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Volume 36 Issue 7
Jul.  2009
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Article Navigation >  Journal of Genetics and Genomics  > 2009  >  36(7): 387-398

Advances in chloroplast engineering

doi: 10.1016/S1673-8527(08)60128-9
  • a 

    Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China

  • b 

    Graduate University of Chinese Academy of Sciences, Beijing 100049, China

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  • Corresponding author: E-mail address: zmhu@genetics.ac.cn (Zan-Min Hu)
  • Received Date: 2009-01-12
  • Accepted Date: 2009-05-04
  • Rev Recd Date: 2009-04-30
    • Available Online: 2009-07-23
  • Publish Date: 2009-07-20
    Abstract
  • The chloroplast is a pivotal organelle in plant cells and eukaryotic algae to carry out photosynthesis, which provides the primary source of the world's food. The expression of foreign genes in chloroplasts offers several advantages over their expression in the nucleus: high-level expression, transgene stacking in operons and a lack of epigenetic interference allowing stable transgene expression. In addition, transgenic chloroplasts are generally not transmitted through pollen grains because of the cytoplasmic localization. In the past two decades, great progress in chloroplast engineering has been made. In this paper, we review and highlight recent studies of chloroplast engineering, including chloroplast transformation procedures, controlled expression of plastid transgenes in plants, the expression of foreign genes for improvement of plant traits, the production of biopharmaceuticals, metabolic pathway engineering in plants, plastid transformation to study RNA editing, and marker gene excision system.
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  • [1]
    Bendich, A.J. Why do chloroplasts and mitochondria contain so many copies of their genome? BioEssays, 6 (1987),pp. 279-282
    [2]
    Block, M.D., Schell, J., Montagu, M.V. EMBO J., 4 (1985),pp. 1367-1372
    [3]
    Bock, R. Sense from nonsense: How the genetic information of chloroplastsis altered by RNA editing Biochimie, 82 (2000),pp. 549-557
    [4]
    Bock, R. Plastid biotechnology: Prospects for herbicide and insect resistance, metabolic engineering and molecular farming Curr. Opin. Biotechnol., 18 (2007),pp. 100-106
    [5]
    Bock, R., Koop, H.-U. Extraplastidic site-specific factors mediate RNA editing in chloroplasts EMBO J., 16 (1997),pp. 3282-3288
    [6]
    Bock, R., Kössel, H., Maliga, P. Introduction of a heterologous editing site into the tobacco plastid genome: the lack of RNA editing leads to a mutant phenotype EMBO J., 13 (1994),pp. 4623-4628
    [7]
    Bock, R., Hermann, M., Kössel, H. In vivo dissection of cis-acting determinants for plastid RNA editing EMBO J, 15 (1996),pp. 5052-5059
    [8]
    Boynton, J.E., Gillham, N.W., Harris, E.H. et al. Chloroplast transformation in Chlamydomonas with high velocity microprojectiles Science, 240 (1988),pp. 1534-1538
    [9]
    Carrer, H., Maliga, P. Targeted insertion of foreign genes into the tobacco plastid genome without physical linkage to the selectable marker gene Bio/Technology, 13 (1995),pp. 791-794
    [10]
    Carrer, H., Hockenberry, T.N., Svab, Z. et al. Kanamycin resistance as a selectable marker for plastid transformation in tobacco Mol. Gen. Genet., 241 (1993),pp. 49-56
    [11]
