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Selected Ectomycorrhizal Fungi of Black Spruce (Picea mariana) can Detoxify Phenolic Compounds of Kalmia angustifolia

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Abstract

Allelopathy has been implicated as a factor contributing toward failure of black spruce (Picea mariana) regeneration in Kalmia angustifolia-dominated sites in eastern Canada. Several phenolic acids of Kalmia origin inhibit primary root growth of black spruce. We tested the hypothesis that some well-adapted conifer ectomycorrhizae can degrade and detoxify water-soluble phenolic compounds produced by Kalmia and use the degraded products as a carbon source to stimulate growth. We found that hyphal growth of Paxillus involutus, a common ectomycorrhizal fungus of black spruce, was stimulated by water leachates of Kalmia leaf and litter. An equimolar mixture of three phenolic acids (ferulic, o-coumaric, and o-hydroxyphenylacetic acid), commonly found in Kalmia, had no negative effects on fungal growth at 1 mM concentration. The o-hydroxyphenylacetic (o-HPA) acid, which is known to be toxic to black spruce, was found to stimulate the growth of Laccaria laccata, L. bicolor, and P. involutus (isolates 211804 and 196554) by 38.4, 29.3, 25.0, and 18.9%, respectively, at 1 mM. Pure ferulic, o-coumaric, and o-HPA acids were degraded by 100, 98, and 79.5%, respectively, within 10 d in the presence of P. involutus 211804. However, L. laccata could not tolerate high concentrations of the Kalmia leachates. P. involutus and L. bicolor used o-HPA acid as a carbon source when cultured in noncarbon nutrient medium. The 0.5 and 0.2 mM o-HPA acid inhibited the root growth of black spruce. However, after solutions had been exposed to a culture of P. involutus, they had no significant effect on seedling growth of black spruce. We concluded that some ectomycorrhizal fungi, such as P. involutus and L. bicolor, are able to degrade Kalmia phenolics. Our findings point to a mechanism by which ectomycorrhizal species can control species interactions in higher plants by changing the rhizosphere chemistry.

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Acknowledgments

We acknowledge the financial support from the Natural Science and Engineering Research Council (NSERC) discovery grant (to AUM) and the National Natural Science Foundation of China (30270230, 30370246), Guangdong Natural Science Foundation of China (039254, 04105977), the National 973 project of China (2006CB100200), Program for New Century Excellent Talents in University (to RSZ). We thank Dr. Christine Gottardo, Debbie Leach, and Andrea Aguirre of the Chemistry Department, Lakehead University, and Haihong Bi of the Department of Ecology, South China Agricultural University for their help in HPLC analyses, and Dr. Ed Setliff of the Faculty of Forestry and the Forest Environment, Lakehead University for his cooperation during the inoculation experiments. Comments of two anonymous reviewers, the journal editor, Drs. Robert D. Guy and Jenelle Curtis (Faculty of Forestry, University of British Columbia), Leonard Hutchison, and Brian McLaren (Faculty of Forestry and the Forest Environment, Lakehead University) were helpful in revising the manuscript.

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Correspondence to Azim U. Mallik.

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Zeng, R.S., Mallik, A.U. Selected Ectomycorrhizal Fungi of Black Spruce (Picea mariana) can Detoxify Phenolic Compounds of Kalmia angustifolia . J Chem Ecol 32, 1473–1489 (2006). https://doi.org/10.1007/s10886-006-9063-6

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