BioMed Research International

BioMed Research International / 2006 / Article

Review Article | Open Access

Volume 2006 |Article ID 25376 | 7 pages | https://doi.org/10.1155/JBB/2006/25376

The Mutational Consequences of Plant Transformation

Received13 Jul 2005
Revised17 Nov 2005
Accepted22 Nov 2005
Published01 Mar 2006

Abstract

Plant transformation is a genetic engineering tool for introducing transgenes into plant genomes. It is now being used for the breeding of commercial crops. A central feature of transformation is insertion of the transgene into plant chromosomal DNA. Transgene insertion is infrequently, if ever, a precise event. Mutations found at transgene insertion sites include deletions and rearrangements of host chromosomal DNA and introduction of superfluous DNA. Insertion sites introduced using Agrobacterium tumefaciens tend to have simpler structures but can be associated with extensive chromosomal rearrangements, while those of particle bombardment appear invariably to be associated with deletion and extensive scrambling of inserted and chromosomal DNA. Ancillary procedures associated with plant transformation, including tissue culture and infection with A tumefaciens, can also introduce mutations. These genome-wide mutations can number from hundreds to many thousands per diploid genome. Despite the fact that confidence in the safety and dependability of crop species rests significantly on their genetic integrity, the frequency of transformation-induced mutations and their importance as potential biosafety hazards are poorly understood.

