The apoplast of ectomycorrhizal roots – site of nutrient uptake and nutrient exchange between the symbiotic partners

  • H. BÜcking
  • R. Hans
  • W. Heyser

Abstract

Between 80 and 90% of all known plant species live in close interaction with mycorrhizal fungi in a mutalistic interaction, the mycorrhizal symbiosis. Mycorrhizal root tips with their extramatrical mycelium increase the absorbing surface area of mycorrhizal roots and contribute significantly to the nutrient uptake of plants. The following paper deals with the role of the apoplast for nutrient uptake and nutrient exchange between both partners. Investigations by use of fluorescent dyes as apoplastic tracers showed that the fungal sheath of the ectomycorrhizal roots does not act as an effective apoplastic barrier for the entry of nutrients into the mycorrhizal root cortex. However, nutrients such as P can be absorbed by hyphae of the extramatrical mycelium or the fungal sheath and the transfer to the host plant is controlled by the fungal symplast. The results indicate that the uptake of P by the extramatrical mycelium and the transfer across the interfacial apoplast to the mycorrhizal host plant is not primarily regulated by the host plant demand for P, but by the flux of carbohydrates from the mycorrhizal host plant to the fungal symbiont. A model system shows how the carbohydrate and P exchange between both symbiotic partners is possibly linked.

