Abstract
Plant transformation has its roots in the research on Agrobacterium that was being undertaken in the early 1980s. The last two decades have seen significant developments in plant transformation technology, such that a large number of transgenic crop plants have now been released for commercial production. Advances in the technology have been due to development of a range of Agrobacterium-mediated and direct DNA delivery techniques, along with appropriate tissue culture techniques for regenerating whole plants from plant cells or tissues in a large number of species. In addition, parallel developments in molecular biology have greatly extended the range of investigations to which plant transformation technology can be applied. Research in plant transformation is concentrating now not so much on the introduction of DNA into plant cells, but rather more on the problems associated with stable integration and reliable expression of the DNA once it has been integrated.
Similar content being viewed by others
References
Birch, R. G. (1997) Plant transformation: problems and strategies for practical application. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 297–326.
Gelvin, S. B. (1998) The introduction and expression of transgenes in plants. Current Opinion in Biotechnology 9, 227–232.
Hansen, G. and Wright, M. S. (1999) Recent advances in the transformation of plants. Trends in Plant Science 4, 226–231.
Komari, T., Hiei, Y., Ishida, Y., Kumashiro, T., and Kubo, T. (1998) Advances in cereal gene transfer. Current Opinion in Plant Biology 1, 161–165.
Prescott, A., Briddon, R., and Harwood, W. (1998) Plant transformation, in Molecular Biomethods Handbook, (Rapley, R. and Walker, J. M., eds.), Humana Press Inc, Totowa, NJ, pp. 251–269.
Galun, E. and Breiman, A. (1997) Transgenic Plants, Imperial College Press, London.
Lindsey, K. (1998) Transgenic Plant Research. Harwood Academic Publishers.
Gheysen, G., Angenon, G., and Van Montagu, M. (1998) Agrobacterium-mediated plant transformation: a scientifically intriguing story with significant applications, in Transgenic Plant Research (Lindsey, K., ed.), Harwood Academic Publishers, pp. 1–33.
Herrera-Estrella, L., Depicker, A., Van Montagu, M., and Schell, J. (1983) Expression of chimaeric genes transferred into plant cells using a Ti-plasmid-derived vector. Nature 303, 209–213.
Trick, H. N. and Finer, J. J. (1998) Sonication assisted Agrobacterium-mediated transformation of soybean [Glycine max (L.) Merrill] embryogenic suspension culture tissue. Plant Cell Rep. 17, 482–488.
Zuker, A., Ahroni, A., Tzfira, T., Ben-Meir, H., and Vainstein, A. (1999) Wounding by bombardment yields highly efficient Agrobacterium-mediated transformation of carnation (Dianthus caryophyllus L.) Mol. Breed. 5, 367–375.
Bidney, D. (1999) Plant transformation method using agrobacterium species adhered to microprojectiles. United States Patent 5,932,782.
Meyer, P. (1998) Stabilities and instabilities in transgene expression, in Transgenic Plant Research (Lindsey, K., ed.), Harwood Academic Publishers, pp. 263–275.
Chilton, M. -D., Tepfer, D. A., Petit, A., David, C., Casse-Delbart, F., and Tempé, J. (1982) Agrobacterium rhizogenes inserts T-DNA into the genomes of the host plant root cells. Nature 295, 432–434.
Tepfer, D. (1984) Transformation of several species of higher plants by Agrobacterium rhizogenes: sexual transmission of the transformed genotype and phenotype. Cell 37, 959–967.
Flores, H. E., Vivanco, J. M., and Loyola-Vargas, V. M. (1999) ‘Radicle’ biochemistry: the biology of root-specific metabolism. Trends in Plant Science 4, 220–226.
Shanks, J. V. and Morgan, J. (1999) Plant ‘hairy root’ culture. Current Opinion in Biotechnology 10, 151–155.
Liu, C. Z., Wang, Y. C., Zhao, B., Guo, C., Ouyang, F., Ye, H. C., and Li, G. F. (1999) Development of a nutrient mist bioreactor for growth of hairy roots. In Vitro Cell. Dev. Biol. — Plant 35, 271–274.