References

  1. B {Tinland}, “The integration of T-DNA into plant genomes,” Trends in Plant Science, vol. 1, no. 6, pp. 178–184, 1996. View at: Google Scholar
  2. T Tzfira, J Li, B Lacroix, and V Citovsky, “Agrobacterium T-DNA integration: molecules and models,” Trends in Genetics, vol. 20, no. 8, pp. 375–383, 2004. View at: Google Scholar
  3. D A Somers and I Makarevitch, “Transgene integration in plants: poking or patching holes in promiscuous genomes?,” Current Opinion in Biotechnology, vol. 15, no. 2, pp. 126–131, 2004. View at: Google Scholar
  4. J M Alonso, A N Stepanova, T J Leisse et al., “Genome-wide insertional mutagenesis of Arabidopsis thaliana,” Science, vol. 301, no. 5633, pp. 653–657, 2003. View at: Google Scholar
  5. S M Jain, “Tissue culture-derived variation in crop improvement,” Euphytica, vol. 118, no. 2, pp. 153–166, 2001. View at: Google Scholar
  6. P J Krysan, J C Young, and M R Sussman, “T-DNA as an insertional mutagen in Arabidopsis,” The Plant Cell, vol. 11, no. 12, pp. 2283–2290, 1999. View at: Google Scholar
  7. M Bardini, M Labra, M Winfield, and F Sala, “Antibiotic-induced DNA methylation changes in calluses of Arabidopsis thaliana,” Plant Cell, Tissue and Organ Culture, vol. 72, no. 2, pp. 157–162, 2003. View at: Google Scholar
  8. J M Lucht, B Mauch-Mani, H-Y Steiner, J-P Metraux, J Ryals, and B Hohn, “Pathogen stress increases somatic recombination frequency in Arabidopsis,” Nature Genetics, vol. 30, no. 3, pp. 311–314, 2002. View at: Google Scholar
  9. A Madlung and L Comai, “The effect of stress on genome regulation and structure,” Annals of Botany, vol. 94, no. 4, pp. 481–495, 2004. View at: Google Scholar
  10. G J Budziszewski, S P Lewis, L W Glover et al., “Arabidopsis genes essential for seedling viability: isolation of insertional mutants and molecular cloning,” Genetics, vol. 159, no. 4, pp. 1765–1778, 2001. View at: Google Scholar
  11. L A Castle, D Errampalli, T L Atherton, L H Franzmann, E S Yoon, and D W Meinke, “Genetic and molecular characterization of embryonic mutants identified following seed transformation in Arabidopsis,” Molecular and General Genetics: MGG, vol. 241, no. 5-6, pp. 504–514, 1993. View at: Google Scholar
  12. G Gheysen, M Van Montagu, and P Zambryski, “Integration of Agrobacterium tumefaciens transfer DNA (T-DNA) involves rearrangements of target plant DNA sequences,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 17, pp. 6169–6173, 1987. View at: Google Scholar
  13. S-R Kim, J Lee, S-H Jun et al., “Transgene structures in T-DNA-inserted rice plants,” Plant Molecular Biology, vol. 52, no. 4, pp. 761–773, 2003. View at: Google Scholar
  14. S Kumar and M Fladung, “Transgene integration in aspen: structures of integration sites and mechanism of T-DNA integration,” The Plant Journal, vol. 31, no. 4, pp. 543–551, 2002. View at: Google Scholar
  15. A Forsbach, D Schubert, B Lechtenberg, M Gils, and R Schmidt, “A comprehensive characterization of single-copy T-DNA insertions in the Arabidopsis thaliana genome,” Plant Molecular Biology, vol. 52, no. 1, pp. 161–176, 2003. View at: Google Scholar
  16. H Kaya, S Sato, S Tabata, Y Kobayashi, M Iwabuchi, and T Araki, “hosoba toge toge, a syndrome caused by a large chromosomal deletion associated with a T-DNA insertion in Arabidopsis,” Plant & Cell Physiology, vol. 41, no. 9, pp. 1055–1066, 2000. View at: Google Scholar
  17. E Revenkova, J Masson, C Koncz, K Afsar, L Jakovleva, and J Paszkowski, “Involvement of Arabidopsis thaliana ribosomal protein S27 in mRNA degradation triggered by genotoxic stress,” The EMBO Journal, vol. 18, no. 2, pp. 490–499, 1999. View at: Google Scholar
  18. P Amedeo, Y Habu, K Afsar, O Mittelsten Scheid, and J Paszkowski, “Disruption of the plant gene MOM releases transcriptional silencing of methylated genes,” Nature, vol. 405, no. 6783, pp. 203–206, 2000. View at: Google Scholar
  19. S Filleur, M-F Dorbe, M Cerezo et al., “An Arabidopsis T-DNA mutant affected in Nrt2 genes is impaired in nitrate uptake,” FEBS Letters, vol. 489, no. 2-3, pp. 220–224, 2001. View at: Google Scholar
  20. F E Tax and D M Vernon, “T-DNA-associated duplication/translocations in Arabidopsis. Implications for mutant analysis and functional genomics,” Plant Physiology, vol. 126, no. 4, pp. 1527–1538, 2001. View at: Google Scholar
  21. P Nacry, C Camilleri, B Courtial, M Caboche, and D Bouchez, “Major chromosomal rearrangements induced by T-DNA transformation in Arabidopsis,” Genetics, vol. 149, no. 2, pp. 641–650, 1998. View at: Google Scholar
  22. Y Sha, S Li, Z Pei, L Luo, Y Tian, and C He, “Generation and flanking sequence analysis of a rice T-DNA tagged population,” Theoretical and Applied Genetics, vol. 108, no. 2, pp. 306–314, 2004. View at: Google Scholar
  23. A S Afolabi, B Worland, J W Snape, and P Vain, “A large-scale study of rice plants transformed with different T-DNAs provides new insights into locus composition and T-DNA linkage configurations,” Theoretical and Applied Genetics, vol. 109, no. 4, pp. 815–826, 2004. View at: Google Scholar
