Skip to main content
SpringerLink
Log in

Biolistic transformation of arbuscular mycorrhizal fungi

Progress and perspectives

  • Review
  • Published:
Molecular Biotechnology Aims and scope Submit manuscript

Abstract

Gene transfer systems have proved effective for the transformation of a range of organisms for both fundamental and applied studies. Biolistic transformation is a powerful method for the gene transfer into various organisms and tissues that have proved recalcitrant to more conventional means. For fungi, the biolistic approach is particularly effective where protoplasts are difficult to obtain and/or the organisms are difficult to culture. This is particularly applicable to arbuscular mycorrhizal (AM) fungi, being as they are obligate symbionts that can only be propagated in association with intact plants or root explants. Furthermore, these fungi are aseptate and protoplasts cannot be released. Recent advancements in gene transformation systems have enabled the use of biolistic technology to introduce foreign DNA linked to molecular markers into these fungi. In this review we discuss the development of transformation strategies for AM fungi by biolistics and highlight the areas of this technology which require further development for the stable transformation of these elusive organisms.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Smith, S. E. and Read, D. J. (1997) Mycorrhizal Symbiosis. Second Edition, Academic Press.

  2. Pirozynski, K. A. and Malloch, D. W. (1975) The origin of land plants: A matter of mycotrophism. Biosystems 6, 153–164.

    Article  PubMed  CAS  Google Scholar 

  3. Pirozynski, K. A. and Dalpe, Y. (1989) Geological history of the Glomaceae with particular reference to mycorrhizal symbiosis. Symbiosis 7, 1–36.

    Google Scholar 

  4. Redecker, D., Kodner, R., and Graham, L. E. (2000) Glomalean fungi from the ordovacian. Science 289, 1920,1921.

    Article  PubMed  CAS  Google Scholar 

  5. Remy, W., Taylor, T. N., Hass, H. et al. (1994) Four hundred million year old vesicular arbuscular mycorrhizae. Proc. Natl. Acad. Sci. USA 91, 11,841–11,843.

    Article  CAS  Google Scholar 

  6. Simon, L., Bousquet, J., Levesque, R. C., et al. (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular plants. Nature 363, 67–69.

    Article  Google Scholar 

  7. Taylor, T. N., Remy, W., Hass, H., et al. (1995) Fossil arbuscular mycorrhizae from the early Devonian. Mycologia 87, 560–573.

    Article  Google Scholar 

  8. Hooker, J. E., Jaizme-Vega, M., and Atkinson, D. (1994). Biocontrol of plant pathogens using arbuscular mycorrhizal fungi, in Impact of Arbuscular Mycorrhizal Fungi on Sustainable Agriculture and Natural Ecosystems (Gianinazzi, S. and Schuepp, H., eds.), Birkhauser-Verlag, Switzerland, pp. 191–200.

    Google Scholar 

  9. Marschner, H. and Dell, B. (1994) Nutrient uptake in mycorrhizal symbiosis. Plant & Soil 159, 89–102.

    CAS  Google Scholar 

  10. Newsham, K. K., Fitter A. H., and Watterson, A. R. (1995) Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J. Ecol. 83, 991–1000.

    Article  Google Scholar 

  11. Ricken, B. and Hofner, W. (1996) Effect of arbuscular mycorrhizal fungi (AMF) on heavy-metal tolerance of Alfafa (Medicago sativa L.) and oat (Avena sativa L.) on a sewage sludge treated soil. Zeit. Planzen. Boken. 159, 189–194.

    CAS  Google Scholar 

  12. Subramanian, K. S., Charest, C., Dwyer, L. M., et al. (1995) Arbuscular mycorrhizas and water relations in Maize under drought stress at Tasseling. New Phytol. 129, 643–650.

    Article  Google Scholar 

  13. Vonreichenbach, H. G. and Schonbeck, F. (1995) Influence of VA-mycorrhiza on drought tolerance of flax (Linum usitatissimum L.). 2. Effect of VA-mycorrhiza on stomatal gas exchange, shoot water potential, phosphorous-nutrition and the accumulation of stress metabolites. J. Appl. Bot. 69, 183–188.

