Skip to main content
Log in

Microbial horizontal gene transfer and the DNA release from transgenic crop plants

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Intraspecific and interspecific horizontal gene transfers among prokaryotes by mechanisms like conjugation, transduction and transformation are part of their life style. Experimental data and nucleotide sequence analyses show that these processes appear to occur in any prokaryotic habitat and have shaped microbial genomes throughout evolution over hundreds of million years. Here we summarize studies with a focus on the possibility of the transfer of free recombinant DNA released from transgenic plants to microorganisms by transformation. A list of 87 species capable of natural transformation is presented. We discuss monitoring techniques which allowed detection of the spread of intact DNA from plants during their growth, in the process of decay and by pollen dispersal including novel biomonitoring assays for measuring the transforming potential of DNA in the environment. Also, studies on the persistence of free DNA in soil habitats and the potential of bacteria to take up DNA in soil are summarized. On the other hand, the various barriers evolved in prokaryotes which suppress interspecific gene transfer and recombination will be addressed along with studies aiming to estimate the chance of a gene transfer from plant to microbe. The results suggest that, although such transfers could be possible in principle, each of the many steps involved from the release of intact DNA from a plant cell to integration into a prokaryotic genome has such a low probability that a successful transfer event be extremely rare. Further, interspecies transfer of chromosomal DNA is mostly negative for the recipient, and, if not, in the absence of a selective advantage the transformant will be lost. It is stressed that the nucleotide sequences introduced into transgenic plants are much less likely to be captured from the transgenic plants than directly from those organisms (often bacteria or viruses) from which they were originally derived.

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

  • Achtman M and Hakenbeck R 1992 Recent developments regarding the evolution of pathogenic bacteria. In Molecular Biology of Bacterial Infection: Current Status and Future Perspective. Ed. C E Hormaeche. pp. 13–31. Cambridge: SGM/Cambridge University, UK.

    Google Scholar 

  • Ahrenholtz I, Lorenz M G and Wackernagel W 1994 The extracellular nuclease of Serratia marcescens: studies on the activity in vitro and effect on transforming DNA in a groundwater aquifer microcosm. Arch. Microbiol. 161, 176–183.

    CAS  PubMed  Google Scholar 

  • Albritton W L, Setlow J K, Thomas M, Sottnek F and Steigerwalt A G 1984 Heterospecific transformation in the genus Haemophilus. Mol. Gen. Genet. 193, 358–363.

    Article  CAS  PubMed  Google Scholar 

  • Arber W 2000 Genetic variation: molecular mechanisms and impact on microbial evolution. FEMS Microbiol. Rev. 24, 1–7.

    CAS  PubMed  Google Scholar 

  • Baur B, Hanselmann K, Schlimme W and Jenni B 1996 Genetic transformation in freshwater: Escherichia coli is able to develop natural competence. Appl. Environ. Microbiol. 62, 3673–3678.

    CAS  PubMed  Google Scholar 

  • Berg D E, Davies J, Allet B and Rochaix J-D 1975 Transposition of R factor genes to bacteriophage λ. Proc. Natl. Acad. Sci. USA 72, 3628–3632.

    CAS  PubMed  Google Scholar 

  • Berndt C, Meier P and Wackernagel W 2003 DNA restriction is a barrier to natural transformation in Pseudomonas stutzeri. Microbiology 149, 895–901.

    Article  CAS  PubMed  Google Scholar 

  • Bertolla F and Simonet P 1999 Horizontal gene transfers in the environment: natural transformation as a putative process for gene transfers between transgenic plants and microorganisms. Res. Microbiol. 150, 375–384.

    Article  CAS  PubMed  Google Scholar 

  • Bertolla F, Van Gijsegem F, Nesme X and Simonet P 1997 Conditions for natural transformation of Ralstonia solanacearum. Appl. Environ. Microbiol. 63, 4965–4968.

    CAS  PubMed  Google Scholar 

  • Bierne H, Ehrlich S D and Michel B 1997 Deletions at stalled replication forks occur by two different pathways. EMBO J. 16, 3332–3340.

    Article  CAS  PubMed  Google Scholar 

  • Blum S A E, Lorenz M G and Wackernagel W 1997 Mechanism of retarded DNA degradation and prokaryotic origin of DNases in nonsterile soil. System. Appl. Microbiol. 20, 513–521.