Barcelo, P. and Lazzeri, P. A. (1998) Direct gene transfer: chemical, electrical and physical methods, in Transgenic Plant Research (Lindsey, K., ed.), Harwood Academic Publishers, pp. 35–55.
Harwood, W. A., Chen, D. -F., and Creissen, G. P. (1996) Transformation of pollen and microspores — a review, in In Vitro Haploid Production in Higher Plants, vol. 2 (Jain, S. M., Sopory, S. K., and Veilleux, R. E., eds.), Kluwer Academic Publishers, Netherlands, pp. 53–71.
Krens, F. A., Molendijk, L., Wullems, G. J., and Schilperoort, R. A. (1982) In vitro transformation of plant protoplasts with Ti-plasmid DNA. Nature 296, 72–74.
Fromm, M., Taylor, L. P., and Walbot, V. (1985) Expression of genes transferred into monocot and dicot plant cells by electroporation. Proc. Natl. Acad. Sci. 82, 5824–5828.
Crossway, A., Oakes, J. V., Irvine, J. M., Ward, B., Knauf, V. C., and Shewmaker, C. K. (1986) Integration of foreign DNA following microinjection of tobacco mesophyll protoplasts. Mol. Gen. Genet. 202, 179–185.
Fischer, R. and Hain, R. (1995) Tobacco protoplast transformation and use for functional analysis of newly isolated genes and gene constructs. Methods Cell Biol. 50, 401–410.
Koop, H. U., Steinmüller, K., Wagner, H., Rössler, C., Eibl, C., and Sacher, L. (1996) Integration of foreign sequences into the tobacco plastome via polyethylene glycol-mediated protoplast transformation. Planta 199, 193–201.
Bates, G. W. (1999) Plant transformation via protoplast electroporation. Methods Mol. Biol. 111, 359–366.
Mathur, J. and Koncz, C. (1998) PEG-mediated protoplast transformation with naked DNA. Methods Mol. Biol. 82, 267–276.
Klein, T. M., Wolf, E. D., Wu, R., and Sanford, J. C. (1987) High-velocity microprojectiles for delivering nucleic acids into living cells. Nature 327, 70–73.
Boynton, J. E. and Gillham, N. W. (1996) Genetics and transformation of mitochondria in the green alga Chlamydomonas. Methods in Enzymology 264, 279–296.
Staub, J. M., Garcia, B., Graves, J., Hajdukiewicz, P. T. J., Hunter, P., Nehra, N., et al. (2000) High-yield production of a human therapeutic protein in tobacco chloroplasts. Nature Biotechnology 18, 333–338.
Lowe, K., Bowen, B., Hoerster, G., Ross, M., Bond, D., Pierce, D., and Gordon-Kamm, B. (1995) Germline transformation of maize following manipulation of chimeric shoot meristems. Bio/Technology 13, 677–682.
Pawlowski, W. P. and Somers, D. A. (1998) Transgenic DNA integrated into the oat genome is frequently interspersed by host DNA. Proc. Natl. Acad. Sci USA 95, 12,106–12,110.
Chen, L., Marmey, P., Taylor, N. J., Brizard, J.-P., Espinoza, C., D’Cruz, P., et al. (1998) Expression and inheritance of multiple transgenes in rice plants. Nature Biotechnology 16, 1060–1064.
Kikkert, J. R., Humiston, G. A., Roy, M. K., and Sanford, J. C. (1999) Biological projectiles (phage, yeast, bacteria) for genetic transformation of plants. In Vitro Cell. Dev. Biol. -Plant 35, 43–50.
Luthra, R., Varsha, R. K. D., Srivastava, A. K., and Kumar, S. (1997) Microprojectile mediated plant transformation: A bibliographic search. Euphytica 95, 269–294.
D’Halluin, K., Bonne, E., Bossut, M., De Beuckeleer, M., and Leemans, J. (1992) Transgenic maize plants by tissue electroporation. Plant Cell 4, 1495–1505.
Chowrira, G. M., Akella, V., and Lurquin, P. F. (1995) Electroporation-mediated gene transfer into intact nodal meristems in planta. Molecular Biotechnology 3, 17–23.