    Chakrabarti, S., Lutz, K., Lertwiriyawong, B. et al. Transgenic Res., 15 (2006),pp. 481-488
    [12]
    Chaudhuri, S., Maliga, P. 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 (1996),pp. 5958-5964
    [13]
    Chebolu, S., Daniell, H. Plant Biotechnol. J., 5 (2007),pp. 230-239
    [14]
    Corneille, S., Lutz, K., Svab, Z. et al. Efficient elimination of selectable marker genes from the plastid genome by the CRE-lox site-specific recombination system Plant J., 27 (2001),pp. 171-178
    [15]
    Corneille, S., Lutz, K.A., Azhagiri, A.K. et al. Identification of functional lox sites in the plastid genome Plant J., 35 (2003),pp. 753-762
    [16]
    Cosa, B.D., Moar, W., Lee, S.-B. et al. Nat. Biotechnol., 19 (2001),pp. 71-74
    [17]
    Craig, W., Lenzi, P., Scotti, N. et al. Transplastomic tobacco plants expressing a fatty acid desaturase gene exhibit altered fatty acid profiles and improved cold tolerance Transgenic Res., 17 (2008),pp. 769-782
    [18]
    Daniell, H., Chebolu, S., Kumar, S. et al. Chloroplast-derived vaccine antigens and other therapeutic proteins Vaccine, 23 (2005),pp. 1779-1783
    [19]
    Daniell, H., Datta, R., Varma, S. et al. Containment of herbicide resistance through genetic engineering of the chloroplast genome Nat. Biotechnol., 16 (1998),pp. 345-348
    [20]
    Daniell, H., Kumar, S., Dufourmantel, N. Breakthrough in chloroplast genetic engineering of agronomically important crops Trends Biotechnol., 23 (2005),pp. 238-245
    [21]
    Daniell, H., Lee, S.B., Panchal, T. et al. Expression of the native cholera toxin B subunit gene and assembly as functional oligomers in transgenic tobacco chloroplasts J. Mol. Biol., 311 (2001),pp. 1001-1009
    [22]
    Daniell, H., Muthukumar, B., Lee, S.B. Marker free transgenic plants: engineering the chloroplast genome without the use of antibiotic selection Curr. Genet., 39 (2001),pp. 109-116
    [23]
    Daniell, H., Vivekananda, J., Nielsen, B.L. et al. Transient foreign gene expression in chloroplasts of cultured tobacco cells after biolistic delivery of chloroplast vectors Proc. Natl. Acad. Sci. USA, 87 (1990),pp. 88-92
    [24]
    DeGray, G., Rajasekaran, K., Smith, F. et al. Plant Physiol., 127 (2001),pp. 852-862
    [25]
    Dufourmantel, N., Pelissier, B., Garcon, F. et al. Generation of fertile transplastomic soybean Plant Mol. Biol., 55 (2004),pp. 479-489
    [26]
    Dufourmantel, N., Tissot, G., Goutorbe, F. et al. Plant Mol. Biol., 58 (2005),pp. 659-668
    [27]
    Eibl, C., Zou, Z., Beck, A. et al. Plant J., 19 (1999),pp. 333-345
    [28]
    Faye, L., Daniell, H. Novel pathways for glycoprotein import into chloroplasts Plant Biotechnol. J., 4 (2006),pp. 275-279
    [29]
    Fischer, N., Stampacchia, O., Redding, K. et al. Selectable marker recycling in the chloroplast Mol. Gen. Genet., 251 (1996),pp. 373-380
    [30]
    Golds, T., Maliga, P., Koop, H.U. Nat. Biotechnol., 11 (1993),pp. 95-97
    [31]
    Goldschmidt-Clermont, M. Transgenic expression of aminoglycoside adenine transferase in the chloroplast: A selectable marker for site-directed transformation of chlamydomonas Nucl. Acids Res., 19 (1991),pp. 4083-4089
    [32]
    Gruissem, W., Tonkyn, J.C. Control mechanisms of plastid gene expression CRC Crit. Rev. Plant Sci., 12 (1993),pp. 19-55
    [33]
    Hagemann R. (2004). The sexual inheritance of plant organelles. In Molecular Biology and Biotechnology of Plant Organelles, pp. 93–113.