  24. S Chen, W Jin, M Wang et al., “Distribution and characterization of over 1000 T-DNA tags in rice genome,” The Plant Journal, vol. 36, no. 1, pp. 105–113, 2003. View at: Google Scholar
  25. W P Pawlowski and D A Somers, “Transgenic DNA integrated into the oat genome is frequently interspersed by host DNA,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 21, pp. 12106–12110, 1998. View at: Google Scholar
  26. S Uthayakumaran, O M Lukow, M C Jordan, and S Cloutier, “Development of genetically modified wheat to assess its dough functional properties,” Molecular Breeding, vol. 11, no. 4, pp. 249–258, 2003. View at: Google Scholar
  27. A Kohli, R M Twyman, R Abranches, E Wegel, E Stoger, and P Christou, “Transgene integration, organization and interaction in plants,” Plant Molecular Biology, vol. 52, no. 2, pp. 247–258, 2003. View at: Google Scholar
  28. S A Jackson, P Zhang, W P Chen et al., “High-resolution structural analysis of biolistic transgene integration into the genome of wheat,” Theoretical and Applied Genetics, vol. 103, no. 1, pp. 56–62, 2001. View at: Google Scholar
  29. P Windels, I Taverniers, A Depicker, E Van Bockstaele, and M De Loose, “Characterisation of the Roundup Ready soybean insert,” European Food Research and Technology, vol. 213, no. 2, pp. 107–112, 2001. View at: Google Scholar
  30. K Shimizu, M Takahashi, N Goshima, S Kawakami, K Irifune, and H Morikawa, “Presence of an SAR-like sequence in junction regions between an introduced transgene and genomic DNA of cultured tobacco cells: its effect on transformation frequency,” The Plant Journal, vol. 26, no. 4, pp. 375–384, 2001. View at: Google Scholar
  31. I Makarevitch, S K Svitashev, and D A Somers, “Complete sequence analysis of transgene loci from plants transformed via microprojectile bombardment,” Plant Molecular Biology, vol. 52, no. 2, pp. 421–432, 2003. View at: Google Scholar
  32. M Hernández, M Pla, T Esteve, S Prat, P Puigdomènech, and A Ferrando, “A specific real-time quantitative PCR detection system for event MON810 in maize YieldGard based on the 3-transgene integration sequence,” Transgenic Research, vol. 12, no. 2, pp. 179–189, 2003. View at: 3-transgene%20integration%20sequence&author=M Hernández&author=M Pla&author=T Esteve&author=S Prat&author=P Puigdomènech&author=&author=A Ferrando&publication_year=2003" target="_blank">Google Scholar
  33. B Ülker, A K Weissinger, and S Spiker, “E. coli chromosomal DNA in a transgene locus created by microprojectile bombardment in tobacco,” Transgenic Research, vol. 11, no. 3, pp. 311–313, 2002. View at: Google Scholar
  34. D-H Jeong, S An, H-G Kang et al., “T-DNA insertional mutagenesis for activation tagging in rice,” Plant Physiology, vol. 130, no. 4, pp. 1636–1644, 2002. View at: Google Scholar
  35. T Ichikawa, M Nakazawa, M Kawashima et al., “Sequence database of 1172 T-DNA insertion sites in Arabidopsis activation-tagging lines that showed phenotypes in T1 generation,” The Plant Journal, vol. 36, no. 3, pp. 421–429, 2003. View at: Google Scholar
  36. L Szabados, I Kovács, A Oberschall et al., “Distribution of 1000 sequenced T-DNA tags in the Arabidopsis genome,” The Plant Journal, vol. 32, no. 2, pp. 233–242, 2002. View at: Google Scholar
  37. C-H Ryu, J-H You, H-G Kang et al., “Generation of T-DNA tagging lines with a bidirectional gene trap vector and the establishment of an insertion-site database,” Plant Molecular Biology, vol. 54, no. 4, pp. 489–502, 2004. View at: Google Scholar
  38. G J Hannon, “RNA interference,” Nature, vol. 418, no. 6894, pp. 244–251, 2002. View at: Google Scholar
  39. B Bartel and D P Bartel, “MicroRNAs: at the root of plant development?,” Plant Physiology, vol. 132, no. 2, pp. 709–717, 2003. View at: Google Scholar
  40. M Kusaba, K Miyahara, S Iida et al., “Low glutelin content1: a dominant mutation that suppresses the glutelin multigene family via RNA silencing in rice,” The Plant Cell, vol. 15, no. 6, pp. 1455–1467, 2003. View at: Google Scholar
  41. M M Fitch, R M Manshardt, D Gonsalves, J L Slightom, and J C Sanford, “Virus resistant papaya derived from tissues bombarded with the coat protein gene of papaya ringspot virus,” Biotechnology, vol. 10, pp. 1466–1472, 1992. View at: Google Scholar
  42. A Rang, B Linke, and B Jansen, “Detection of RNA variants transcribed from the transgene in Roundup Ready soybean,” European Food Research and Technology, vol. 220, no. 3-4, pp. 438–443, 2005. View at: Google Scholar
  43. D Weigel, J H Ahn, M A Blázquez et al., “Activation tagging in Arabidopsis,” Plant Physiology, vol. 122, no. 4, pp. 1003–1013, 2000. View at: Google Scholar
  44. M Prudhomme, V Libante, and J-P Claverys, “Homologous recombination at the border: insertion-deletions and the trapping of foreign DNA in Streptococcus pneumoniae,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 4, pp. 2100–2105, 2002. View at: Google Scholar
  45. J de Vries and W Wackernagel, “Integration of foreign DNA during natural transformation of Acinetobacter {sp.} by homology-facilitated illegitimate recombination,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 4, pp. 2094–2099, 2002. View at: Google Scholar