Wang, K., Drayton, P., Frame, B., Dunwell, J., and Thompson, J. (1995) Whisker-mediated plant transformation: an alternative technology. In Vitro Cell Dev. Biol. 31, 101–104.
Neuhaus, G., Spangenberg, G., Scheid, O. M., and Schweiger, H.-G. (1987) Transgenic rapeseed plants obtained by the microinjection of DNA into microspore-derived embryoids. Theor. Appl. Genet. 75, 30–36.
Jones-Villeneuve, E., Huang, B., Prudhomme, I., Bird, S., Kemble, R., Hattori, J., and Miki, B. (1995) Assessment of microinjection for introducing DNA into uninuclear microspores of rapeseed. Plant Cell Tissue Org. Cult. 40, 97–100.
Park, S. H., Rose, S. C., Zapata, C., Srivatanakul, M., and Smith, R. H. (1998) Cross-protection and selectable marker genes in plant transformation. In Vitro Cell. Dev. Biol. -Plant 34, 117–121.
Irdani, T., Bogani, P., Mengoni, A., Mastromei, G., and Buiatti, M. (1998) Construction of a new vector conferring methotrexate resistance in Nicotiana tabacum plants. Plant Mol. Biol. 37, 1079–1084.
Hallmann, A. and Rappel, A. (1999) Genetic engineering of the multicellular green alga Volvox: a modified and multiplied bacterial antibiotic resistance gene as a dominant selectable marker. Plant J. 17, 99–109.
Haldrup, A., Petersen, S. G., and Okkels, F. T. (1998) The xylose isomerase gene from Thermoanaerobacterium thermosulfurogenes allows effective selection of transgenic plant cells using D-xylose as the selection agent. Plant Mol. Biol. 37, 287–296.
Nap, J. P., Bijvoet, J., and Stiekema, W. J. (1992) Biosafety of kanamycin-resistant transgenic plants: an overview. Transgenic Crops 1, 239–249.
Fuchs, R. L., Ream, J. E., Hammond, B. G., Naylor, M. W., Leimgruber, R. M., and Berberich, S. A. (1993) Safety assessment of the neomycin phosphotransferase II (NPTII) protein. Bio/Technology 11, 1543–1547.
Gleave, A. P., Mitra, D. S., Mudge, S. R., and Morris, B. A. M. (1999) Selectable marker-free transgenic plants without sexual crossing: transient expression of cre recombinase and use of a conditional lethal dominant gene. Plant Mol. Biol. 40, 223–235.
Sheen, J., Hwang, S., Niwa, Y., Kobayashi, H., and Galbraith, D. W. (1995) Green-fluorescent protein as a new vital marker in plant cells. Plant J. 8, 777–784.
Sidorov V. A., Kasten, D., Pang, S.-Z., Hajdukiewicz, P. T. J., Staub, J. M., and Nehra, N. S. (1999) Stable chloroplast transformation in potato: use of green fluorescent protein as a plastid marker. Plant J. 19, 209–216.
Khan, M. S. and Maliga, P. (1999) Fluorescent antibiotic resistance marker for tracking plastid transformation in higher plants. Nature Biotechnology 17, 910–915.
McCormac, A. C., Elliott, M. C., and Chen, D. F. (1997) pBECKS. A flexible series of binary vectors for Agrobacterium-mediated plant transformation. Mol. Biotechnol. 8, 199–213.
Xiang, C., Han, P., Lutziger, I., Wang, K., and Oliver, D. J. (1999) A mini binary vector series for plant transformation. Plant Mol. Biol. 40, 711–717.
Hamilton, C. M., Frary, A., Lewis, C., and Tanksley, S. D. (1996) Stable transfer of intact high molecular weight DNA into plant chromosomes. Proc. Natl. Acad. Sci. USA 93, 9975–9979.
Mullen, J., Adam, G., Blowers, A., and Farle, E. (1998) Biolistic transfer of large DNA fragments to tobacco cells using YACs retrofitted for plant transformation. Mol. Breeding 4, 449–457.
