Stimulation of vesicular-arbuscular mycorrhiza formation and growth of white clover by flavonoid compounds
J. O. SIQUEIRA
Department of Botany and Plant Pathology, Michigan State University, East Lansing, MI 48824, USA
On leave from Escola Superior de Agricultura de Lavras, 372000-Lavras, MG-Brazil.
Search for more papers by this authorG. R. SAFIR
Department of Botany and Plant Pathology, Michigan State University, East Lansing, MI 48824, USA
Search for more papers by this authorM. G. NAIR
The Natural Products Chemistry Laboratory, Department of Horticulture, Michigan State University, East Lansing, MI 48824, USA
Search for more papers by this authorJ. O. SIQUEIRA
Department of Botany and Plant Pathology, Michigan State University, East Lansing, MI 48824, USA
On leave from Escola Superior de Agricultura de Lavras, 372000-Lavras, MG-Brazil.
Search for more papers by this authorG. R. SAFIR
Department of Botany and Plant Pathology, Michigan State University, East Lansing, MI 48824, USA
Search for more papers by this authorM. G. NAIR
The Natural Products Chemistry Laboratory, Department of Horticulture, Michigan State University, East Lansing, MI 48824, USA
Search for more papers by this authorsummary
The effects of flavonoid compounds on VA mycorrhiza root colonization and growth of white clover (Trifolium repens L.) plants under growth chamber conditions are reported. The isoflavonoids, formononetin and biochanin A, previously identified from clover roots, stimulated colonization and growth of clover, while several other flavonoid compounds were inactive when tested at concentrations of 5 mg 1−1. The flavone, chrysin, when applied at concentrations higher than those tested for formononetin and biochanin A, also increased root colonization and plant growth. The stimulatory effects of the isoflavonoids on plant growth were mediated by VA mycorrhizal fungi and were dependent on concentration, period of growth and soil spore density. Maximum responses were found when 5 mg 1−1 solutions were applied to soil containing 2 to 4 VA mycorrhiza spores g−1 of soil. These results may provide insights on the molecular mechanisms of host-fungus interaction and for the development of technology to exploit the potential of the indigenous VA mycorrhizal fungi in field soil.
references
- Adesanya, S. A., O'Neill, M. J. & Roberts, M. F. (1986). Structure-related fungitoxicity of isoflavonoids. Physiological and Molecular Plant Pathology 29: 95–103.
- Anderson, A. J. (1988). Mycorrhizae-host specificity and recognition. Phytopathology 78: 375–380.
- Bécard, G. & Fortin, J. A. (1988). Early events of vesicular-arbuscular mycorrhizae formation on Ri T-DNA transformed roots. New Phytologist 108: 211–218.
- Bécard, G. & Piché, Y. (1989). New aspects on the acquisition of biotrophic status by a vesicular-arbuscular mycorrhizal fungus. Gigaspora margartia. New Phytologist 112: 77–83.
- Bécard, G. & Piché Y. (1990). Physiological factors determining vesicular-arbuscular mycorrhizal formation in host and nonhost Ri T-DNA transformed roots. Canadian Journal Botany 68: 1260–1264.
-
Bonfante-Fasolo, P. (1988). The role of the cell wall as a signal in mycorrhizal associations. In: Cell to Signals in Plant, Animal and Microbial Symbiosis (Ed. by
S. Scannerini,
D. Smith,
P. Bonfante-Fasolo &
V. Gianinazzi-Pearson), pp. 219–235, Springer-Verlag,
Berlin
.
10.1007/978-3-642-73154-9_16 Google Scholar
- Burggraaf, A. P. J. & Beringer, J. E. (1989). Absence of nuclear DNA synthesis in vesicular-arbuscular mycorrhizal fungi during in vitro development. New Phytologist, 111, 25–33.
- Carr, G. R., Hinkley, F., Le Tacon, F., Hepper, C. M., Jones, M. G. K. & Thomas, E. (1985). Improved hyphal growth of two species of vesicular-arbuscular mycorrhizal fungi in the presence of suspension-cultured plant cells. New Phytologist 101: 417–426.
- Chang, C. F., Suzuki, Kumai, A. & Tamura, S. (1969). Chemical studies on ‘clover sickness’. Part II. Biological functions of isoflavonoids and their related compounds. Agricultural and Biological Chemistry 33: 398–408.
- Debnam, J. R. & Smith, I. M. (1976). Changes in the isoflavones and pterocarpans of red clover on infection with Sclerotina trifoliorum and Botrytis cinerea. Physiological Plant Pathology 9: 9–23.
- Elias, K. S. & Safir, G. R. (1987). Hyphal elongation of Glomus fasciculatum in response to root exudates. Applied and Environmental Microbiology, 53, 1928–1933.
-
Gerdemann, J. W. &
Nicolson, T. H. (1963). Spores of mycorrhizal endogone species extracted from soil by wet sieving and decanting.
Transactions of the British Mycological Society
46: 235–244.
10.1016/S0007-1536(63)80079-0 Google Scholar
- Gianinazzi-Pearson, V., Branzanti, B. & Gianinazzi, S. (1989). In vitro Enhancement of spore hyphal growth of vesicular-arbuscutar mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis 7: 243–255.
- Graham, J. H. (1982). Effect of citrus root exudates on germination of chlamydospores of the vesicular-arbuscular mycorrhizal fungus. Glomus epigaeum. Mycologia 74: 831–835.
