Patterns of Interaction between Populus Esch5 and Piriformospora indica: A Transition from Mutualism to Antagonism

Abstract

Piriformospora indica (Sebacinaceae, Basidiomycota) is an axenically cultivable, plant growth promoting root endophyte with a wide host range, including Populus. Rooting of Populus Esch5 explants started within 6 days after transfer to WPM medium. If such plantlets with roots were inoculated with P. indica, there was an increase in root biomass, and the number of 2nd order roots was increased significantly. A totally different observation was recorded when the explants were placed into WPM with pre-grown P. indica. The interaction led to complete blocking of root production and severely inhibited plant growth. Additionally, branched aerial roots appeared which did not penetrate the medium. On contact with the fungal colony or the medium, the ends of the aerial roots became inflated. Prolonged incubation stimulated the fungus to colonize aerial parts of the plant (stem and leaves). Mycelium not only spread on the surface of the aerial parts, but also invaded the cortical tissues inter- and intracellularly. Detached Populus leaves remained vital for 4 - 5 weeks on sterile agar media or on AspM medium with pre-grown P. indica. When the fungus was pre-grown on culture media such as WPM, containing ammonium as the main source of nitrogen, leaves in contact with the cultures turned brownish within 4 - 12 h. Thereafter, the leaves bleached, and about one day later had become whitish. Thus, cultural conditions could alter the behaviour of the fungus drastically: the outcome of the interaction between plant and fungus can be directed from mutualistic to antagonistic, characterized by fungal toxin formation and extension of the colonization to Populus shoots.

Key words

Piriformospora indica - Populus Esch5 - mutualism - antagonism - rooting pattern - woody plant medium (WPM) - Sebacinaceae - Basidiomycota