Han, K. H., Ma, C. P., and Strauss, S. H. (1997) Matrix attachment regions (MARs) enhance transformation frequency and transgene expression in poplar. Transgenic Research 6, 415–420.
Srivastava, V., Anderson, O. D., and Ow, D. W. (1999) Single-copy transgenic wheat generated through the resolution of complex integration patterns. Proc. Natl. Acad. Sci. USA 96, 11,117–11,121.
Torisky, R. S., Kovacs, L., Avdiushko, S., Newman, J. D., Hunt, A. G., and Collins, G. B. (1997) Development of a binary vector system for plant transformation based on the supervirulent Agrobacterium tumefaciens strain Chry 5. Plant Cell Rep. 17, 102–108.
Gressel, J. (1999) Tandem constructs: preventing the rise of superweeds, Tibtech 17, 361–366.
Rochaix, J.-D. and van Dillewijn, J. (1982) Transformation of the green alga Chlamydomonas reinhardii with yeast DNA. Nature 296, 70–72.
Renn, D. (1997) Biotechnology and the red seaweed polysaccharide industry: status, needs and prospects. Tibtech 15, 9–14.
Day, J. G., Benson, E. E., and Fleck, R. A. (1999) In vitro culture and conservation of microalgae: applications for aquaculture, biotechnology and environmental research. In Vitro Cell. Dev. Biol.—Plant 35, 127–136.
El-Sheekh, M. M. (1999) Stable transformation of the intact cells of Chlorella kessleri with high velocity microprojectiles. Biol. Plant. 42, 209–216.
Shimogawara, K., Fujiwara, S., Grossman, A., and Usuda, H. (1998) High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics 148, 1821–1828.
Boynton, J. E. and Gillham, N. W. (1993) Chloroplast transformation in Chlamydomonas. Methods in Enzymology 217, 510–536.
Apt, K. E., Kroth-Pancic, P. G., and Grossman, A. R. (1996) Stable nuclear transformation of the diatom Phaedactylum tricornutum. Mol. Gen. Genet. 252, 572–579.
Cho, S. -H., Chung, Y. -S., Cho, S. -K., Rim, Y.-W., and Shin, J. -S. (1999) Particle bombardment mediated transformation and GFP expression in the moss Physcomitrella patens. Mol. Cells 9, 14–19.
Zeidler, M., Hartmann, E., and Hughes, J. (1999) Transgene expression in the moss Ceratodon purpureus. J. Plant Physiol. 154, 641–650.
De Block, M., Schell, J., and Van Montagu, M. (1985) Chloroplast transformation by Agrobacterium tumefaciens. Embo J. 4, 1367–1372.
McBride, K. E., Svab, Z., Schaaf, D. J., Hogan, P. S., Stalker, D. M., and 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.
Daniell, H., Datta, R., Varma, S., Gray, S., and Lee, S. -B. (1998) Containment of herbicide resistance through genetic engineering of the chloroplast genome. Nat. Biotechnol. 16, 345–348.
Jang, I. -C., Nahm, B. H., and Kim, J. -K. (1999). Subcellular targeting of green fluorescent protein to plastids in transgenic rice plants provides a high-level expression system. Mol. Breeding 5, 453–461.
McBride, K. E., Schaaf, D. J., Daley, M., and Stalker, D. M. (1994) Controlled expression of plastid transgenes in plants based on a nuclear DNA-encoded and plastid-targeted T7 RNA polymerase. Proc. Natl. Acad. Sci. 91, 7301–7305.
Grierson, D. (1998) Manipulation of fruit ripening by genetic modification, in Transgenic Plant Research (Lindsey, K., ed.), Harwood Academic Publishers, pp. 109–124.
Mitten, D. H., MacDonald, R., and Klonus, D. (1999) Regulation of foods derived from genetically engineered crops. Current Opinion in Biotechnology 10, 298–302.
Briggs, S. P. and Koziel, M. (1998) Engineering new plant strains for commercial markets, Current Opinion in Biotechnology 9, 233–235.
Brasileiro, A. C. M., Leplé, J.-C., Muzzin, J., Ounnoughi, D., Michel, M.-F., and Jouanin, L. (1991) An alternative approach for gene transfer in trees using wild-type Agrobacterium strains. Plant Mol. Biol. 17, 441–452.