    CAS  Google Scholar 

  • Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, Weissenbach J, Ehrlich S D and Sorokin A 2001 The complete genome sequence of the lactic acid bacterium Lactococcus ssp. lactis IL 1403. Genome Res. 11, 731–753.

    Article  CAS  PubMed  Google Scholar 

  • Bräutigam M, Hertel C and Hammes W P 1997 Evidence for natural transformation of Bacillus subtilis in foodstuffs. FEMS Microbiol. Lett. 155, 93–98.

    Article  PubMed  Google Scholar 

  • Bron S, Luxen E and Venema G 1980 Restriction and modification in B. subtilis. Mol. Gen. Genet. 179, 103–110.

    CAS  PubMed  Google Scholar 

  • Canosi U, Iglesias A and Trautner T A 1981 Plasmid transformation in Bacillus subtilis: Effects of insertion of Bacillus subtilis DNA into plasmid pC194. Mol. Gen. Genet. 181, 434–440.

    Article  CAS  PubMed  Google Scholar 

  • Carlson C A, Pierson L S, Rosen J J and Ingraham J L 1983 Pseudomonas stutzeri and related species undergo natural transformation. J. Bacteriol. 153, 93–99.

    CAS  PubMed  Google Scholar 

  • Chamier B, Lorenz M G and Wackernagel W 1993 Natural transformation of Acinetobacter calcoaceticus by plasmid DNA adsorbed on sand and groundwater aquifer material. Appl. Environ. Microbiol. 59, 1662–1667.

    CAS  PubMed  Google Scholar 

  • Cohan F M 2002 Sexual isolation and speciation in bacteria. Genetica 116, 359–370.

    Article  CAS  PubMed  Google Scholar 

  • Correia F F, McKay T L, Farrow M F, Rosan B and DiRienzo J M 1996 Natural transformation of Streptococcus crista. FEMS Microbiol. Lett. 143, 13–18. Davison J 1999 Genetic exchange between bacteria in the environment. Plasmid 42, 73–91.

    CAS  PubMed  Google Scholar 

  • Day M 1998 Transformation in aquatic environments. In Horizontal gene transfer. Eds. M Syvanen and C Kado. pp 144–167. Chapman & Hall, London, UK

    Google Scholar 

  • Demanèche S, Bertolla F, Buret F, Nalin R, Sailland A, Auriol P, Vogel T M and Simonet P 2001a Laboratory-scale evidence for lightning-mediated gene transfer in soil. Appl. Environ. Microbiol. 67, 3440–3444.

    PubMed  Google Scholar 

  • Demanèche S, Kay E, Gourbière F and Simonet P 2001b Natural transformation of Pseudomonas fluorescens and Agrobacterium tumefaciens in soil. Appl. Environ. Microbiol. 67, 2617–2621.

    PubMed  Google Scholar 

  • de Vries J, Meier P and Wackernagel W 2001 The natural transformation of Pseudomonas stutzeri and Acinetobacter sp. by kanamycin resistance genes (nptII) present in plasmids and the genome of transgenic plants depends on homologous sequences in the recipient cells. FEMS Microbiol. Lett. 195, 211–215.

    Article  PubMed  Google Scholar 

  • de Vries J and Wackernagel W 1998 Detection of nptII (kanamycin resistance) genes in genomes of transgenic plants by marker rescue transformation. Mol. Gen. Genet. 257, 606–613.

    PubMed  Google Scholar 

  • de Vries J and Wackernagel W 2002 Integration of foreign DNA during natural transformation of Acinetobacter sp. by homology-facilitated illegitimate recombination. Proc. Natl. Acad. Sci. USA 99, 2094–2099.

    PubMed  Google Scholar 

  • de Vries J, Heine M, Harms K and Wackernagel W 2003 Spread of recombinant DNA by roots and pollen of transgenic potato plants, identified by highly specific biomonitoring using natural transformation of an Acinetobacter sp. Appl. Environ. Microbiol. 69, in press.

  • Dietz A 1993 Risk assessment of genetically modified plants introduced into the environment. In Transgenic organisms. Risk assessment of deliberate release. Eds. W Wöhrmann and J Tomiuk. pp 209–227. Birkhäuser-Verlag, Basel, Switzerland.

