Skip to main content
Log in

The cell biology of plant transformation: Current state, problems, prospects and the implications for the plant breeding

  • Review Paper
  • Published:
Euphytica Aims and scope Submit manuscript

Summary

The DNA delivery systems which are routinely used to introduce genes into crop plants are Agrobacterium tumefaciens, electroporation and particle bombardment. The differences and similarities between these different transformation techniques are outlined. The influence of the cell biological approach, and more specifically the impact of the state of the plant cell at the moment of transformation, on the genotype and phenotype of the regenerated transgenic plant is analysed. In this respect phenomena such as position effects, gene silencing, co-suppression, epistasis, co-transformation and somaclonal variation are discussed. The relevance of these factors for plant breeders is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Binns A.N. & M.F. Thomashow, 1988. Cell biology of Agrobacterium infection and transformation of plants. Ann. Rev. Microbiol. 42: 575–606.

    Google Scholar 

  • Boulton M.I., W.G. Buchholz, M.S. Marks, P.G. Markham & J.W. Davies, 1989. Specificity of Agrobacterium-mediated delivery of maize streak virus DNA to members of the gramineae. Plant Mol. Biol. 12: 31–40.

    Google Scholar 

  • Breyne P., M. Van Montagu, A. Depicker & G. Gheysen, 1992. Characterization of a plant scaffold attachment region in a DNA fragment that normalizes transgene expression in tobacco. The Plant Cell 4: 463–471.

    Google Scholar 

  • Chan M.-T., T.-M. Lee & H.-H. Chang, 1992. Transformation of indica rice (Oryza sativa L.) mediated by Agrobacterium tumefaciens. Plant Cell Physiol. 33: 577–583.

    Google Scholar 

  • Chee P.P., K.A. Fober & J.L. Slightom, 1989. Transformation of soybean (Glycine max) by infecting germinating seeds with Agrobacterium tumefaciens. Plant Physiol. 91: 1212–1218.

    Google Scholar 

  • Christou P., 1992. Genetic transformation of crop plants using microprojectile bombardment. The Plant Journal 2: 275–281.

    Google Scholar 

  • Christou P. & D.E. McCabe, 1992. Prediction of germ-line transformation events in chimeric R0 transgenic soybean plantlets using tissue-specific expression patterns. The Plant Journal 2(3): 283–290.

    Google Scholar 

  • Christou P., W.F. Swain, N.-S. Yang & D.E. McCabe, 1989. Inheritance and expression of foreign genes in transgenic soybean plants. Proc. Natl. Acad. Sci. 86: 7500–7504.

    Google Scholar 

  • Citovsky V., J. Zupan, D. Warnick & P. Zambryski, 1992. Nuclear localizaton of Agrobacterium VirE2 protein in plant cells. Science 256: 1802–1805.

    Google Scholar 

  • Colby S.M., A.M. Juncosa & C.P. Meredith, 1991. Cellular differences in Agrobacterium susceptibility and regenerative capacity restrict the development of transgenic grapevines. J. Amer. soc. Hort. Sci. 116: 356–361.

    Google Scholar 

  • Conner A.J. & E.M. Dommisse, 1992. Monocotyledonous plants as hosts for Agrobacterium. Int. J. Plant Sci. 153(4): 550–555.

    Google Scholar 

  • D'Halluin K., E. Bonne, M. Bossut, M. De Beuckeleer & J. Leemans, 1992. Transgenic maize plants by tissue electroporation. The Plant Cell 4: 1495–1505.

    Google Scholar 

  • Davey M.R., E.L. Rech & B.J. Mulligan, 1989. Direct DNA transfer to plant cells. Plant Mol. Biol. 13: 273–285.

    Google Scholar 

  • De Block M. & D. Debrouwer, 1991. Two T-DNA's co-transformed into Brassica napus by a double Agrobacterium tumefaciens infection are mainly integrated at the same locus. Theor. Appl. Genet. 82: 257–263.

    Google Scholar 

  • De Block M., D. Debrouwer & P. Tenning, 1989. Transformation of Brassica napus and Brassica oleracea using Agrobacterium tumefaciens and the expression of the bar and neo genes in the transgenic plants. Plant Physiol. 91: 694–701.

    Google Scholar 

  • de Framond A.J., E.W. Back, W.S. Chilton, L. Kayes & M.-D. Chilton, 1986. Two unlinked T-DNAs can transform the same tobacco plant cell and segregate in the F1 generation. Mol. Gen. Genet. 202: 125–131.