    [34]
    Hajdukiewicz, P.T.J., Gilbertson, L., Staub, J.M. Multiple pathways for Cre/lox-mediated recombination in plastids Plant J., 27 (2001),pp. 161-170
    [35]
    Hayes, M.L., Reed, M.L., Hegeman, C.E. et al. Sequence elements critical for efficient RNA editing of a tobacco chloroplast transcript in vivo and in vitro Nucl. Acids Res., 34 (2006),pp. 3742-3754
    [36]
    Hoch, B., Maier, R.M., Appel, K. et al. Editing of a chloroplast mRNA by creation of an initiation codon Nature, 353 (1991),pp. 178-180
    [37]
    Hou, B.K., Zhou, Y.H., Wan, L.H. et al. Chloroplast transformation in oilseed rape Transgenic Res., 12 (2003),pp. 111-114
    [38]
    Iamtham, S., Day, A. Removal of antibiotic resistance genes from transgenic tobacco plastids Nat. Biotechnol., 18 (2000),pp. 1172-1176
    [39]
    Kanamoto, H., Yamashita, A., Asao, H. et al. Transgenic Res., 15 (2006),pp. 205-217
    [40]
    Karcher, D., Kahlau, S., Bock, R. Faithful editing of a tomato-specific mRNA editing site in transgenic tobacco chloroplasts RNA, 14 (2008),pp. 217-224
    [41]
    Keravala, A., Groth, A., Jarrahian, S. et al. A diversity of serine phage integrases mediate site-specific recombination in mammalian cells Mol. Genet. Genomics, 276 (2006),pp. 135-146
    [42]
    Kindle, K.L., Richards, K.L., Stern, D.B. Proc. Natl. Acad. Sci. USA, 88 (1991),pp. 1721-1725
    [43]
    Kittiwongwattana, C., Lutz, K., Clark, M. et al. Plastid marker gene excision by the phiC31 phage site-specific recombinase Plant Mol. Biol., 64 (2007),pp. 137-143
    [44]
    Klaus, S.M.J., Huang, F.C., Golds, T.J. et al. Generation of marker-free plastid transformants using a transiently cointegrated selection gene Nat. Biotechnol., 22 (2004),pp. 225-229
    [45]
    Koop, H.U., Kofer, W.
    [46]
    Koop, H.U., Steinmüller, K., Wagner, H. et al. Planta, 199 (1996),pp. 193-201
    [47]
    Kota, M., Daniell, H., Varma, S. et al. Proc. Natl. Acad. Sci. USA, 96 (1999),pp. 1840-1845
    [48]
    Kumar, S., Dhingra, A., Daniell, H. Stable transformation of the cotton plastid genome and maternal inheritance of transgenes Plant Mol. Biol., 56 (2004),pp. 203-216
    [49]
    Kumar, S., Dhingra, A., Daniell, H. Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves confers enhanced salt tolerance Plant Physiol., 136 (2004),pp. 2843-2854
    [50]
    Kuroda, H., Maliga, P. Complementarity of the 16S rRNA penultimate stem with sequences downstream of the AUG destabilizes the plastid mRNAs Nucl. Acids Res., 29 (2001),pp. 970-975
    [51]
    Kuroda, H., Maliga, P. Sequences downstream of the translation initiation codon are important determinants of translation efficiency in chloroplasts Plant Physiol., 125 (2001),pp. 430-436
    [52]
    Liu, C.W., Lin, C.C., Chen, J. et al. Plant Cell Rep., 26 (2007),pp. 1733-1744
    [53]
    Lössl, A., Eibl, C., Harloff, H.J. et al. Plant Cell Rep., 21 (2003),pp. 891-899
    [54]
    Lee, S.B., Kwon, H.B., Kwon, S.J. et al. Accumulation of trehalose within transgenic chloroplasts confers drought tolerance Mol. Breed., 11 (2003),pp. 1-13
    [55]
    Lee, S.M., Kang, K., Chung, H. et al. Mol. Cells, 21 (2006),pp. 401-410
    [56]
    Lelivelt, C., McCabe, M., Newell, C. et al. Plant Mol. Biol., 58 (2005),pp. 763-774
    [57]
    Lossl, A., Bohmert, K., Harloff, H. et al. Plant Cell Physiol., 46 (2005),pp. 1462-1471
    [58]
    Lutz, K.A., Maliga, P. Construction of marker-free transplastomic plants Curr. Opin. Biotechnol., 18 (2007),pp. 107-114