Key words

apoplast ectomycorrhiza interface nutrient exchange P transport 

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References

  1. Ashford, A. E., Allaway, W. G., Peterson, C. A. and Cairney, J. W. G. (1989). Nutrient transfer and the fungus-root interface. Aust. J. Plant Physiol., 16, 85–97.CrossRefGoogle Scholar
  2. Behrmann, P. (1995). Entwicklung, Struktur und Funktion der Endodermis in mykorrhizierten und nicht-mykorrhizierten Baumwurzeln unter besonderer Berücksichtigung der Kiefer (Pinus sylvestris L.). Ph.D. thesis, University of Bremen, Germany.Google Scholar
  3. Bücking, H. and Heyser, W. (1994). The effect of ectomycorrhizal fungi on Zn uptake and distribution in seedlings of Pinus sylvestris L. Plant Soil, 167, 203–212.CrossRefGoogle Scholar
  4. Bücking, H. and Heyser, W. (2000). Subcellular compartmentation of elements in non-mycorrhizal and mycorrhizal roots of Pinus sylvestris: an X-ray microanalytical study. I. The distribution of phosphate. New Phytol., 145, 311–320.CrossRefGoogle Scholar
  5. Bücking, H. and Heyser, W. (2001). Microautoradiographic localization of phosphate and carbohydrates in mycorrhizal roots of Populus tremula x Populus alba and the implications for transfer processes in ectomycorrhizal associations. Tree Physiol., 21, 101–107.PubMedGoogle Scholar
  6. Bücking, H. and Heyser, W. (2003). Uptake and transfer of nutrients in ectomycorhizal associations: interactions between photosynthesis and phosphate nutrition. Mycorrhiza, 13, 59–68.PubMedCrossRefGoogle Scholar
  7. Bücking, H., Warner, J., Hespe, C. and Heyser, W. (2001).Google Scholar
  8. Autoradiographische und cytochemische Untersuchungen zum Assimilattransfer in der ektotrophen Mykorrhiza. In R. Langenfeld-Heyser, A. Polle and E. Fritz (eds), Schriften aus der Forstlichen Fakultät der Universität Göttingen und der Niedersächsischen Forstlichen Versuchsanstalt. Band 131: Neues zum Stofftransport in Bäumen. J. D. Sauerländer’s Verlag. Frankfurt am Main, pp. 108–120.Google Scholar
  9. Bücking, H. and Shachar-Hill, Y. (2005). Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimulated by increased carbohydrate availability. New Phytol., 165, 899–912.PubMedCrossRefGoogle Scholar
  10. Bücking, H., Kuhn, A. J., Schröder, W. H. and Heyser, W. (2002). The fungal sheath of ectomycorrhizal pine roots: an apoplastic barrier for the entry of calcium, magnesium and potassium into the root cortex? J. Exp. Bot., 53, 1659–1669.PubMedCrossRefGoogle Scholar
  11. Cairney, J. W. G. and Smith, S. E. (1992). Influence of intracellular phosphorus concentration on phosphate absorption by the ectomycorrhizal basidiomycete Pisolithus tinctorius. Mycol. Res., 96, 673–676.CrossRefGoogle Scholar
  12. Chalot, M., Javelle, A., Blaudez, D., Lambilliote, R., Cooke, R., Sentenac, H., Wipf, D. and Botton, B. (2002). An update on nutrient transport processes in ectomycorrhizas. Plant Soil, 244, 165–175.CrossRefGoogle Scholar
  13. Duddridge, J. A. and Read, D. J. (1984). The development and ultrastructure of ectomycorrhizas. II. Ectomycorrhizal development on pine in vitro. New Phytol., 96, 575–582.CrossRefGoogle Scholar
  14. Finlay, R. and Söderström, B. (1992). Mycorrhiza and carbon flow to the soil. In M. J. Allen (ed.), Mycorrhizal Functioning. Chapman and Hall, New York, pp. 134–160.Google Scholar
  15. Harley, J. L. and Smith, S. E. (1983). Mycorrhizal symbiosis. Academic Press, London.Google Scholar
  16. Harold, F. M. (1994). Ionic and electrical dimensions of hyphal growth. In J. G. H. Wessels and F. Meinhardt (eds), The Mycota I. Growth, Differentiation and Sexuality. Springer-Verlag, Berlin. pp. 89–109.Google Scholar
  17. Häussling, M., Jorns, C. A., Lehmbecker, G., Hecht-Buchholz, C. and Marschner, H. (1988). Ion 0and water uptake in relation to root development in norway spruce (Picea abies (L.) Karst.). J. Plant Physiol., 133, 486–491.Google Scholar
  18. Jones, M. D., Durall, D. M. and Tinker, P. B. (1991). Fluxes of carbon and phosphorus between symbionts in willow ectomycorrhizas and their changes with time. New Phytol., 119, 99–106.CrossRefGoogle Scholar
  19. Kuhn, A. J., Schröder, W. H. and Bauch, J. (2000). The kinetics of calcium and magnesium entry into mycorrhizal spruce roots. Planta, 210, 488–496.PubMedCrossRefGoogle Scholar
  20. Kulaev, I., Vagabov, V. and Kulakovskaya, T. (1999). New aspects of inorganic polyphosphate metabolism and function. J. Biosci. Bioeng., 88, 111–129.PubMedCrossRefGoogle Scholar
  21. Lei, J. and Dexheimer, J. (1988). Ultrastructural localization of ATPase activity in the Pinus sylvestris/Laccaria laccata ectomycorrhizal association. New Phytol., 108, 329–334.CrossRefGoogle Scholar
  22. Lewis, D. H. and Harley, J. L. (1965). Carbohydrate physiology of mycorrhizal roots of beech. I. Identity of endogenous sugars and utilization of exogenous sugars. New Phytol., 64, 224–237.CrossRefGoogle Scholar
  23. Marschner, H. and Dell, B. (1994). Nutrient uptake in mycorrhizal symbiosis. Plant Soil, 159, 89–102.Google Scholar
  24. Nehls, U., Mikolajewski, S., Magel, E. and Hampp, R. (2001). Carbohydrate metabolism in ectomycorrhizas: gene expression, monosaccharide transport and metabolic control. New Phytol., 150, 533–541.CrossRefGoogle Scholar
  25. Peng, S., Eissenstat, D. M., Graham, J. H., Williams, K., Hodge, N. C. (1993) Growth depression in mycorrhizal citrus at high-phosphorus supply. Plant Physiol., 101, 1063–1071.PubMedGoogle Scholar
  26. Peterson R. L. and Bonfante, P. (1994). Comparative structure of vesicular-arbuscular mycorrhizas and ectomycorrhizas. Plant Soil, 159, 79–88.Google Scholar
  27. Rosewarne, G. M., Barker, S. J., Smith, S. E., Smith, F. A. and Schachtman, D. P. (1999). A Lycopersicon esculentum phosphate transporter (LePT1) involved in phosphorus uptake from a vesicular-arbuscular mycorrhizal fungus. New Phytol., 144, 507–516.CrossRefGoogle Scholar
  28. Salzer, P. and Hager, A. (1993). Characterization of wall bound invertase isoforms of Picea abies cells and regulation by ectomycorrhizal fungi. Physiol. Plant., 88, 52–59.CrossRefGoogle Scholar
  29. Smith, S. E. and Read, D. J. (1997). Mycorrhizal Symbiosis (2nd ed). Academic Press, London.Google Scholar
  30. Smith, S. E. and Smith, F. A. (1990). Tansley review No. 20. structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol., 114, 1–38.CrossRefGoogle Scholar
  31. Smith, S. E., Dickson, S., Morris, C. and Smith, F. A. (1994a). Transfer of phosphate from fungus to plant in VA mycorrhizas: calculations of the area of symbiotic interface and of fluxes of P from two different fungi to Allium porrum L. New Phytol. 127, 93–99.CrossRefGoogle Scholar
  32. Smith S. E., Gianinazzi-Pearson, V., Koide, R. and Cairney, J. W. G. (1994b). Nutrient transport in mycorrhizas: structure, physiology and consequences for efficiency of the symbiosis. Plant Soil, 159, 103–113.CrossRefGoogle Scholar
  33. Smith, S. E., Dickson, S. and Smith, F. A. (2001). Nutrient transfer in arbuscular mycorrhizas: how are fungal and plant processes integrated? Aust. J. Plant Physiol., 28, 683–694.Google Scholar
  34. Tarkka, M., Niini, S. S. and Raudaskoski, M. (1998). Developmentally regulated proteins during differentiation of root system and ectomycorrhiza in Scots pine (Pinus sylvestris) with Suillus bovinus. Physiol. Plant., 104, 449–455.CrossRefGoogle Scholar
  35. Thomson, B. D., Clarkson, D. T. and Brain, P. (1990). Kinetics of phosphorus uptake by the germ-tubes of the vesicular-arbuscular mycorrhizal fungus, Gigaspora margarita. New Phytol., 116, 647–653.CrossRefGoogle Scholar
  36. Vesk, P. A., Ashford, A. E., Markovina, A. -L. and Allaway, W. G. (2000). Apoplasmic barriers and their significance in the exodermis and sheath of Eucalyptus pilularisPisolithus tinctorius ectomycorrhizas. New Phytol., 145, 333–346.CrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • H. BÜcking
    • 1
  • R. Hans
    • 2
  • W. Heyser
    • 2
  1. 1.Biology DepartmentState University of New JerseyUSA
  2. 2.University Bremen, Center for Environmental Research and TechnologyGermany

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