    Google Scholar 

  • Depicker A., L. Herman, A. Jacobs, J. Schell & M. Van Montagu, 1985. Frequencies of simultaneous transformation: with different T-DNAs and their relevance to the Agrobacterium/plant cell interaction. Mol. Gen. Genet. 201: 477–484.

    Google Scholar 

  • Dillon N. & F. Grosveld, 1993. Transcriptional regulation of multigene loci: multilevel control. Trends in Genetics 9: 134–137.

    Google Scholar 

  • Dyck P.L., 1987. The association of a gene for leaf rust resistance with the chromosome 7D suppressor of stem rust resistance in common wheat. Genome 29: 467–469.

    Google Scholar 

  • Eissenberg J.C. & S.C.R. Elgin, 1991. Boundary functions in the control of gene expression. Trends in Genetics 7: 335–340.

    Google Scholar 

  • Errampalli D., D. Patton, L. Castle, L. Mickelson, K. Hansen, J. Schnall, K. Feldmann & D. Meinke, 1991. Embryonic lethals and T-DNA insertional mutagenesis in Arabidopsis. Plant Cell 3: 149–157.

    Google Scholar 

  • Feldmann A.K., 1991. T-DNA insertion mutagenesis in Arabidopsis: mutational spectrum. The Plant Journal 1(1): 71–82.

    Google Scholar 

  • Feldmann K.A. & M.D. Marks, 1987. Agrobacterium-mediated transformation of germinating seeds of Arabidopsis thaliana: A non-tissue culture approach. Mol. Gen. Genet. 208: 1–9.

    Google Scholar 

  • Finer J.J. & M.D. McMullen, 1990. Transformation of cotton (Gossypium hirsutum L.) via particle bombardment. Plant Cell Rep. 8: 586–589.

    Google Scholar 

  • Flavell R.B., 1989. Variation in structure and expression of ribosomal DNA loci in wheat. Genome 31: 963–968.

    Google Scholar 

  • Fujiwara T. & R.N. Beachy, 1993. Expression of soybean seed storage protein genes in transgenic plants; their effects on expression of a neightboring gene and position dependency. Plant Cell Physiol. 34: 13–20.

    Google Scholar 

  • Gould J., M. Devey, O. Hasewaga, E.C. Ulian, G. Peterson & R.H. Smith, 1991. Transformation of Zea mays L. using Agrobacterium tumefaciens and the shoot apex. Plant Physiol. 95: 426–434.

    Google Scholar 

  • Hall G., G.C. Allen, D.S. Loer, W.F. Thompson & S. Spiker, 1991. Nuclear scaffolds and scaffold-attachment regions in higher plants. Proc. Natl. Acad. Sci. 88: 9320–9324.

    Google Scholar 

  • Herman L., A. Jacobs, M. Van Montagu & A. Depicker, 1990. Plant chromosome/marker gene fusion assay for study of normal and truncated T-DNA integration events. Mol. Gen. Genet. 224: 248–256.

    Google Scholar 

  • Hilliker A.J. & R. Appels, 1989. The arrangement of interphase chromosomes: structural and functional aspects. Exp. Cell Res. 185: 297–318.

    Google Scholar 

  • Hobbs S.L.A., T.D. Warkentin & C.M.O. Delong, 1993. Transgene copy number can be positively or negatively associated with transgene expression. Plant Mol. Biol. 21: 17–26.

    Google Scholar 

  • Iida A., T. Yamashita, Y. Yamada & H. Morikawa, 1991. Efficiency of particle-bombardment-mediated transformation is influenced by cell stage in synchronized cultured cells of tobacco. Plant Physiol. 97: 1585–1587.

    Google Scholar 

  • Joersbo M. & J. Brunstedt, 1992. Sonication: A new method for gene transfer to plants. Phys. Plant. 85: 230–234.

    Google Scholar 

  • Kartzke S., H. Saedler & P. Meyer, 1990. Molecular analysis of transgenic plants derived from transformations of protoplasts at various stages of the cell cycle. Plant Sci. 67: 63–72.

    Google Scholar 

  • Kellum R. & P. Schedl, 1991. A position-effect assay for boundaries of higher order chromosomal domains. Cell 64: 941–950.

    Google Scholar 

  • Kellum R. & P. Schedl, 1992. A group of scs elements function as domain boundaries in an enhancer-blocking assay. Mol. Cell. Biol. 12: 2424–2431.

