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Plant and Soil

, Volume 205, Issue 2, pp 181–192 | Cite as

Extracellular enzyme activities of the ericoid mycorrhizal endophyte Hymenoscyphus ericae (Read) Korf & Kernan: their likely roles in decomposition of dead plant tissue in soil

  • J.W.G. Cairney
  • R. M. Burke
Article

Abstract

Hymenoscyphus ericae (Read) Korf & Kernan is known to form mycorrhizas with a number of host plants in the Ericaceae. The fungus produces a range of extracellular enzyme activities which have the potential to mediate utilisation of organic sources of nitrogen and phosphorus in soil. H. ericae has recently been shown also to produce enzyme activities that may allow the fungus to decompose components of the plant cell wall, facilitating access to mineral nutrients sequestered within the walls of moribund plant cells. In this review we assess the evidence for production of cellulolytic, hemicellulolytic, pectinolytic and ligninolytic activities by H. ericae and discuss their likely relevance to nutrient cycling processes.

cellulase ericoid mycorrhizas hemicellulase lignin degradation pectinase 

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References

  1. Abuarghub S M and Read D J 1988a The biology of mycorrhizas in the Ericaceae. XI. The distribution of nitrogen in the soil of a typical upland Callunetum with special reference to the 'free’ amino acids. New Phytol. 108, 425-431.Google Scholar
  2. Abuarghub S M and Read D J 1988b The biology of mycorrhizas in the Ericaceae. XII. Quantitative analysis of individual 'free’ amino acids in relation to time and depth in the soil profile. New Phytol. 108, 433-441.Google Scholar
  3. Ander P, Mishra C, Farrell R L and Eriksson K-E L 1990 Redox reactions in lignin degradation: interactions between laccase, different peroxidases and cellobiose: quinone oxidoreductase. J. Biotechnol. 13, 189-198.Google Scholar
  4. Argyropoulos D S and Menachem S B 1997 Lignin. In Biotechnology in the pulp and paper industry. Ed. K-E L Eriksson. pp 127-158. Springer-Verlag, Berlin.Google Scholar
  5. Backa S, Gierer J, Reitberger T and Nilsson T 1992 Hydroxyl radical activity in brown-rot fungi studied by a new chemiluminescence method. Holzforschung 46, 61-67.Google Scholar
  6. Bajwa R, Abuarghub S M and Read D J 1985 The biology of mycorrhiza in the Ericaceae. X. The utilization of proteins and the production of proteolytic enzymes by the mycorrhizal endophyte and by mycorrhizal plants. New Phytol. 101, 469-486.Google Scholar
  7. Bending G D 1994 The mobilisation of organic nitrogen by mycorrhizal fungi with special reference to natural substrates. Ph.D. Thesis, University of Sheffield, UK.Google Scholar
  8. Bending G D and Read D J 1996a Effects of the soluble polyphenol tannic acid on the activities of ericoid and ectomycorrhizal fungi. Soil Biol. Biochem. 28, 1995-1602.Google Scholar
  9. Bending G D and Read D J 1996b Nitrogen mobilization from protein-polyphenol complex by ericoid and ectomycorrhizal fungi. Soil Biol. Biochem. 28, 1603-1612.Google Scholar
  10. Bending G D and Read D J 1997 Lignin and soluble-phenolic degradation by ectomycorrhizal and ericoid mycorrhizal fungi. Mycol. Res. 101, 1348-1354.Google Scholar
  11. Benoit R E and Starkey R L 1968 Enzyme inactivation as a factor in the inhibition of decomposition of organic matter by tannins. Soil Sci. 105, 203-208.Google Scholar
  12. Broda P, Birch P R J, Brooks P R and Sims P F G 1995 PCR-mediated analysis of lignocellulolytic gene transcription by Phanerochaete chrysosporium — substrate-dependent differential expression within gene families. Appl. Env. Microbiol. 61, 2358-2364.Google Scholar