  46. A K Wilson, J R Latham, and R A Steinbrecher, “Genome Scrambling-Myth or reality? Transformation-induced mutations in transgenic crop plants,” Technical Report, EcoNexus, Brighton, UK, 2004. View at: Google Scholar
  47. M Cailloux, “Plant tissue culture: rapid propagation, induced mutations, and the potential role of protoplast techniques,” in Crop Breeding: A Contemporary Basis, P B Vose and S G Blixt, Eds., pp. 311–345, Pergamon, Oxford, UK, 1984. View at: Google Scholar
  48. P J Larkin and W R Scowcroft, “Somaclonal variation—a novel source of variability from cell cultures for plant improvement,” Theoretical and Applied Genetics, vol. 60, no. 4, pp. 197–214, 1981. View at: Google Scholar
  49. A D Arencibia, E Gentinetta, E Cuzzoni et al., “Molecular analysis of the genome of transgenic rice (Oryza sativa L.) plants produced via particle bombardment or intact cell electroporation,” Molecular Breeding, vol. 4, no. 2, pp. 99–109, 1998. View at: Google Scholar
  50. P H Bao, S Granata, S Castiglione et al., “Evidence for genomic changes in transgenic rice (Oryza sativa L.) recovered from protoplasts,” Transgenic Research, vol. 5, no. 2, pp. 97–103, 1996. View at: Google Scholar
  51. G Wang, S Castiglione, Y Chen et al., “Poplar (Populus nigra L.) plants transformed with a Bacillus thuringiensis toxin gene: insecticidal activity and genomic analysis,” Transgenic Research, vol. 5, no. 5, pp. 289–301, 1996. View at: Google Scholar
  52. M Labra, C Savini, M Bracale et al., “Genomic changes in transgenic rice (Oryza sativa L.) plants produced by infecting calli with Agrobacterium tumefaciens,” Plant Cell Reports, vol. 20, no. 4, pp. 325–330, 2001. View at: Google Scholar
  53. A D Arencibia, E R Carmona, M T Cornide et al., “Somaclonal variation in insect-resistant transgenic sugarcane (Saccharum hybrid) plants produced by cell electroporation,” Transgenic Research, vol. 8, no. 5, pp. 349–360, 1999. View at: Google Scholar
  54. M Labra, C Vannini, F Grassi et al., “Genomic stability in Arabidopsis thaliana transgenic plants obtained by floral {dip},” Theoretical and Applied Genetics, vol. 109, no. 7, pp. 1512–1518, 2004. View at: Google Scholar
  55. F Sala, A D Arencibia, S Castiglione et al., “Somaclonal variation in transgenic plants,” Acta Horticulturae, vol. 530, pp. 411–420, 2000. View at: Google Scholar
  56. A G Haslberger, “Codex guidelines for GM foods include the analysis of unintended effects,” Nature Biotechnology, vol. 21, no. 7, pp. 739–741, 2003. View at: Google Scholar
  57. H A Kuiper, G A Kleter, H PJM Noteborn, and E J Kok, “Assessment of the food safety issues related to genetically modified foods,” The Plant Journal, vol. 27, no. 6, pp. 503–528, 2001. View at: Google Scholar
  58. K K Donegan, C J Palm, V J {Fieland} et al., “Changes in levels, species and DNA fingerprints of soil microorganisms associated with cotton expressing the Bacillus thuringiensis var. kurstaki endotoxin,” Applied Soil Ecology, vol. 2, no. 2, pp. 111–124, 1995. View at: Google Scholar
  59. H-L Pasonen, S-K Seppänen, Y Degefu, A Rytkönen, K von Weissenberg, and A Pappinen, “Field performance of chitinase transgenic silver birches (Betula pendula): resistance to fungal diseases,” Theoretical and Applied Genetics, vol. 109, no. 3, pp. 562–570, 2004. View at: Google Scholar
  60. A NE Birch, I E Geoghegan, D W Griffiths, and J W McNicol, “The effect of genetic transformations for pest resistance on foliar solanidine-based glycoalkaloids of potato (Solanum tuberosum),” Annals of Applied Biology, vol. 140, no. 2, pp. 143–149, 2002. View at: Google Scholar
  61. J Bergelson, C B Purrington, and G Wichmann, “Promiscuity in transgenic plants,” Nature, vol. 395, no. 6697, p. 25, 1998. View at: Google Scholar
  62. J M Jr Gertz, W K Vencill, and N S Hill, “Tolerance of transgenic soybean (Glycine max) to heat stress,” in Proceedings of the 1999 Brighton Conference Weeds (The BCPC Conference), vol. 3, pp. 835–840, Brighton, UK, November 1999. View at: Google Scholar
  63. G G Presting, O P Smith, and C R Brown, “Resistance to potato leafroll virus in potato plants transformed with the coat protein gene or with vector control constructs,” Phytopathology, vol. 85, no. 4, pp. 436–442, 1995. View at: Google Scholar
  64. S S Mahmoud and R B Croteau, “Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 15, pp. 8915–8920, 2001. View at: Google Scholar
  65. E Millstone, E Brunner, and S Mayer, “Beyond ‘substantial equivalence’,” Nature, vol. 401, no. 6753, pp. 525–526, 1999. View at: Google Scholar
  66. W Freese and D Schubert, “Safety testing and regulation of genetically engineered foods,” Biotechnology and Genetic Engineering Reviews, vol. 21, pp. 299–324, 2004. View at: Google Scholar
  67. A Spök, H Hofer, P Lehner, R Valenta, S Stirn, and H Gaugitsch, “Risk Assessment of GMO-Products in the European Union,” Bundesministerium für Gesundheit und Frauen, 2004. View at: Google Scholar

Copyright © 2006 Jonathan R. Latham et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

0 Views | 0 Downloads | 0 Citations
 PDF  Download Citation  Citation
 Order printed copiesOrder