    Google Scholar 

  • Dower W J, Miller J F and Ragsdale C W 1988 High-efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 16, 6127–6145.

    CAS  PubMed  Google Scholar 

  • Dubnau D 1999 DNA uptake in bacteria. Annu. Rev. Microbiol. 53, 217–244.

    Article  CAS  PubMed  Google Scholar 

  • Dutta C and Pan A 2002 Horizontal gene transfer and bacterial diversity. J. Biosci. 27, 27–33.

    PubMed  Google Scholar 

  • Ehrlich S D 1989 Illegitimate recombination in bacteria. In Mobile DNA. Eds. D E Berg and M M Howe. pp 799–824. American Society for Microbiology, Washington, D.C., USA.

    Google Scholar 

  • Frigaard N U and Bryant D 2001 Chromosomal gene inactivation in the green sulfur bacterium Chlorobium tepidum by natural transformation. Appl. Environ. Microbiol. 67, 2538–2544.

    Article  CAS  PubMed  Google Scholar 

  • Frischer M E, Williams H G, Bennison B, Drake G R, Balkwill D L and Paul J H 1996 The naturally transformable marine bacterium WJT-1C formally identified as ‘Vibrio’ is pseudomonad. Curr. Microbiol. 33, 287–291.

    Article  CAS  PubMed  Google Scholar 

  • Gebhard F and Smalla K 1998 Transformation of Acinetobacter sp. strain BD413 by transgenic sugar beet DNA. Appl. Environ. Microbiol. 64, 1550–1554.

    CAS  PubMed  Google Scholar 

  • Gebhard F and Smalla K 1999 Monitoring field releases of genetically modified sugar beets for persistence of transgenic plant DNA and horizontal gene transfer. FEMS Microbiol. Ecol. 28, 261–272.

    CAS  Google Scholar 

  • Graupner S and Wackernagel W 1996 Identification of multiple plasmids released from recombinant genomes of Hansenula polymorpha by transformation of Escherichia coli. Appl. Environ. Microbiol. 62, 1839–1841.

    CAS  PubMed  Google Scholar 

  • Hacker J and Kaper JB 2000 Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54, 641–679.

    Article  CAS  PubMed  Google Scholar 

  • Hanahan D 1983 Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166, 557–580.

    CAS  PubMed  Google Scholar 

  • Hanahan D 1987 Mechanisms of DNA transformation In Escherichia coli and Salmonella typhimurium. Eds. F C Neidhardt et al. pp 1177–1183. American Society for Microbiology, Washington, D.C., USA.

    Google Scholar 

  • Jonas D A, Elmadfa I, Engel K-H, Heller K J, Kozianowski G, König A, Müller D, Narbonne J-F, Wackernagel W and Kleiner J 2001 Safety considerations of DNA in food. Ann. Nutr. Metab. 45, 1–20.

    Article  Google Scholar 

  • Kay E, Vogel T M, Bertolla F, Nalin R and Simonet P 2002 In situ transfer of antibiotic resistance genes from transgenic (transplastomic) tobacco plants to bacteria. Appl. Environ. Microbiol. 68, 3345–3351.

    Article  CAS  PubMed  Google Scholar 

  • Kennan R M, Dhungyel O P, Whittington R J, Egerton J R and Rood J I 2001 The type IV fimbrial subunit gene (finA) of Dichelobacter nodosus is essential for virulence, protease secretion, and natural competence. J. Bacteriol. 183, 4451–4458.

    Article  CAS  PubMed  Google Scholar 

  • Khanna M and Stotzky G 1992 Transformation of Bacillus subtilis by DNA bound on montmorillonite and effect of DNase on the transforming ability of bound DNA. Appl. Environ. Microbiol. 58, 1930–1939.

    CAS  PubMed  Google Scholar 

  • Koncz C and Schell J 1986 The promoter of T L -DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol. Gen. Genet. 204, 383–396.

    Article  CAS  Google Scholar 

  • Lacks S A 2000 DNA uptake by transformable bacteria. In Transport of molecules across microbial membranes. Eds. J K Broome-Smith, S Baumberg, C J Stirling and F B Ward. pp 138–168. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Lacks S A and Springhorn S S 1984 Transfer of recombinant plasmids containing the gene for DpnII DNA methylase into strains of Streptococcus pneumoniae that produce DpnI or DpnII restriction endonucleases. J. Bacteriol. 158, 905–909.