  13. Burke R M and Cairney J W G 1997a Carbohydrolase production by the ericoid mycorrhizal fungus Hymenoscyphus ericae under solid-state fermentation conditions. Mycol. Res. 101, 1135-1139.Google Scholar
  14. Burke R M and Cairney J W G 1997b Purification and characterization of a β-1,4-enxoxylanase from the ericoid mycorrhizal fungus Hymenoscyphus ericae. New Phytol. 135, 345-352.Google Scholar
  15. Burke R M and Cairney J W G 1998 Carbohydrate oxidases in ericoid and ectomycorrhizal fungi: a possible source of Fenton radicals during degradation of lignocellulose. New Phytol. 139, 637-645.Google Scholar
  16. Cairney J W G and Burke R M 1994 Fungal enzymes degrading plant cell walls: their possible significance in the ectomycorrhizal symbiosis. Mycol. Res. 98, 1345-1346.Google Scholar
  17. Cairney J W G and Burke R M 1996a Physiological heterogeneity within fungal mycelia: an important concept for a functional understanding of the ectomycorrhizal symbiosis. New Phytol. 134, 685-695.Google Scholar
  18. Cairney J W G and Burke R M 1996b Plant cell wall-degrading enzymes in ericoid and ectomycorrhizal fungi. In Mycorrhizas in integrated systems. Eds. C Azcon-Aguilar and J M Barea. pp 218-221. European Commission, Brussels.Google Scholar
  19. Carleton T J and Read D J 1991 Ectomycorrhizas and nutrient transfer in conifer-feather moss ecosystems. Can. J. Bot. 69, 778-785.Google Scholar
  20. Carpita N C and Gibeaut D M 1993 Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 3, 1-30.Google Scholar
  21. Coughlan M P, Tuohy M G, Filho E X F, Puls J, Claeyssens M, Vranská M and Hughes M M 1993 Enzymological aspects of microbial hemicellulases with emphasis on fungal systems. In Hemicellulose and hemicellulases. Eds. M P Coughlan and G P Hazlewood. pp 53-84. Portland Press, London.Google Scholar
  22. Couture M, Fortin J A and Dalpé Y 1983 Oidiodendron griseum (Robak): and endophyte of ericoid mycorrhizas in Vaccinium spp. New Phytol. 95, 375-380.Google Scholar
  23. Dalpé Y 1986 Axenic synthesis of ericoid mycorrhiza in Vaccinium angustifolium Ait. by Oidiodendron species. New Phytol. 103, 391-396.Google Scholar
  24. Di Battista C, Selosse M-A, Bouchard D, Stenström E and Le Tacon F 1996 Variations in symbiotic efficiency, phenotypic characters and ploidy level among isolates of the ectomycorrhizal basidiomycete Laccaria bicolor strain S 238. Mycol. Res. 100, 1315-1324.Google Scholar
  25. Douglas G C, Heslin M C and Reid C P P 1989 Isolation of Oidiodendron maius from Rhododendron and ultrastructural characterization of synthesised mycorrhizas. Can. J. Bot. 67, 2206-2212.Google Scholar
  26. Egger K N 1986 Substrate hydrolysis patterns of post-fire ascomycetes (Pezizales). Mycologia 78, 771-780.Google Scholar
  27. Egger K N and Sigler L 1993 Relatedness of the ericoid endophytes Scytalidium vaccinii and Hymenoscyphus ericae inferred from analysis of ribosomal DNA. Mycologia 85, 219-230.Google Scholar
  28. Eriksson K-E L, Blanchette R A and Ander P 1990 Microbial and enzymatic degradation of wood and wood components. Springer-Verlag, Berlin.Google Scholar
  29. Fengel D and Wegener G 1983 Wood: chemistry, ultrastructure, reactions. Walter de Gruyter, Berlin.Google Scholar
  30. Fenton H J H 1894 Oxidation of tartaric acid in the presence of iron. J. Chem. Soc. 65, 899-910.Google Scholar
  31. Gierer J, Yang E and Reitberger T 1992 The reactions of hydroxyl radicals with aromatic rings in lignins, studied with creosol and 4-methylveratrol. Holzforschung 46, 495-504.Google Scholar
