Abstract
Brassicaceae plants are nonmycorrhizal. They were found to inhibit VA mycorrhizal infection in their host plants. We tested if they can influence growth of ectomycorrhizal (ECM) fungi. When roots and leaves of Brassicaceae plants and ECM fungi were cultured together in the same petri dishes, the root exudates of turnip (Brassica rapa), swede (B. napobrassica), cabbage (B. oleracea, var. capitata), broccoli (B. oleracea, var. italica Plenck), kohlrobi (B. caulorapa Pasq.), mustard (B. juncea), radish (Raphanus sativus), and choy (B. napus) significantly stimulated hyphal growth of the ectomycorrhizal fungus Paxillus involutus. Root exudates of turnip and cabbage stimulated hyphal growth of Pisolithus tinctorius and two isolates of P. involutus. Colony area of P. involutus was increased by 452 and 414%, respectively, in the presence of turnip and cabbage germinants. Root exudates of turnip increased the biomass of P. involutus and P. tinctorius by 256 and 122% and cabbage by 220 and 82%, respectively. The stimulatory effect was not affected by autoclaving the root exudates. Root exudates had chemical reactions with glutathione and lysine, which resulted in a reduction of the growth stimulation of ECM fungi. Myrosinase enhanced further the stimulatory effects of turnip on the ECM colony diameter growth by 23%. Autoclaved roots and leaves of turnip did not stimulate fungal growth, but mechanically ground roots and leaves of turnip stimulated growth of involutus by 147 and 135%, respectively. After desulfuration with aryl sulphatase, the glucosinolates (GLSs) in turnip roots and leaves were identified by HPLC. The major ones were indole GLSs. Prominent compounds identified were 1-methoxy-3-indolymethyl GLS and 4-methoxy-3-indolymethyl GLS. The finding provides an opportunity to field test the use of Brassicaceae plants in enhancing ectomycorrhizal formation in conifers by interplanting conifers with Brassicaceae plants in forest tree nursery and agroforestry systems.
Similar content being viewed by others
References
Bennett, R. N. and Wallsgrove, R. M. 1994. Secondary metabolites in plant defence mechanism. New Phytol. 127:617–633.
Brunner, I. 2001. Ectomycorrhizas: Their role in forest ecosystems under the impact of acidifying pollutants. Persp. Plant Ecol. Evol. System. 4:13–27.
Chevolleau, S., Gasc, N., Rollin, P., and Tulliez, J. 1997. Enzymatic, chemical, and thermal breakdown of 3H-labeled glucobrassicin, the parent indole glucosinolate. J. Agric. Food Chem. 45:4290–4296.
Fahey, J. W., Zalcmann, A. T., and Talalay, P. 2001. The chemical diversity and distribution of glucosinlates and isothiocyanates among plants. Phytochemistry 56:5–51.
Haselwandter, K. and Bowen, G. D. 1996. Mycorrhizal relation in trees for agroforestry and land rehabilitation. For. Ecol. Manage. 81:1–17.
Jones, M. D., Durall, D. M., and Tinker, P. B. 1990. Phosphorus relations and production of extramatrical hyphae by two types of willow ectomycorrhizas at different soil phosphorus levels. New Phytol. 115:259–267.
Kawakishi, S. and Kaneko, T. 1985. Interaction of oxidized glutathione with allyl isothiocyanate. Phytochemistry 24:715–718.
Koide, R. T. and Schreiner, R. P. 1992. Regulation of the vesicular–arbuscular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:557–581.
Luthy, B. and Matile, P. 1984. The mustard oil bomb: Rectified analysis of the subcellular organization of the myrosinase system. Biochem. Physiol. Pflanzen. 179:5–12.
Marx, D. H. 1969. The influence of ectotrophic mycorrhizal fingi on the resistance of pine roots to pathogenic infection. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59:153–163.
Melin, E. 1954. Growth factor requirements of mycorrhizal fungi of forest trees. Svensk Botanisk Tidskrift. 48:86-94
Minchinton, I., Sang, J., Bruke, D., and Truscott, R. J. W. 1982. Separation of desulphoglucosinolates by reversed-phase high-performance liquid chromatography. J. Chromatogr. 247:141–148.
Mithen, R. F., Lewis, B. G., Heaney, R. K., and Fenwick, G. R. 1987. Glucosinolates of wild and cultivated Brassica species. Phytochemistry 26:1969–1973.
Petersen, J., Belz, R., Walker, F., and Gurle, K. 2001. Weed suppression by release of isothiocyanates from turnip-rape mulch. Agron. J. 93:37–43.
Rosa, E. A. S. and Rodrigues, P. M. F. 1999. Towards a more sustainable agriculture system: Effect of glucosinolates on the control of soil borne diseases. J. Hort. Sci. Biotech. 74:667–674.
Sang, J. P., Minchinton, I. R., Johnstone, P. K., and Truscott, R. J. W. 1984. Glucosinolate profiles in the seed, root and leaf tissue of cabbage, mustard, rapeseed, radish and swede. Can. J. Plant Sci. 64:77–93.
Satyanarayana, T., Gupta, V., and Garg, S. 1996. Ectomycorrhizal fungi as experimental organisms, pp. 333-346. in K. G. Mukerji (ed.). Concepts in Mycorrhizal Research. Kluwer Academic Publishers, Dordrecht, the Netherlands
Schreiner, R. P. 1992. The Role of Isothiocyanates in the Resistance of Mustards to Vesicular–Arbuscular Mycorrhizal Fungi, Ph.D. Dissertation, Pennsylvania State University, Pennsylvania
Schreiner, R. P. and Koide, R. T. 1993. Mustards, mustard oils and mycorrhizas. New Phytol. 123:107–113.
Straatsma, G., Van Griensven, L. J. L. D, and Bruinsma, J. 1986. Root influence on in vitro growth of hyphae of the mycorrhizal mushroom Cantharellus cibarius replaced by carbon deoxide. Physiol. Plantarum 67:521–528.
Sun, Y. P. and Fries, N. 1992. The effects of tree-root exudates on the growth rate of ectomycorrhizal and saprotrophic fungi. Mycorrhiza 1:63–69.
Tang, C. S. and Takenaka, T. 1983. Quantification of a bioactive metabolite in undisturbed rhizosphere-benzyl isothiocyanate from Carica papaya L. J. Chem. Ecol. 9:1247–1253.
Tester, M., Smith, S. E., and Smith, F. A. 1987. The phenomenon of ‘nonmycorrhizal’ plants. Can. J. Bot. 65:419–431.
Vierheilig, H., Bennett, R., Kiddle, G., Kaldorf, M., and Müller, J. L. 2000. Difference in glucosinolate patterns and arbuscular mycorrhizal status of glucosinolate-containing plant species. New Phytol. 129:343–352.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zeng, R.S., Mallik, A.U. & Setliff, E. Growth Stimulation of Ectomycorrhizal Fungi by Root Exudates of Brassicaceae Plants: Role of Degraded Compounds of Indole Glucosinolates. J Chem Ecol 29, 1337–1355 (2003). https://doi.org/10.1023/A:1024257218558
Issue Date:
DOI: https://doi.org/10.1023/A:1024257218558