References

• 1 Ahuja M. R.. Aspen. Evans, D. A., Sharp, W. R., and Ammirato, P. J., eds. Handbook of Plant Cell Culture 4, Techniques and Applications. New York; Macmillan Publishing Company (1986): 626-651
• 2 Berch S. M., Allen T. R., Berbee T. D.. Community structure and phylogeny of ericoid mycorrhizal fungi.  Plant and Soil. (2002);  244 55-66
• 3 Blechert O., Kost G., Hassel A., Rexer K.-H.. First remarks on the symbiotic interaction between Piriformospora indica and terrestrial orchids. Varma, A. and Hock, B., eds Mycorrhiza Structure, Function, Molecular Biology and Biotechnology. Heidelberg; Springer Verlag (1999): 683-688
• 4 Glen M., Tommerup I. C., Bougher N. L., O'Brien P. A.. Are Sebacinaceae common and widespread ectomycorrhizal associated of Eucalyptus species in Australian forests?.  Mycorrhiza. (2002);  12 243-247
• 5 Hill T. W., Käfer E.. Improved protocols for Aspergillus minimal medium: trace element and minimal medium salt stock solutions.  Fungal Genetic Newsletters. (2001);  48 20-21
• 6 Kaldorf M., Ludwig-Müller J.. AM fungi might affect the root morphology of maize by increasing indole-3-butyric acid biosynthesis.  Physiologia Plantarum. (2000);  109 58-67
• 7 Kottke I., Beiter A., Weiß M., Haug I., Oberwinkler F., Nebel M.. Heterobasidiomycetes from symbiontic associations with hepatics: Jungermanniales have sebacinoid mycobionts while Aneura pinguis (Metzgeriales) is associated with a Tulasnella species.  Mycological Research. (2003);  107 957-968
• 8 Lloyd G., McCown B.. Commercially feasible micropropagation of mountain laurel (Kalimia latiflora) by use of shoot tip culture.  Proceedings of International Plant Propagators Society. (1981);  30 421-427
• 9 McKendrick S. L., Leake J. R., Taylor D. L., Read D. J.. Symbiotic germination and development of the myco-heterotrophic orchid Neottia nidus-avis in nature and its requirement for locally distributed Sebacina spp.  New Phytologist. (2002);  154 233-247
• 10 Pham G. H., Kumari R., Singh A., Malla R., Prasad R., Sachdev M., Kaldorf M., Buscot F., Oelmuller R., Hampp R., Saxena A. K., Rexer K.-H., Kost G., Varma A.. Axenic culture of symbiotic fungus Piriformospora indica. . Varma, A., Abbott, L. K., Werner, D., and Hampp, R., eds. Plant Surface Microbiology. Heidelberg; Springer Verlag (2004 a): 593-613
• 11 Pham G. H., Singh A., Malla R., Kumari R., Prasad R., Sachdev M., Rexer K.-H., Kost G., Luis P., Kaldorf M., Buscot F., Herrmann S., Peskan T., Oelmüller R., Saxena A. K., Declerck S., Mittag M., Stabentheiner E., Hehl S., Varma A.. Interaction of Piriformospora indica with diverse microorganisms and plants. Varma, A., Abbott, L. K., Werner, D., and Hampp, R., eds. Plant Surface Microbiology. Heidelberg; Springer Verlag (2004 b): 237-265
• 12 Rai M., Acharya D., Singh A., Varma A.. Positive growth responses of the medical plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial.  Mycorrhiza. (2001);  11 123-128
• 13 Sahay N. S., Varma A.. Piriformospora indica: a new biological hardening tool for micropropagated plants.  FEMS Microbiology Letters. (1999);  181 297-302
• 14 Selosse M. A., Bauer R., Moyersoen B.. Basal Hymenomycetes belonging to the Sebacinaceae are ectomycorrhizal on temperate deciduous trees.  New Phytologist. (2002 a);  155 183-195
• 15 Selosse M. A., Weiß M., Jany J. L., Tiller A.. Communities and populations of sebacinoid basidiomycetes associated with the achlorophyllous orchid Neottia nidus-avis (L.) L. C. M. Rich. and neighbouring tree ectomycorrhizae.  Molecular Ecology. (2002 b);  11 1831-1844
• 16 Singh A., Singh A., Kumari M., Rai M. K., Varma A.. Biotechnological importance of Piriformospora indica - a novel symbiotic mycorrhiza-like fungus: an overview.  Indian Journal of Biotechnology. (2003);  2 65-75
• 17 Spurr A. R.. A low-viscosity epoxy resin embedding medium for electron microscopy.  Journal of Ultrastructural Research. (1969);  26 31-43
• 18 Sudha. In vitro study of endosymbionts associated with tissue culture raised medicinal plants. PhD thesis, Jamia Hamdard University, New Delhi. (2000)
• 19 Urban A., Weiß M., Bauer R.. Ectomycorrhizas involving sebacinoid mycobionts.  Mycological Research. (2003);  107 3-14
• 20 Varma A., Verma S., Sudha Sahay N., Bütehorn B., Franken P.. Piriformospora indica, a cultivable plantgrowth-promoting root endophyte.  Applied and Environmental Microbiology. (1999);  65 2741-2744
• 21 Varma A., Singh A., Sudha Sahay N. S., Sharma J., Roy A., Kumari M., Rana D., Thakran S., Deka D., Bharati K., Hurek T., Blechert O., Rexer K.-H., Kost G., Hahn A., Hock B., Maier W., Walter M., Strack D., Kranner I.. Piriformospora indica: an axenically culturable mycorrhizal fungus. Hock, B., ed. The Mycota IX. Berlin; Springer Verlag (2001): 125-150
• 22 Varma A., Hock B.. Mycorrhiza Structure, Function, Molecular Biology, Biotechnology. Heidelberg, Berlin; Springer Verlag (1999)
• 23 Varma A., Schuepp H.. Mycorrhizae: their application in micropropagated plantlets.  Critical Reviews in Biotechnology. (1995);  15 313-328
• 24 Verma S.. Plant endomycorrhizal fungal interactions: a biotechnological approach. PhD thesis, Barakatullah University, Bhopal. (1996)
• 25 Verma S., Varma A., Rexer K.-H., Hassel A., Kost G., Sarbhoy A., Bisen P., Bütehorn B., Franken P.. Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus.  Mycologia. (1998);  90 898-905
• 26 Warcup J. H.. Mycorrhizal associations of isolates of Sebacina vermifera. .  New Phytologist. (1988);  110 227-231
• 27 Weiß M., Selosse M.-A., Rexer K.-H., Urban A., Oberwinkler F.. Sebacinales: A hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential.  Mycological Research. (2004);  108 1003-1010

Editor: J. Cullimore