    CAS  Google Scholar 

  14. Bethlenfalvay, G. J. and Schuepp, H. (1994) Arbuscular mycorrhizas and agrosystem stability, in Impact of Arbuscular Mycorrhizas on Sustainable Agriculture and Natural Ecosystems (Gianinazzi, S. and Schuepp, H., eds.), Birkhauser Verlag, Basel, Switzerland, pp. 117–131.

    Google Scholar 

  15. Burleigh, S. H. and Harrison, M. J. (1998) A cDNA from the arbuscular mycorrhizal fungus Glomus versiforme with homology to a cruciform DNA binding protein from Ustilago maydis. Mycorrhiza 7, 301–306.

    Article  CAS  Google Scholar 

  16. Butehorn, B., Gianinazzi-Pearson, V., and Franken, P. (1999) Quantification of beta-tubulin RNA expression during asymbiotic and symbiotic development of the arbuscular mycorrhizal fungus Glomus mosseae. Mycol. Res. 103, 360–364.

    Article  CAS  Google Scholar 

  17. Delp, G., Smith, S. E., and Barker, S. J. (2000) Isolation by differential display of three partial cDNAs potentially coding for proteins from the VA mycorrhizal Glomus intraradices. Mycol. Res. 104, 293–300.

    Article  CAS  Google Scholar 

  18. Ferrol, N., Miguel-Barea, J., and Azcon-Aguilar, C. (2000) The plasma membrane H+-ATPase gene family in the arbuscular mycorrhizal fungus Glomus mosseae. Curr. Gen. 37, 112–118.

    Article  CAS  Google Scholar 

  19. Franken, P., Lapopin, L., Meyer-Gauen, G., et al. (1997) RNA accumulation and genes expressed in spores of the mycorrhizal fungus Gigasporsa rosea. Mycologia 89, 293–297.

    Article  CAS  Google Scholar 

  20. Harrier, L. A., Wright, F., and Hooker, J. E. (1998) Isolation of the 3-phosphoglycerate kinase gene from the arbuscular mycorrhizal fungus Glomus mosseae Nicol. & Gerd. Gerdemann & Trappe. Curr. Gen. 34, 386–392.

    Article  CAS  Google Scholar 

  21. Harrison, M. J. and Van Buuren, M. L. (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378, 626–629.

    Article  PubMed  CAS  Google Scholar 

  22. Kaldorf, M., Schmelzer, E., and Bothe, H. (1998) Expression of maize and fungal nitrate reductase genes in arbuscular mycorrhiza. M. P. M. I. 11, 439–448.

    CAS  Google Scholar 

  23. Kaldorf, M., Zimmer, W., and Bothe, H. (1994) Genetic evidence for the occurrence of assimilatory nitrate reductase in arbuscular mycorrhizal and other fungi. Mycorrhiza 5, 23–28.

    Article  CAS  Google Scholar 

  24. Lanfranco, L., Garnero, L., and Bonfante, P. (1999) Chitin synthase genes in the arbuscular mycorrhizal fungus Glomus versiforme: full sequence of a gene encoding a class IV chitin synthase. FEMS Micro. Lett. 170, 59–67.

    Article  CAS  Google Scholar 

  25. Lanfranco, L., Vallino, M., and Bonfante, P. (1999) Expression of chitin synthase genes in the arbuscular mycorrhizal fungus Gigaspora margarita. New Phytol. 142, 347–354.

    Article  CAS  Google Scholar 

  26. Requena, N., Fuller, P., and Franken, P. (1999) Molecular characterisation of GmFOX2 an evolutionary highly conserved gene from the mycorrhizal fungus Glomus mosseae, down-regulated during the interaction with rhizobacteria. M. P. M. I. 12, 934–942.

    CAS  Google Scholar 

  27. Carpecchi, M. R. (1980) High efficiency transformation by direct microinjection of DNA into cultured mammalian cells. Cell 22, 479–488.

    Article  Google Scholar 

  28. Fernandez, S. M., Lurquin, P. F., and Kado, C. I. (1978) Incorporation and maintenance of recombinant-DNA plasmid vehicles pBR313 and pCR1 in plant protoplasts. Fed. Europ. Biochem. Soc. Lett. 87, 277–282.