    [59]
    Lutz, K.A., Knapp, J.E., Maliga, P. Expression of bar in the plastid genome confers herbicide resistance Plant Physiol., 125 (2001),pp. 1585-1590
    [60]
    Lutz, K.A., Bosacchi, M.H., Maliga, P. Plastid marker-gene excision by transiently expressed CRE recombinase Plant J., 45 (2006),pp. 447-456
    [61]
    Lutz, K.A., Svab, Z., Maliga, P. Construction of marker-free transplastomic tobacco using the Cre-loxP site-specific recombination system Nat. Protocols, 1 (2006),pp. 900-910
    [62]
    Lutz, K.A., Azhagiri, A.K., Tungsuchat-Huang, T. et al. A guide to choosing vectors for transformation of the plastid genome of higher plants Plant Physiol., 145 (2007),pp. 1201-1210
    [63]
    Lutz, K.A., Corneille, S., Azhagiri, A.K. et al. A novel approach to plastid transformation utilizes the phiC31 phage integrase Plant J., 37 (2004),pp. 906-913
    [64]
    Magee, A., Coyne, S., Murphy, D. et al. T7 RNA polymerase-directed expression of an antibody fragment transgene in plastids causes a semi-lethal pale-green seedling phenotype Transgenic Res., 13 (2004),pp. 325-337
    [65]
    Maliga, P. Engineering the plastid genome of higher plants Curr. Opin. Plant Biol., 5 (2002),pp. 164-172
    [66]
    Maliga, P. Progress towards commercialization of plastid transformation technology Trends Biotechnol., 21 (2003),pp. 20-28
    [67]
    Maliga, P. Plastid transformation in higher plants Annu. Rev. Plant Biol., 55 (2004),pp. 289-313
    [68]
    McBride, K.E., Schaaf, D.J., Daley, M. et al. Controlled expression of plastid transgenes in plants based on a nuclear DNA-encoded and plastid-targeted T7 RNA polymerase Proc. Natl. Acad. Sci. USA, 91 (1994),pp. 7301-7305
    [69]
    McCabe, M.S., Klaas, M., Rabade, N. et al. 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 (2008),pp. 914-929
    [70]
    Millán, A.F.S., Mingo-Castel, A., Miller, M. et al. A chloroplast transgenic approach to hyper-express and purify Human Serum Albumin, a protein highly susceptible to proteolytic degradation Plant Biotechnol. J., 1 (2003),pp. 71-79
    [71]
    Molina, A., Hervás-Stubbs, S., Daniell, H. et al. High-yield expression of a viral peptide animal vaccine in transgenic tobacco chloroplasts Plant Biotechnol. J., 2 (2004),pp. 141-153
    [72]
    Muhlbauer, S.K., Koop, H.U. External control of transgene expression in tobacco plastids using the bacterial lac repressor Plant J., 43 (2005),pp. 941-946
    [73]
    Nakashita, H., Arai, Y., Shikanai, T. et al. Introduction of bacterial metabolism into higher plants by polycistronic transgene expression Biosci. Biotechnol. Biochem., 65 (2001),pp. 1688-1691
    [74]
    Nugent, G.D., Coyne, S., Nguyen, T.T. et al. Plant Sci., 170 (2006),pp. 135-142
    [75]
    O'Neillt, C., Horvath, G.V., Horvath, E. et al. Chloroplast transformation in plants: Polyethylene glycol (PEG) treatment of protoplasts is an alternative to biolistic delivery systems Plant J., 3 (1993),pp. 729-738
    [76]
    Okumura, S., Sawada, M., Park, Y. et al. Transgenic Res., 15 (2006),pp. 637-646
    [77]
    Rhodes, D., Hanson, A.D. Quaternary ammonium and tertiary sulfonium compounds in higher plants Annu. Rev. Plant Physiol. Plant Mol. Biol., 44 (1993),pp. 357-384
    [78]
    Roffey, R.A., Golbeck, J.H., Hille, C.R. et al. Photosynthetic electron transport in genetically altered photosystem II reaction centers of chloroplasts Proc. Natl. Acad. Sci. USA, 88 (1991),pp. 9122-9126
    [79]