Grayburn, W. S. and Vick, B. A. (1995) Transformation of sunflower (Helianthus annuus L.) following wounding with glass beads. Plant Cell Rep. 14, 285–289.
Bechtold, N. and Pelletier, G. (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol. Biol. 82, 259–266.
Clough, S. J. and Bent, A. F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743.
Chang, S. S., Park, S. K., Kim, B. C., Kang, B. J., Kim, D. U., and Nam, H. G. (1994) Stable genetic transformation of Arabidopsis thaliana by Agrobacterium inoculation in planta. Plant J. 5, 551–558.
Feldmann, K. A. and Marks, M. D. (1987) Agrobacterium-mediated transformation of germinating seeds of Arabidopsis thaliana: a non-tissue culture approach. Mol. Gen. Genet. 208, 1–9.
Zaghmout, O. M. -F. and Trolinder, N. L. (1993) Simple and efficient method for directly electroporating Agrobacterium plasmid DNA into wheat callus cells. Nucleic Acids Res. 21, 1048.
Kikkert, J. R. (1993) The Biolistic®PDS-1000/He device. Plant Cell, Tissue and Organ Culture 33, 221–226.
McCabe, D. and Christou, P. (1993) Direct DNA transfer using electric discharge particle acceleration (ACCELLTM technology). Plant Cell, Tissue and Organ Culture 33, 227–236.
Vain, P., Keen, N., Murillo, J., Rathus, C., Nemes, C., and Finer, J. J. (1993) Development of the Particle Inflow Gun. Plant Cell, Tissue and Organ Culture 33, 237–246.
Oard, J. (1993) Development of an airgun device for particle bombardment. Plant Cell, Tissue and Organ Culture 33, 247–250.
Sautter, C. (1993) Development of a microtargeting device for particle bombardment of plant meristems. Plant Cell, Tissue and Organ Culture 33, 251–257.
Takeuchi, Y., Dotson, M., and Keen, N. T. (1992) Plant transformation: a simple particle bombardment device based on flowing helium. Plant Mol. Biol. 18, 835–839.
Guo, Y., Liong, H., and Bouss, M. W. (1995) Laser mediated gene transfer in rice. Physiologia Plantarum 93, 19–24.
Hirsch, R. E. and Sussman, M. R. (1999) Improving nutrient capture from soil by the genetic manipulation of crop plants. Tibtech 17, 356–361.
Heyer, A. G., Lloyd, J. R., and Kossmann, J. (1999) Production of modified polymeric carbohydrates. Current Opinion in Biotechnology 10, 169–174.
Slater, S., Mitsky, T. A., Houmiel, K. L., Hao, M., Reiser, S. E., Taylor, N. B., et al. (1999) Metabolic engineering of Arabidopsis and Brassica for poly(3-hydroxybutyrate-co-3-hydroxyvalerate) copolymer production. Nature Biotechnology 17, 1011–1016.
Murphy, D. J. (1999) Production of novel oils in plants. Current Opinion in Biotechnology, 10, 175–180.
Ohlrogge, J. and Browse, J. (1998) Manipulation of seed oil production, in Transgenic Plant Research (Lindsey, K., ed.), Harwood Academic Publishers, pp. 151–174.
Lange, B. M. and Croteau, R. (1999) Genetic engineering of essential oil production in mint. Current Opinion in Plant Biology 2, 139–144.
Poirier, Y. (1999) Production of new polymeric compounds in plants. Current Opinion in Biotechnology 10, 181–185.
Kusnadi, A. R., Hood, E. E., Witcher, D. R., Howard, J. A., and Nikolov, Z. L. (1998) Production and purification of two recombinant proteins from transgenic corn. Biotechnol. Prog. 14, 149–155.
Herbers, K. and Sonnewald, U. (1999) Production of new/modified proteins in transgenic plants. Current Opinion in Biotechnology 10, 163–168.
Raskin, I., Smith, R. D., and Salt, D. E. (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Current Opinion in Biotechnology 8, 221–226.