    CAS  Google Scholar 

  29. Gordon, J. W., Scangos, G. A., Platkin, D. J., et al. (1980) Genetic transformation of mouse embryos by microinjection of purified DNA. Proc. Natl. Acad. Sci. USA. 77, 7380–7384.

    Article  PubMed  CAS  Google Scholar 

  30. Marton, L., Wullems, G. J., Molendyk, L., et al. (1979) In vitro transformation of cultured cells from Nicotiana tabacum by Agrobacterium tumefaciens. Nature 277, 129–131.

    Article  Google Scholar 

  31. Schaffner, W. (1980) Direct transfer of cloned genes from bacteria to mammalian cells. Proc. Natl. Acad. Sci. USA 77, 2163–2167.

    Article  PubMed  CAS  Google Scholar 

  32. Sanford, J. C. (1988) The biolistic process. Trends Biotechnol. 6, 299–302.

    Article  CAS  Google Scholar 

  33. Sanford, J. C. (1990) Biolistic transformation—a critical assessment. Physiol. Plant. 79, 206–209.

    Article  CAS  Google Scholar 

  34. Sanford, J. C. (1990) The biolistic process—an emerging tool for research and clinical applications, in Proceedings of the Biomedical Society (Milukeck, D. C. and Clarke, A. M., eds.). Virginia Polytechnic Institute. Blacksburg, VA. NY. New York University Press, NY, pp. 89–98.

    Google Scholar 

  35. Sanford, J. C., Devit, M. J., Russel, J. A., et al. (1991) An improved Helium driven biolistic device. Technique 3, 3–16.

    CAS  Google Scholar 

  36. Sanford, J. C., Klein, T. M., Wolf, E. D., et al. (1987) Delivery of substances into cells and tissues using a particle bombardment process. J. Part. Sci. Tech. 5, 27–37.

    Article  CAS  Google Scholar 

  37. Sanford, J. C., Smith, F. D., and Russel, J. A. (1993) Optimizing the biolistic process for different biological applications. Meth. Enzymo. 217, 483–509

    CAS  Google Scholar 

  38. Becker, D. K., Dugdale, B., Smith, M. K., et al. (2000) Genetic transformation of cavendish banana (Musa spp. AAA group) cv “Grand nain” via microprojectile bombardment. Plant Cell Rep. 19, 229–234.

    Article  CAS  Google Scholar 

  39. Fernando, D. D., Owens, J. N., and Misra, S. (2000) Transient gene expression in pine pollen tubes following particle bombardment. Plant Cell Rep. 12, 224–228.

    Article  Google Scholar 

  40. Fukuoka, H., Ogawa, T., Matsuoka, M., et al. (1998) Direct gene delivery into isolated microspores of rapeseed (Brassica napus L.) and production of fertile transgenic plants. Plant Cell Rep. 17, 323–328.

    Article  CAS  Google Scholar 

  41. Klein, T. M., Harper, E. C., Svab, Z., et al. (1988) Stable genetic transformation of intact Nicotiana cells by the particle bombardment process. Proc. Natl. Acad. Sci. USA 85, 8502–8505.

    Article  PubMed  CAS  Google Scholar 

  42. Maenpaa, P., Gonzalez, E. B., Ahlandsberg, S., et al. (1999) Transformation of nuclear and plastonic plant genomes by biolistic particle bombardment. Mol. Biotech. 13, 67–72.

    Article  CAS  Google Scholar 

  43. Rasco-Gaunt, S., Riley, A., Barcelo, P., et al. (1999) Analysis of particle bombardment parameters to optimise DNA delivery into wheat tissues. Plant Cell Rep. 19, 118–127.

    Article  CAS  Google Scholar 

  44. Tang, K., Tinjuangjun, P., Xu, Y., et al. (1999) Particle bombardment mediated cotransformation of elite chinese rice cultivars with genes conferring resistance to bacterial blight and sap sucking insect pests. Planta 208, 552–563.