    Ruf, S., Hermann, M., Berger, I.J. et al. Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit Nat. Biotechnol., 19 (2001),pp. 870-875
    [80]
    Ruiz, O.N., Daniell, H. Plant Physiol., 138 (2005),pp. 1232-1246
    [81]
    Rumeau, D., Becuwe-Linka, N., Beyly, A. et al. New subunits NDH-M, -N, and -O, encoded by nuclear genes, are essential for plastid Ndh complex functioning in higher plants Plant Cell, 17 (2005),pp. 219-232
    [82]
    Sidorov, V.A., Kasten, D., Pang, S.Z. et al. Stable chloroplast transformation in potato: Use of green fluorescent protein as a plastid marker Plant J., 19 (1999),pp. 209-216
    [83]
    Sikdar, S.R., Serino, G., Chaudhuri, S. et al. Plant Cell Rep., 18 (1998),pp. 20-24
    [84]
    Skarjinskaia, M., Svab, Z., Maliga, P. Transgenic Res., 12 (2003),pp. 115-122
    [85]
    Sporlein, B., Streubel, M., Dahlfeld, G. et al. PEG-mediated plastid transformation: A new system for transient gene expression assays in chloroplasts Theor. Appl. Genet., 82 (1991),pp. 717-722
    [86]
    Staub, J.M., Maliga, P. Expression of a chimeric uidA gene. indicates that polycistronic mRNAs are efficiently translated in tobacco plastids Plant J., 7 (1995),pp. 845-848
    [87]
    Staub, J.M., Garcia, B., Graves, J. et al. High-yield production of a human therapeutic protein in tobacco chloroplasts Nat. Biotech., 18 (2000),pp. 333-338
    [88]
    Sutton, C.A., Zoubenko, O.V., Hanson, M.R. et al. A plant mitochondrial sequence transcribed in transgenic tobacco chloroplasts is not edited Mol. Cell. Biol., 15 (1995),pp. 1377-1381
    [89]
    Svab, Z., Maliga, P. Proc. Natl. Acad. Sci. USA, 90 (1993),pp. 913-917
    [90]
    Svab, Z., Hajdukiewicz, P., Maliga, P. Stable transformation of plastids in higher plants Proc. Natl. Acad. Sci. USA, 87 (1990),pp. 8526-8530
    [91]
    Thomson, J.G., Ow, D.W. Site-specific recombination systems for the genetic manipulation of eukaryotic genomes Genesis, 44 (2006),pp. 465-476
    [92]
    Tsudzuki, T., Wakasugi, T., Sugiura, M. Comparative analysis of RNA editing sites in higher plant chloroplasts J. Mol. Evol., 53 (2001),pp. 327-332
    [93]
    Verma, D., Daniell, H. Chloroplast vector systems for biotechnology applications Plant Physiol., 145 (2007),pp. 1129-1143
    [94]
    Watson, J., Koya, V., Leppla, S.H. et al. Vaccine, 22 (2004),pp. 4374-4384
    [95]
    Wurbs, D., Ruf, S., Bock, R. Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome Plant J., 49 (2007),pp. 276-288
    [96]
    Ye, G.-N., Colburn, S.M., Xu, C.W. et al. Persistence of unselected transgenic DNA during a plastid transformation and segregation approach to herbicide resistance Plant Physiol., 133 (2003),pp. 402-410
    [97]
    Zhang, J., Tan, W., Yang, X.H. et al. Plastid-expressed choline monooxygenase gene improves salt and drought tolerance through accumulation of glycine betaine in tobacco Plant Cell Rep., 27 (2008),pp. 1113-1124
    [98]
    Zou, Z., Eibl, C., Koop, H.U. The stem-loop region of the tobacco psbA 5′UTR is an important determinant of mRNA stability and translation efficiency Mol. Genet. Genomics, 269 (2003),pp. 340-349
    [99]
    Zoubenko, O.V., Allison, L.A., Svab, Z. et al. Efficient targeting of foreign genes into the tobacco plastid genome Nucl. Acids Res., 22 (1994),pp. 3819-3824
    [100]
    Zubko, M.K., Zubko, E.I., Zuilen, K.V. et al. Stable transformation of petunia plastids Transgenic Res., 13 (2004),pp. 523-530
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