    Google Scholar 

  • Kerber E.R. & G.J. Green, 1980. Suppression of stem rust resistance in hexaploid wheat cv. Canthatch by chromosome 7DL. Can. J. Bot. 58: 1347–1350.

    Google Scholar 

  • Kertbundit S., H. De Greve, F. Deboeck, M. Van Montagu & J.-P. Hernalsteens, 1991. In vivo random B-glucuronidase gene fusions in Arabidopsis thaliana. Proc. Natl. Acac. Sci. 88: 5212–5216.

    Google Scholar 

  • Koncz C., N. Martini, R. Mayerhofer, Z. Koncz-Kalman, H. Körber, G.P. Redei & J. Schell, 1989. High-frequency T-DNA-mediated gene tagging in plants. Proc. Natl. Acad. Sci. 86: 8467–8471.

    Google Scholar 

  • Li X.-Q., C.-N. Liu, S.W. Ritchie, J.-Y. Peng, S.B. Gelvin & T.K. Hodges, 1992. Factors influencing Agrobacterium-mediated transient expression of gusA in rice. Plant Mol. Biol. 20: 1037–1048.

    Google Scholar 

  • Linn F., I. Heidmann, H. Saedler & P. Meyer, 1990. Epigenetic changes in the expression of the maize A1 gene in Petunia hybrida: Role of numbers of integrated gene copies and state of methylation. Mol. Gen. Genet. 222: 329–336.

    Google Scholar 

  • Matzke M.A. & A.J.M. Matzke, 1991. Differential inactivation and methylation of a transgene in plants by two suppressor loci containing homologous sequences. Plant Mol. Biol. 16: 821–830.

    Google Scholar 

  • Matzke M.A., M. Primig, J. Trnovsky & A.J.M. Matzke, 1989. Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants. EMBO J 8(3): 643–649.

    Google Scholar 

  • McCabe D.E. & B.J. Martinell, 1993. Transformation of elite cotton cultivars via particle bombardment of meristems. Bio/Technology 11: 596–598.

    Google Scholar 

  • McCabe D.E., W.F. Swain, B.J. Martinell & P. Christou, 1988. Stable transformation of soybean (Glycine max) by particle acceleration. Bio/Technology 6: 923–926.

    Google Scholar 

  • McHughen A., M. Jordan & G. Feist, 1989. A preculture period prior to Agrobacterium inoculation increases production of transgenic plants. J. Plant Physiol. 135: 245–248.

    Google Scholar 

  • McKnight T.D., M.T. Lillis & R.B. Simpson, 1987. Segregation of genes transferred to one plant cell from two separate Agrobacterium strains. Plant Mol. Biol. 8: 439–445.

    Google Scholar 

  • Meyer P., F. Linn, I. Heidmann, H. Meyer, I. Niedenhof & H. Saedler, 1992. Endogenous and environmental factors influence 35S promoter methylation of a maize A1 gene construct in transgenic petunia and its colour phenotype. Mol. Gen. Genet. 231: 343–352.

    Google Scholar 

  • Mooney P.A., P.B. Goodwin, E.S. Dennis & D.J. Llewellyn, 1991. Agrobacterium tumefaciens-gene transfer into wheat tissues. Plant Cell Tissue Organ Culture 25: 209–218.

    Google Scholar 

  • Offringa R., M.J.A. de Groot, H.J. Haagsman, M.P. Does, P.J.M. van der Elzen & P.J.J. Hooykaas, 1990. Extrachromosomal homologous recombination and gene targeting in plant cells after Agrobacterium mediated transformation. EMBO J 9(10): 3077–3084.

    Google Scholar 

  • Offringa R., P.J.M. van den Elzen & P.J.J. Hooykaas, 1992. Gene targeting in plants using the Agrobacterium vector system. Transgenic Res. 1: 114–123.

    Google Scholar 

  • Okada K., I. Takebe & T. Nagata, 1986. Expression and integration of genes introduced into highly synchronized plant protoplasts. Mol. Gen. Genet. 205: 398–403.

    Google Scholar 

  • Omirulleh S., M. Abraham, M. Golovkin, I. Stefanov, M.K. Karabaev, L. Mustardy, S. Morocz & D. Dudits, 1993. Activity of a chimeric promoter with the doubled CaMV 35S enhancer element in protoplast-derived cells and transgenic plants in maize. Plant Mol. Biol. 21: 415–428.