    Article  CAS  Google Scholar 

  45. Johnston, S. A. (1990) Biolistic transformation: Microbes to mice. Nature 346, 776,777.

    Article  PubMed  CAS  Google Scholar 

  46. Mayfield, S. P. and Kindle, K. L. (1990) Stable nuclear transformation of Chlamydomonas reinhardtii by using a C. reinhardtii gene as the selectable marker. Proc. Natl. Acad. Sci. USA 87, 2087–2091.

    Article  PubMed  CAS  Google Scholar 

  47. Shark, K. B., Smith, F. D., Harpending, P. R., et al. (1991) Biolistic transformation of a procaryote, Bacillus megaterium. Appl. Environ. Micro. 57, 480–485.

    CAS  Google Scholar 

  48. Bills, S. N., Richter, D. L., and Podila, G. K. (1995) Genetic transformation of the ectomycorrhizal fungus Paxillus involutus by particle bombardment, Mycol. Res. 99, 557–561.

    Google Scholar 

  49. Durand, R., Rascle, C., Fischer, M., et al. (1997) Transient expression of the β-glucuronidase gene after biolistic transformation of the anerobic fungus Neocallimastix frontalis. Curr. Gen. 31, 158–161.

    Article  CAS  Google Scholar 

  50. Fungaro, M. H., Rech, E., Muhlen, G. S., et al. (1995) Transformation of Aspergillus nidulans by microprojectile bombardment on intact conidia. FEMS Micro. Lett. 125, 193–298.

    Article  Google Scholar 

  51. St. Leger, R. J., Shimizu, S., Joshi, L., et al. (1995) Co-transformation of Metarrhizium anisopliae by electroporation or using the gene gun to produce stable GUS transformants. FEMS Micro. Lett. 131, 289–294.

    Article  CAS  Google Scholar 

  52. Kikkert, J. R. (1993) The Biolistic® PDS-1000/He device. Plant, Cell, Tiss. Org. Cult. 33, 221–226.

    Article  CAS  Google Scholar 

  53. Kikkert, J. R., Humiston, G. A., Roy, M. K., et al. (1999) Biological projectiles (Phage, yeast, bacteria) for genetic transformation of plants. In Vitro Cell. Dev. Biol.-Plant 35, 43–50.

    Article  CAS  Google Scholar 

  54. Rasmussen, J. L., Kikert, J. R., Roy, M. K., et al. (1994) Biolistic transformation of tobacco and maize suspension cells using bacterial cells as microprojectiles. Plant Cell Rep. 13, 212–217.

    Article  CAS  Google Scholar 

  55. Forbes, P. J., Millam, S., Hooker, J. E., et al. (1998) Transformation of the arbuscular mycorrhizal fungus Gigaspora rosea Nicolson & Schenck using particle bombardment. Mycol. Res. 102, 497–501.

    Article  Google Scholar 

  56. Bianciotto, V., Bandi, C., Minerdi, D., et al. (1996) An obligately endosymbiotic mycorrhizal fungus itself harbours obligately intracellular bacteria. Appl. Environ. Micro. 62, 3005–3010.

    CAS  Google Scholar 

  57. Wilson, K. J., Jefferson, R. A., and Hughes, S. G. (1992) The Escherichia coli gus operon: Induction and expression of the gus operon in E. coli and the occurrence and use of GUS in other bacteria, in, GUS Protocols: Using the GUS Gene as a Reporter of Gene Expression (Gallagher, S. R., ed.), Academic Press, CA, pp. 7–22.

    Google Scholar 

  58. Blowers, A. D., Bogorod, L., Shark, K. B., et al. (1989) Studies on Chlamydomonas chloroplast transformation-Foreign DNA can be stably maintained in the chromosome. Plant Cell 1, 123–132.

    Article  PubMed  CAS  Google Scholar 

  59. Klein, T. M., Wolf, E. D., Wu, R., et al. (1987) High-velocity microprojectiles for delivering nucleic acids into living cells. Nature 327, 70–73.

    Article  CAS  Google Scholar 

  60. Jones, E., Carpenter, M., Fong, D., et al. (1999) Transformation of the sclerotial mycoparasite Coniothyrium minitans with hygromycin B resistance and beta-glucuronidase markers. Mycol. Res. 103, 929–938.