  32. Glenn J K and Gold M H 1985 Purification and characterization of an extracellular Mn(II)-dependent peroxidase from the lignin-degrading basidiomycete Phanerochaete chrysosporium. Arch. Biochem. Biophys. 242, 329-341.Google Scholar
  33. Gold M H, Wariishi H and Valli K 1989 Extracellular peroxidases involved in lignin degradation by the white rot basidiomycete Phanerochaete chrysosporium. Am. Chem. Soc. Symp. Ser. 389, 127-140.Google Scholar
  34. Green T R 1977 Significance of glucose oxidaze in lignin degradation. Nature 268, 78-80.Google Scholar
  35. Haemmerli S D, Leisola M S A and Fiechter A 1986 Polymerization of lignins by ligninases from Phanerochaete chrysosporium. FEMS Microbiol. Lett. 35, 33-36.Google Scholar
  36. Hambleton S and Currah R S 1997 Fungal endophytes from roots of alpine and boreal Ericaceae. Can. J. Bot. 75, 1570-1581.Google Scholar
  37. Hammel K E, Kalyaranaman B and Kirk T K 1986 Substrate free radicals are intermediates in ligninase catalysis. Proc. Natl Acad. Sci. USA. 83, 3709-3712.Google Scholar
  38. Hammel KE and Moen M A 1991 Depolymerization of a synthetic lignin in vitro by lignin peroxidase. Enzyme Microb. Technol. 13, 15-18.Google Scholar
  39. Heal O W, Latter P M and Howson G 1978 A study of the rates of decomposition of organic matter. In Production ecology of British moors and montane grasslands. Eds. O W Heal and D F Perkins. pp 136-159. Springer-Verlag, Berlin.Google Scholar
  40. Haselwandter K, Bobleter O and Read D J 1990 Degradation of 14C-labelled lignin and dehydropolymer of coniferyl alcohol by ericoid and ectomycorrhizal fungi. Arch. Microbiol. 153, 352-354.Google Scholar
  41. Hatakka A 1994 Lignin-modifying enzymes from selected whiterot fungi: production and role in lignin degradation. FEMS Microbiol. Rev. 13, 125-135.Google Scholar
  42. Higuchi T 1985a Biosynthesis of lignin. In Biosynthesis and biodegradation of wood components. Ed. T Higuchi. pp 140-160. Academic Press, London.Google Scholar
  43. Higuchi T 1985b Degradative pathways of lignin model compounds. In Biosynthesis and biodegradation of wood components. Ed. T Higuchi. pp 557-576. Academic Press, London.Google Scholar
  44. Hutton B J, Dixon K W and Sivasithamparam K 1994 Ericoid endophytes of Western Australian heaths (Epacridaceae). New Phytol. 127, 557-566.Google Scholar
  45. Jalal M A F and Read D J 1983a The organic acid composition of Calluna heathland with special reference to phyto-and fungitoxicity. I. Isolation and identification of organic acids. Plant Soil 70, 257-272.Google Scholar
  46. Jalal M A F and Read D J 1983b The organic acid composition of Calluna heathland with special reference to phyto-and fungitoxicity. II. Monthly quantitative determination of the organic acid content of Calluna and spruce dominated soils. Plant Soil 70, 273-286.Google Scholar
  47. Joseleau J-P, Gharibian S, Comtat J, Lefebvre A and Ruel K 1994 Indirect involvement of ligninolytic enzyme systems in cell wall degradation. FEMS Microbiol. Rev. 13, 255-264.Google Scholar
  48. Kerley S J and Read D J 1995 The biology of mycorrhiza in the Ericaceae. XVIII. Chitin degradation by Hymenoscyphus ericae and transfer of chitin-nitrogen to the host plant. New Phytol. 131, 369-375.Google Scholar
  49. Kerley S J and Read D J 1997 The biology of mycorrhiza in the Ericaceae. XIX. Fungal mycelium as a nitrogen source for the ericoid mycorrhizal fungus Hymenoscyphus ericae and its host plants. New Phytol. 136, 691-701.Google Scholar
  50. Kersten P J, Tien M, Kalyaranaman B and Kirk T K 1985 The ligninase of Phanerochaete chrysosporium generates cation radicals from methoxybenzenes. J. Biol. Chem. 260, 2609-2612.Google Scholar
  51. Kirk T K and Farrell R L 1987 Enzymatic 'combustion': the microbial degradation of lignin. Ann. Rev. Microbiol. 41, 465-505.Google Scholar