    Google Scholar 

  • Palmgren G., O. Mattson & F.T. Okkels, 1993. Treatment of Agrobacterium or leaf disks with 5-azacytidine increases transgene expression in tobacco. Plant Mol. Biol. 21: 429–435.

    Google Scholar 

  • Peach C. & J. Velten, 1991. Transgene expression variability (position effect) of CAT and GUS reporter genes driven by linked divergent T-DNA promoters. Plant Mol. Biol. 17: 49–60.

    Google Scholar 

  • Potrykus I., 1990. Gene transfer to plants: assessment and perspectives. Phys. Plant. 79: 125–134.

    Google Scholar 

  • Radke S.E., J.C. Turner & D. Facciotti, 1992. Transformation and regeneration of Brassica rapa using Agrobacterium tumefaciens. Plant Cell Rep. 11: 499–505.

    Google Scholar 

  • Raineri D.M., P. Bottino, M.P. Gordon & E.W. Nester, 1990. Agrobacterium-mediated transformation of rice (Oryza sativa L.). Biotechnology 8: 33–38.

    Google Scholar 

  • Raineri D.M., M.I. Boulton, J.W. Davies & E.W. Nester, 1993. VirA, the plant-signal receptor, is responsible for the Ti plasmid-specific transfer of DNA to maize by Agrobacterium. Proc. Natl. Acad. Sci. 90: 3549–3553.

    Google Scholar 

  • Rathore K.S., V.K. Chowdhury & T.K. Hodges, 1993. Use of bar as a selectable marker gene and for the production of herbicide-resistant rice plants from protoplasts. Plant Mol. Biol. 21: 871–884.

    Google Scholar 

  • Sahi S.V., M.-D. Chilton & W.S. Chilton, 1990. Corn metabolites affect growth and virulence of Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. 87: 3879–3883.

    Google Scholar 

  • Scheid O.M., J. Paszkowski & I. Potrykus, 1991. Reversible inactivation of a transgene in Arabidopsis thaliana. Mol. Gen. Genet. 228: 104–112.

    Google Scholar 

  • Spencer T.M., J.V. O'Brien, W.G. Start & T.R. Adams, 1992. Segregation of transgenes in maize. Plant Mol. Biol. 18: 201–210.

    Google Scholar 

  • Valvekens D., M. Van Montagu & M. Van Lijsebettens, 1988. Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc. Natl. Acad. Sci. 85: 5536–5540.

    Google Scholar 

  • Van Lijsebettens M., B. den Boer, J.-P. Hernalsteens & M. Van Montagu, 1991. Insertional mutagenesis in Arabidopsis thaliana. Plant Sci. 80: 27–37.

    Google Scholar 

  • Van Lijsebettens M., D. Inzé, J. Schell & M. Van Montagu, 1986. Transformed cell clones as a tool to study T-DNA integration mediated by Agrobacterium tumefaciens. J. Mol. Biol. 188: 129–145.

    Google Scholar 

  • Van Lijsebettens, R. Vanderhaeghen & M. Van Montagu, 1991. Insertional mutagenesis in Arabidopsis thaliana: isolation of a T-DNA-linked mutation that alters leaf morphology. Theor. Appl. Genet. 81: 277–284.

    Google Scholar 

  • van Wordragen M.F. & H.J.M. Dons, 1992. Agrobacterium tumefaciens-mediated transformation of recalcitrant crops. Plant Mol. Biol. Rep. 10: 12–36.

    Google Scholar 

  • Vasil V., A.M. Castillo, M.E. Fromm & I.K. Vasil, 1992. Herbicide resistant fertile transgenic wheat plants obtained by microprojectile bombardment of regenerable embryogenic callus. Bio/Technology 10: 667–674.

    Google Scholar 

  • Walter C., I. Broer, D. Hillemann & A. Pühler, 1992. High frequency, heat treatment-induced inactivation of the phosphinothricin resistance gene in transgenic single cell suspension cultures of Medicago sativa. Mol. Gen. Genet. 235: 189–196.

    Google Scholar 

  • Zambryski P.C., 1992. Chronicles from the Agrobacterium-plant cell DNA transfer story. Ann. Rev. Plant Physiol. and Plant Mol. Biol. 43: 465–490.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

De Block, M. The cell biology of plant transformation: Current state, problems, prospects and the implications for the plant breeding. Euphytica 71, 1–14 (1993). https://doi.org/10.1007/BF00023461

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00023461

Key words

Navigation