    Article  CAS  Google Scholar 

  61. Roberts, I. N., Oliver, R. P., Punt, P. J., et al. (1989) Expression of the Escherichia coli β-glucuronidase gene in industrial and phytopathogenic filamentous fungi. Curr. Gen. 15, 177–180.

    Article  CAS  Google Scholar 

  62. Grace, C. and Stribley, D. P. (1991) A safer procedure for root staining of vesicular arbuscular mycorrhizal fungi. Mycol. Res. 95, 1160–1162.

    Article  Google Scholar 

  63. Forbes, P., Millam, S., Harrier, L., et al. (1998) Transformation of the arbuscular mycorrhizal fungus Gigaspora rosea Nicolson & Schenck by particle bombardment, in Proceedings of the Second International Conference on Mycorrhiza, July 5–10, SLU Service/Repro, Uppsala, pp. 63,64.

  64. Hosny, M., Païs de Barros, J., Gianinazzi-Pearson, V., et al. (1997) Base composition of DNA from Glomalean Fungi: high amounts of methylated cytosine. Fun. Gen. Biol. 22, 103–111.

    Article  CAS  Google Scholar 

  65. Hargreaves, J. and Turner, G. (1992) Gene transformation in plant pathogenic fungi, in Molecular Plant Pathology (Gurr, S.J., McPherson, M.J., and Bowles, D.J., eds.) Oxford University Press, pp. 79–97.

  66. Judelson, H. S., Tyler, B. M., and Micelmore, R. W. (1992) Regulatory sequences for expressing genes in oomycete fungi. Mol. Gen. Genet. 234, 138–146.

    PubMed  CAS  Google Scholar 

  67. Fischer, M., Durand, R., and Fevre M. (1995) Characterisation of the promoter region of the enolase encoding gene ENOL from the anaerobic fungus Neocallimastix frontalis. Sequence and Promoter analysis. Curr. Gen. 28, 80–86.

    Article  CAS  Google Scholar 

  68. Harrier, L. A. (2001) Isolation and sequence analysis of the arbuscular mycorrhizal fungus Glomus mosseae (Nicol. & Gerd.) Gerdemann & Trappe 3-phosphoglycerale kinase (PGK) gene promoter region. DNA Seq., in press.

  69. Laufs, J., Wirtz, U., Kammann, M., et al. (1990) Wheat dwarf virus AC/DS vectors-expression and excision of transposable elements introduced into various cereals by a viral replicon. Proc. Natl. Acad. Sci. USA 87, 7752–7756.

    Article  PubMed  CAS  Google Scholar 

  70. Zeze, A., Hosny, M., Gianinazzi-Pearson, V., et al. (1996) Characterisation of a highly repeated DNA sequence (SC1) from the arbuscular mycorrhizal fungus Scutellospora castanea and its detection in planta. Appl. Environ. Micro. 62, 2443–2448.

    CAS  Google Scholar 

  71. Zeze, A., Hosny, M., Tuinen, D., et al. (1999) MYC-DIRE, a dispersed repetitive DNA element in arbuscular mycorrhizal fungi. Mycol. Res. 103, 572–576.

    Article  CAS  Google Scholar 

  72. Ruiz-Diez, B. and Martinez-Suarez, J. V. (1999) Electrotransformation of the human pathogenic fungus Scedosporium prolificans mediated by repetitive rDNA sequences. FEMS Immuno. Med. Micro. 25, 275–282.

    Article  CAS  Google Scholar 

  73. Kaya, S., Imai, T., and Ishige, M. (1990) The efficiency of transformation by Agrobacterium tumefaciens without selection marker. Jpn. J. Breed. 40, 82,83.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Plant and Crop Science Division, Scottish Agricultural College, West Mains Road, Edinburgh, West Lothian, Scotland, UK

    Lucy A. Harrier

Authors
  1. Lucy A. Harrier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Steve Millam
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lucy A. Harrier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harrier, L.A., Millam, S. Biolistic transformation of arbuscular mycorrhizal fungi. Mol Biotechnol 18, 25–33 (2001). https://doi.org/10.1385/MB:18:1:25

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1385/MB:18:1:25

Index Entries

Search

Navigation