Google Scholar]
  190. Zhou F, Karcher D, Bock R. 190.  2007. Identification of a plastid Intercistronic Expression Element (IEE) facilitating the expression of stable translatable monocistronic mRNAs from operons. Plant J. 52:961–72 [Google Scholar]
  191. Zou Z, Eibl C, Koop H-U. 191.  2003. The stem-loop region of the tobacco psbA 5′UTR is an important determinant of mRNA stability and translation efficiency. Mol. Gen. Genomics 269:340–49 [Google Scholar]
  192. Zoubenko OV, Allison LA, Svab Z, Maliga P. 192.  1994. Efficient targeting of foreign genes into the tobacco plastid genome. Nucleic Acids Res. 22:3819–24 [Google Scholar]
/content/journals/10.1146/annurev-arplant-050213-040212
Loading
/content/journals/10.1146/annurev-arplant-050213-040212
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error