    CAS  PubMed  Google Scholar 

  • Lawrence J G and Ochman H 1998 Molecular archaeology of the Escherichia coli genome. Proc. Natl. Acad. Sci. USA 95, 9413–9417.

    Article  CAS  PubMed  Google Scholar 

  • Li Y-H, Lau P C Y, Lee J H, Ellen R P and Cvitkovitch D G 2001 Natural genetic transformation of Streptococcus mutans growing in biofilms. J. Bacteriol. 183, 897–908.

    CAS  PubMed  Google Scholar 

  • Lorenz M G, Aardema B W and Wackernagel W 1998 Highly efficient genetic transformation of Bacillus subtilis attached to sand grains. J. Gen. Microbiol. 134, 107–112.

    Google Scholar 

  • Lorenz M G and Sikorski J 2000 The potential for intraspecific horizontal gene exchange by natural genetic transformation: sexual isolation among genomovars of Pseudomonas stutzeri. Microbiology 146, 3081–3090.

    CAS  PubMed  Google Scholar 

  • Lorenz M G and Wackernagel W 1987 Adsorption of DNA to sand and variable degradation rates of adsorbed DNA. Appl. Environ. Microbiol. 53, 2948–2952.

    CAS  PubMed  Google Scholar 

  • Lorenz M G and Wackernagel W 1990 Natural genetic transformation of Pseudomonas stutzeri by sand-adsorbed DNA. Arch. Microbiol. 154, 380–385.

    Article  CAS  PubMed  Google Scholar 

  • Lorenz M G and Wackernagel W 1992 DNA binding to various clay minerals and retarded enzymatic degradation of DNA in a sand/clay microcosm. In Gene Transfers and Environment. Ed. M J Gauthier. pp 103–113. Springer-Verlag, New York.

    Google Scholar 

  • Lorenz M G and Wackernagel W 1994 Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Rev. 58, 563–602.

    CAS  PubMed  Google Scholar 

  • Majewski J 2001 Sexual isolation in bacteria. FEMS Microbiol. Lett. 199, 161–169.

    CAS  PubMed  Google Scholar 

  • Majewski J, Zawadzki P, Pickerill P, Cohan F M and Dowson C G 2000 Barriers to genetic exchange between bacterial species: Streptococcus pneumoniae transformation. J. Bacteriol. 182, 1016–1023.

    Article  CAS  PubMed  Google Scholar 

  • McDermott P F, Zhao S, Wagner D D, Simjee S, Walker R D and White D G 2002 The food safety perspective antibiotic resistance. Anim. Biotechnol. 13, 71–84.

    Article  CAS  PubMed  Google Scholar 

  • Meier P and Wackernagel W 2003a Monitoring the spread of recombinant DNA from field plots with transgenic sugar beet plants by PCR and natural transformation of Pseudomonas stutzeri. Transgenic Res. 12, 293–304.

    Article  CAS  PubMed  Google Scholar 

  • Meier P and Wackernagel W 2003b Mechanisms of homology-facilitated illegitimate recombination for foreign DNA acquisition in transformable Pseudomonas stutzeri. Mol. Microbiol. 48, 1107–1118.

    Article  CAS  PubMed  Google Scholar 

  • Meima R, Haan G-J, Venema G, Bron S and de Jong S 1998 Sequence specificity of illegitimate plasmid recombination in Bacillus subtilis: Possible recognition sites for DNA topoisomerase I. Nucleic Acids Res. 26, 2366–2373.

    Article  CAS  PubMed  Google Scholar 

  • Mercer D K, Melville C M, Scott K P and Flint H J 1999 Natural genetic transformation in the rumen bacterium Streptococcus bovis JB1. FEMS Microbiol. Lett. 179, 485–490.

    CAS  PubMed  Google Scholar 

  • Mercer D K, Scott K P, Melville C M, Glover L A and Flint H J 2001 Transformation of an oral bacterium via chromosomal integration of free DNA in the presence of human saliva. FEMS Microbiol. Lett. 200, 163–167.

    CAS  PubMed  Google Scholar 

  • Miura-Masuda A and Ikeda H 1990 The DNA gyrase of Escherichia coli participates in the formation of a spontaneous deletion by recA-independent recombination in vivo. Mol. Gen. Genet. 220, 345–352.