- Hepper, C. M. (1979). Germination and growth of Glomus Caledonius spore: The effects of inhibitors and nutrients. Soil Biology Biochemistry 11: 269–277.
- Jacobs, M. & Rubery, P. H. (1988). Naturally occurring auxin transport regulators. Science 241: 346–349.
- Kebmann, M., Daniel, S. & Barz, W. (1988). Elicitation of ptero carpan phytoalexins in cell suspension cultures of different chickpea (Cicer arientinum L.) cultivars by an elicitor from the fungus Aschochyta rabiet, Zeitschrift für Naturforschung 43: 529–535.
- Kormanik, P. P. & McGraw, A. C. (1982). Quantification of vesicular-arbuscular mycorrhizae in plant roots. Methods and Principles of Mycorrhizae Research (Ed. by N. C. Schenck), pp. 37–45, APS, St Paul .
- Koster, J., Strack, D. & Barz, W. (1983). High performance liquid chromatographic separation of isoflavones and structural elucidation of isoflsvone 7-0-glucoside 6-malonates from Cicer arientnum. Plant Medica 48: 131–135.
- Lindeberg, G. & Lindeberg, M. (1980). Stimulation of litter-decomposing Basidiomycetes by fluvonoids. Transactions of the British Mycological Society 75: 445–459.
- Lynn, D. G & Chang, M. (1990). Phenolic signals in cohabitation: Implications for plant development. Annual Review Plant Physiology and Plant Molecular Biology 41: 497–526.
- Melchers, L. S., Regensburg-Tuink, A. J. G., Schilperoort, R. A. & Hooykaas, P. J. J. (1989). Specificity of signal molecules in the activation of Agrobacterium virulence gen expression. Molecular Microbiology 3: 969–977.
- Morandi, D. (1989). Effect of xenobiotics on endomycorrhizal infection and isoflavonoid accumulation in soybean roots. Plant Physiology and Biochemistry 27: 697–701.
- Morandi, D., Bailey, J. A. & Gianinazzi-Pearson, V. (1984). Isoflavonoid accumulation in soybean roots infected with vesicular-arbuscular mycorrhizal fungi. Physiological Plant Pathology 24: 357–364.
- Mosse, B. (1988). Some studies relating to ‘independent’ growth of vesicular-arbuscular endophytes. Canadian Journal of Botany 66: 2533–2540.
- Nair, M. G., Safir, G. R. & Siqueira, J. O. (1991). Isolation and identification of vesicular-arbuscular mycorrhiza stimulatory compounds from clover (Trifolium repens) root. Applied and Environmental Microbiology 57: 434–439.
- Paula, M. A. & Siqueira, J. O. (1990). Stimulation of hyphal growth of the VA mycorrhizal fungus Gigaspora margarita by suspension-cultured Pueraria phaseoloides cells and cell products. New Phytologist 115: 69–75.
- Phillips, J. M. & Hayman, D. S. (1970). Improved procedures for clearing roots, and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55: 158–162.
- Rao, A. S. (1990). Root flavonoids. The Botanical Review 56: 1–75.
- Rolfe, B. G. (1988). Flavones and isoflavone as inducing substances of legume nodulation. Biofactors 1: 3–10.
- Rossiter, R. C. & Beck, A. B. (1966). Physiological and ecological studies on the oestrogenic isoflavones in subterranean clover (T. subterraneaum L.). II. Effects of phosphate supply. Australian Journal of Agricultural Research 17: 447–456.
- Schlieper, D. & Barz, W. (1987). NADPH: Biochanin A oxidoreductase from the fungus Fusarium javanicum. Phytochemistry 26: 2495–2498.
- Siqueira, J. O. (1987). Cultura axenica e monoxenica de fungos micorrizicos vesiculo-arbusculares. II. Reuniao Brasileira sobre micorrizas. pp. 44–70.SMA/SA/USP, Sao Paulo.
- Siqueira, J. O., Safir, G. R. & Nair, M. G. (1991). VA-mycorrhiza and mycorrhizal stimulating isoflavonoid compounds reduce plant herbicide injury. Plant and Soil (in the press).
- Siqueira, J. O., Sylvia, D. M., Gibson, J. & Hubbel, D. H. (1985). Spores, germination, and germ tubes of vesicular-arbuscular mycorrhizal fungi. Canadian Journal Microbiology 31: 965–971.
- Smith, S. E., Nicholas, D. J. D. & Smith, F. A. (1979). Effect of early mycorrhizal infection on nodulation and nitrogen fixation in Trifolium subterraneum L. Australian Journal of Plant Physiology 6: 305–316.
- Tamura, S., Chang, C. F., Suzuki, A. & Kumai, S. (1969). Chemical studies on ‘clover sickness’. Part I. Isolation and structural elucidation of two isoflavonoids in red clover. Agricultural and Biological Chemistry 33: 391–397.
- van Etten, H. D. (1976). Antifungal activity of pteroearpans and other selected isoflavonoids. Phytochemistry 15: 655–659.
- Weltring, K. M., Mackenbrock, K. & Barz, W. (1982). Demethylation, methylation and 3′-hydroxylation of iso-flavones by Fusarium fungi. Zeitschrift für Naturforschung 37c: 570–574.