Whitelam, G. C. and Cockburn, W. (1998) Production of recombinant antibodies in transgenic plants, in Transgenic Plant Research (Lindsey, K., ed.), Harwood Academic Publishers, pp. 219–227.
Rodgers, P. B., Hamilton, W. D. O., and Adair, J. R. (1999) The therapeutic potential of plant-derived vaccines and antibodies. Exp. Opin. Invest. Drugs 8, 211–227.
Mol, J., Cornish, E., Mason, J., and Koes, R. (1999) Novel coloured flowers. Current Opinion in Biotechnology 10, 198–201.
Hu, W.-J., Harding, S. A., Lung, J., Popko, J. L., Ralph, J., Stokke, D. D., et al. (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nat. Biotechnol. 17, 808–812.
O’Connell, A., Bolwell, P., and Schuch, W. (1998) Impact of forest tree biotechnology on the pulp and paper-making processes in the 21st century, in Transgenic Plant Research (Lindsey, K., ed.), Harwood Academic Publishers, pp. 175–186.
Holmberg, N. and Bülow, L. (1998) Improving stress tolerance in plants by gene transfer. Trends in Plant Science 3, 61–66.
Nuccio, M. L., Rhodes, D., McNeil, S. D., and Hanson, A. D. (1999) Metabolic engineering of plants for osmotic stress resistance. Current Opinion in Plant Biology 2, 128–134.
Frey, A., Audran, C., Marin, E., Sotta, B., and Marion-Poll, A. (1999) Engineering seed dormancy by the modification of zeaxanthin epoxidase gene expression. Plant Mol. Biol. 39, 1267–1274.
Anthony, R. G., Reichelt, S., and Hussey, P. J. (1999) Dinitroaniline herbicide-resistant transgenic tobacco plants generated by co-overexpression of a mutant α-tubulin and a β-tubulin. Nat. Biotechnology, 17, 712–716.
De Maagd, R. A., Bosch, D., and Stiekema, W. (1999) Bacillus thuringiensis toxin-mediated insect resistance in plants. Trends in Plant Science 4, 9–13.
Dempsey, D.’M. A., Silva, H., and Klessig, D. F. (1998) Engineering disease and pest resistance in plants. Trends in Microbiology 6, 54–61.
Mourgues, F., Brisset, M. -N., and Chevreau, E. (1998) Strategies to improve plant resistance to bacterial diseases through genetic engineering. Trends in Biotechnology 16, 203–210.
Zhang, L., Xu, J., and Birch, R. G. (1999) Engineered detoxification confers resistance against a pathogenic bacterium. Nature Biotechnology 17, 1021–1024.
Salmeron, J. M. and Vernooij, B. (1998) Transgenic approaches to microbial disease resistance in crop plants. Current Opinion in Plant Biology 1, 347–352.
Beachy, R. (1997) Mechanisms and applications of pathogen-derived resistance in transgenic plants. Current Opinion in Biotechnology 8, 215–220.
Jung, C., Cai, D., and Kleine, M. (1998) Engineering nematode resistance in crop species. Trends in Plant Science 3, 266–271.
Lilley, C. J., Devlin, P., Urwin, P. E., and Atkinson, H. J. (1999) Parasitic nematodes, proteinases and transgenic plants. Parasitology Today 15, 414–417.
Shewry, P. R. (1998) Manipulation of seed storage proteins, in Transgenic Plant Research (Lindsey, K., ed.), Harwood Academic Publishers, pp. 135–149.
Tabe, L. and Higgins, T. J. V. (1998) Engineering plant protein composition for improved nutrition. Trends in Plant Science 3, 282–286.
Hirschberg, J. (1999) Production of high-value compounds: carotenoids and vitamin E. Current Opinion in Biotechnology 10, 186–191.
Broun, P., Gettner, S., and Somerville, C. (1999) Genetic engineering of plant lipids. Annu. Rev. Nutr. 19, 197–216.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Newell, C.A. Plant transformation technology. Mol Biotechnol 16, 53–65 (2000). https://doi.org/10.1385/MB:16:1:53
Issue Date:
DOI: https://doi.org/10.1385/MB:16:1:53