    Article  CAS  PubMed  Google Scholar 

  • Nap J P, Bijvoet J and Stiekema W J 1992 Biosafety of kanamycin-resistant transgenic plants. Transgenic Res. 1, 239–249.

    CAS  PubMed  Google Scholar 

  • Nielsen K M, Bones A M, Smalla K and van Elsas J D 1998 Horizontal gene transfer from transgenic plants to terrestrial bacteria- A rare event? FEMS Microbiol. Rev. 22, 79–103.

    CAS  PubMed  Google Scholar 

  • Nielsen K M, Gebhard F, Smalla K, Bones A M and van Elsas J D 1997a Evaluation of possible horizontal gene transfer from transgenic plants to the soil bacterium Acinetobacter. Theor. Appl. Genet. 95, 815–821.

    Article  CAS  Google Scholar 

  • Nielsen K M, van Weerelt M D M, Berg T N, Bones A M, Hagler A N and van Elsas J D 1997b Natural transformation and availability of transforming DNA to Acinetobacter calcoaceticus in soil microcosms. Appl. Environ. Microbiol. 63, 1945–1952.

    CAS  PubMed  Google Scholar 

  • Normark B H and Normark S 2002 Evolution and spread of antibiotic resistance. J. Intern. Med. 252, 91–106.

    Article  CAS  PubMed  Google Scholar 

  • Nwosu V C 2001 Antibiotic resistance with particular reference to soil microorganisms. Res. Microbiol. 152, 421–430.

    Article  CAS  PubMed  Google Scholar 

  • Ochman H, Lawrence J G and Groisman E A 2000 Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304.

    Article  CAS  PubMed  Google Scholar 

  • Odell J T, Nagy F and Chua N H 1985 Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313, 810–812.

    Article  CAS  PubMed  Google Scholar 

  • Paget E, Simonet L J and Monrozier P 1992 Adsorption of DNA on clay minerals: Protection against DNaseI and influence on gene transfer. FEMS Microbiol. Lett. 97, 31–40.

    Article  CAS  Google Scholar 

  • Paget E, Lebrun M, Freyssinet G and Simonet P 1998 The fate of recombinant plant DNA in soil. Eur. J. Soil Biol. 34, 81–88.

    Article  CAS  Google Scholar 

  • Palmen R and Hellingwerf K J 1997 Uptake and processing of DNA by Acinetobacter calcoaceticus - A review. Gene 192, 179–190.

    Article  CAS  PubMed  Google Scholar 

  • Prudhomme M, Libante V and Claverys J P 2002 Homologous recombination at the border: Insertion-deletions and the trapping of foreign DNA in Streptococcus pneumoniae. Proc. Natl. Acad. Sci USA 99, 2100–2105.

    Article  CAS  PubMed  Google Scholar 

  • Redfield R J 2001 Do bacteria have sex? Nat. Rev. Genet. 2, 634–639. Roberts M S and Cohan F M 1993 The effect of DNA sequence divergence on sexual isolation in Bacillus. Genetics 134, 401–408.

    Article  CAS  PubMed  Google Scholar 

  • Romanowski G, Lorenz M G, Sayler G and Wackernagel W 1992 Persistence of free plasmid DNA in soil monitored by various methods, including a transformation assay. Appl. Environ. Microbiol. 58, 3012–3019.

    CAS  PubMed  Google Scholar 

  • Romanowski G, Lorenz M G and Wackernagel W 1993a Use of polymerase chain reaction and electroporation of Escherichia coli to monitor the persistence of extracellular plasmid DNA introduced into natural soils. Appl. Environ. Microbiol. 59, 3438–3446.

    CAS  PubMed  Google Scholar 

  • Romanowski G, Lorenz M G and Wackernagel W 1993b Plasmid DNA in a groundwater aquifer microcosm: adsorption, DNase resistance and natural genetic transformation of Bacillus subtilis. Mol. Ecol. 2, 171–181.

    CAS  PubMed  Google Scholar 

  • Schlimme W, Marchiani M, Hanselmann K and Jenni B 1997 Gene transfer between bacteria within digestive vacuoles of protozoa. FEMS Microbiol. Ecol. 23, 239–247.

