Visual evidence of horizontal gene transfer between plants and bacteria in the phytosphere of transplastomic tobacco.

Alessandra Pontiroli, Aurora Rizzi, Pascal Simonet, Daniele Daffonchio, Timothy M Vogel, Jean-Michel Monier
Author Information
  1. Alessandra Pontiroli: Environmental Microbial Genomics Group, Laboratoire Ampère, Ecole Centrale de Lyon, Université de Lyon, Ecully, France.

Abstract

Plant surfaces, colonized by numerous and diverse bacterial species, are often considered hot spots for horizontal gene transfer (HGT) between plants and bacteria. Plant DNA released during the degradation of plant tissues can persist and remain biologically active for significant periods of time, suggesting that soil or plant-associated bacteria could be in direct contact with plant DNA. In addition, nutrients released during the decaying process may provide a copiotrophic environment conducive for opportunistic microbial growth. Using Acinetobacter baylyi strain BD413 and transplastomic tobacco plants harboring the aadA gene as models, the objective of this study was to determine whether specific niches could be shown to foster bacterial growth on intact or decaying plant tissues, to develop a competence state, and to possibly acquire exogenous plant DNA by natural transformation. Visualization of HGT in situ was performed using A. baylyi strain BD413(rbcL-DeltaPaadA::gfp) carrying a promoterless aadA::gfp fusion. Both antibiotic resistance and green fluorescence phenotypes were restored in recombinant bacterial cells after homologous recombination with transgenic plant DNA. Opportunistic growth occurred on decaying plant tissues, and a significant proportion of the bacteria developed a competence state. Quantification of transformants clearly supported the idea that the phytosphere constitutes a hot spot for HGT between plants and bacteria. The nondisruptive approach used to visualize transformants in situ provides new insights into environmental factors influencing HGT for plant tissues.

References

  1. Environ Int. 2005 May;31(4):575-84 [PMID: 15788197]
  2. FEMS Microbiol Ecol. 2000 Jan 1;31(1):39-45 [PMID: 10620717]
  3. Environ Biosafety Res. 2007 Jan-Jun;6(1-2):37-53 [PMID: 17961479]
  4. New Phytol. 2003 Mar;157(3):525-537 [PMID: 33873398]
  5. Environ Biosafety Res. 2008 Jul-Sep;7(3):123-49 [PMID: 18801324]
  6. Appl Environ Microbiol. 1998 May;64(5):1902-9 [PMID: 9572970]
  7. Nat Biotechnol. 2004 Sep;22(9):1110-4 [PMID: 15340481]
  8. J Appl Microbiol. 2000 Sep;89(3):423-32 [PMID: 11021574]
  9. Nat Rev Microbiol. 2005 Sep;3(9):700-10 [PMID: 16138098]
  10. FEMS Microbiol Rev. 1998 Jun;22(2):79-103 [PMID: 9729765]
  11. FEMS Microbiol Ecol. 2008 May;64(2):153-66 [PMID: 18355294]
  12. J Gen Microbiol. 1993 Feb;139(2):295-305 [PMID: 8436948]
  13. Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15977-82 [PMID: 14665692]
  14. Res Microbiol. 1999 Jul-Aug;150(6):375-84 [PMID: 10466405]
  15. Appl Environ Microbiol. 2000 Jan;66(1):369-74 [PMID: 10618250]
  16. Appl Environ Microbiol. 2002 Jul;68(7):3345-51 [PMID: 12089013]
  17. Appl Environ Microbiol. 2004 Jan;70(1):346-55 [PMID: 14711662]
  18. Microb Ecol. 2002 Apr;43(3):291-7 [PMID: 12037607]
  19. Microbiol Mol Biol Rev. 2000 Sep;64(3):624-53 [PMID: 10974129]
  20. Environ Biosafety Res. 2007 Jan-Jun;6(1-2):15-35 [PMID: 17961478]
  21. Appl Environ Microbiol. 2008 Feb;74(4):1250-4 [PMID: 18165369]
  22. Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3446-53 [PMID: 11248098]
  23. FEMS Microbiol Ecol. 2002 Nov 1;42(2):187-97 [PMID: 19709278]
  24. Curr Microbiol. 2003 Aug;47(2):129-33 [PMID: 14506860]
  25. Appl Environ Microbiol. 2003 Apr;69(4):1875-83 [PMID: 12676659]
  26. Annu Rev Phytopathol. 2003;41:429-53 [PMID: 12730399]
  27. Appl Environ Microbiol. 1994 Feb;60(2):496-500 [PMID: 8135513]
  28. Antonie Van Leeuwenhoek. 1998 Jan;73(1):69-77 [PMID: 9602280]
  29. Appl Environ Microbiol. 2003 Jan;69(1):673-8 [PMID: 12514059]
  30. Appl Environ Microbiol. 2004 May;70(5):2709-16 [PMID: 15128522]
  31. FEMS Microbiol Ecol. 2001 Mar;35(1):75-84 [PMID: 11248392]
  32. Curr Opin Biotechnol. 2003 Jun;14(3):255-61 [PMID: 12849777]
  33. Methods Enzymol. 2005;395:491-520 [PMID: 15865981]
  34. Annu Rev Phytopathol. 2000 Sep;38:145-180 [PMID: 11701840]

MeSH Term

Acinetobacter
Artificial Gene Fusion
DNA, Plant
Gene Transfer, Horizontal
Genes, Reporter
Green Fluorescent Proteins
Plants, Genetically Modified
Recombination, Genetic
Nicotiana

Chemicals

DNA, Plant
Green Fluorescent Proteins

Word Cloud

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