    CAS  Google Scholar 

  • Schlüter K, Fütterer J and Potrykus I 1995 ‘Horizontal’ gene transfer from a transgenic potato line to a bacterial pathogen (Erwinia chrysanthemi) occurs - if at all - at an extremely low frequency. BioTechnology 13, 1094–1098.

    PubMed  Google Scholar 

  • Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler D R and Dean D H 1998 Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62, 775–806.

    CAS  PubMed  Google Scholar 

  • Sikorski J, Graupner S, Lorenz M G and Wackernagel W 1998 Natural genetic transformation of Pseudomonas stutzeri in a nonsterile soil. Microbiology 144, 569–576.

    CAS  PubMed  Google Scholar 

  • Sikorski J, Teschner N and Wackernagel W 2002 Highly different levels of natural transformation are associated with genomic subgroups within a local population of Pseudomonas stutzeri from soil. Appl. Environ. Microbiol. 68, 865–873.

    Article  CAS  PubMed  Google Scholar 

  • Stone B J and Kwaik Y A 1999 Natural competence for DNA transformation by Legionella pneumophila and its association with expression of type IV pili. J. Bacteriol. 181, 1395–1402.

    CAS  PubMed  Google Scholar 

  • Stotzky G, Devanas M A and Zeph L R 1990 Methods for studying bacterial gene transfer in soil by conjugation and transduction. Adv. Appl. Microbiol. 35, 57–169.

    CAS  PubMed  Google Scholar 

  • Stuy J H 1976 Restriction enzymes do not play a significant role in Haemophilus homospecific or heterospecific transformation. J. Bacteriol. 128, 212–220.

    CAS  PubMed  Google Scholar 

  • Thompson C J, Movva N R, Tizard R, Crameri R, Davies J E, Lauwereys M and Bottermann J 1987 Characterization of the herbicide-resistance gene bar from Streptomyces hygroscopicus. EMBO J. 6, 2519–2523.

    CAS  PubMed  Google Scholar 

  • Tønjum T, Bøvre K and Juni E 1995 Fastidious Gram-negative bacteria: Meeting the diagnostic challenge with nucleic acid analysis. APMIS 103, 609–627.

    PubMed  Google Scholar 

  • Wang Y, Goodman S D, Redfield R J and Chen C 2002 Natural transformation and DNA uptake signal sequences in Actinobacillus actinomycetemcomitans. J. Bacteriol. 184, 3442–3449.

    CAS  PubMed  Google Scholar 

  • Ween O, Teigen S, Gaustad P, Kilian M and Havarstein L S 2002 Competence without a competence pheromone in a natural isolate of Streptococcus infantis. J. Bacteriol. 184, 3426–3432.

    Article  CAS  PubMed  Google Scholar 

  • Widmer F, Seidler R J and Watrud L S 1996 Sensitive detection of transgenic plant marker gene persistence in soil microcosms. Mol. Ecol. 5, 603–613.

    CAS  Google Scholar 

  • Widmer F, Seidler R J, Donegan K K and Reed G L 1997 Quantification of transgenic plant marker gene persistence in the field. Mol. Ecol. 6, 1–7.

    Article  CAS  Google Scholar 

  • Williamson M 1992 Environmental risks from the release of genetically modified microorganisms (GMOs) - the need for molecular ecology. Mol. Ecol. 1, 3–8.

    Google Scholar 

  • Worth L Jr., Clark S, Radman M and Modrich P 1994 Mismatch repair proteins MutS and MutL inhibit RecA-catalyzed strand transfer between diverged DNAs. Proc. Natl. Acad. Sci. USA 91, 3238–3241.

    CAS  PubMed  Google Scholar 

  • Zalacain M, Gonzales A, Guererro M C, Mattaliano R J, Malpartida F and Jimenez A 1986 Nucleotide sequence of the hygromycin B phosphotransferase gene from Streptomyces hygroscopicus. Nucleic Acids Res. 14, 1565–1581.

    CAS  PubMed  Google Scholar 

  • Zawadski P, Roberts M S and Cohan F M 1995 The log-linear relationship between sexual isolation and sequence divergence in Bacillus transformation is robust. Genetics 140, 917–932.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wilfried Wackernagel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Vries, J., Wackernagel, W. Microbial horizontal gene transfer and the DNA release from transgenic crop plants. Plant Soil 266, 91–104 (2005). https://doi.org/10.1007/s11104-005-4783-x

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-005-4783-x

Key words

Navigation