  52. Kirk T K, Mozuch M D and Tien M 1985 Free hydroxyl radical is not involved in an important reaction of lignin degradation by Phanerochaete chrysosporium Burds. Biochem. J. 226, 445-460.Google Scholar
  53. Kirk T K and Shimida M 1985 Lignin biodegradatiuon: the microorganisms involved and the physiology and biochemistry of degradation by white-rot fungi. In Biosynthesis and biodegradation of wood components, Ed. T Higuchi. pp 579-605. Academic Press, London.Google Scholar
  54. Kolbe J and Kubicek CP 1990 Quantification and identification of the main components of the Trichorerma reesei cellulase complex with monoclonal antibodies using an enzyme-linked immunosorbent assay (ELISA). Appl. Microbiol. Biotechnol. 24, 26-30.Google Scholar
  55. Kuhad R C, Singh A and Eriksson K-E L 1997 Microorganisms and enzymes involved in the degradation of plant fiber cell walls. In Biotechnology in the pulp and paper industry, Ed. K-E L Eriksson. pp 45-125. Springer-Verlag, Berlin.Google Scholar
  56. Kuiters A T and Dennemann C A J 1987 Water soluble phenolic substances in soils under several coniferous and deciduous tree species. Soil Biol. Biochem. 19, 765-769.Google Scholar
  57. Lamport D T A 1980 Structure, biosynthesis and significance of cell wall glycoproteins. In The structures, biosynthesis and degradation of wood, Eds. F A Loewus and V C Runeckles. pp 79-115. Plenum Press, New York.Google Scholar
  58. Leake J R and Miles W 1996 Phosphodiesters as mycorrhizal P sources. I. Phosphodiesterase production and the utilization of DNA as a phosphorus source by the ericoid mycorrhizal fungus Hymenoscyphus ericae. New Phytol. 132, 435-443.Google Scholar
  59. Leake J R and Read D J 1989a The biology of mycorrhiza in the Ericaceae. XIII. Some characteristics of the extracellular proteinase activity of the ericoid endophyte Hymenoscyphus ericae. New Phytol. 112, 69-76.Google Scholar
  60. Leake J R and Read D J 1989b The effects of phenolic compounds on nitrogen metabolism by ericoid mycorrhizal systems. Agric. Ecosystems Environ. 29, 225-236.Google Scholar
  61. Leake J R and Read D J 1990a Chitin as a nitrogen source for mycorrhizal fungi. Mycol. Res. 94, 993-1008.Google Scholar
  62. Leake J R and Read D J 1990b Proteinase activity in mycorrhizal fungi. I. The effect of extracellular pH on the production and activity of proteinase by ericoid endophytes from soils of contrasted pH. New Phytol. 115, 243-250.Google Scholar
  63. Leake J R and Read D J 1990c Proteinase activity in mycorrhizal fungi. II. The effects of mineral and organic nitrogen sources on induction of extracellular proteinase in Hymenoscyphus ericae (Read) Korf and Kernan. New Phytol. 116, 123-128.Google Scholar
  64. Leake J R and Read D J 1991 Experiments with ericoid mycorrhiza. In Methods in microbiology, Vol. 23. Eds. J R Norris, D J Read and A K Varma. pp 435-459. Academic Press, London.Google Scholar
  65. Lemoine M C 1992 Etudes des interactions cellulaires entre symbiotes endomycorhiziens chez les Ericales. Role des phosphatases acides fongiques: approaches physiologiques, biochemiques, immunologiques et cytologiques. Doctoral Thesis, Univeristy of Nancy.Google Scholar
  66. Lemoine M C, Gianinazzi-Pearson V, Gianinazzi S and Straker C J 1992 Occurrence and expression of acid phosphatase of Hymenoscyphus ericae (Read) Korf and Kernan, in isolation or associated with plant roots. Mycorrhiza 1, 137-146.Google Scholar
  67. Marx D H and Bryan W C 1975 growth and ectomycorrhizal development of loblolly pine seedlings in fumigated soil infested with the fungal symbiont Pisolithus tinctorius. For. Res. 21, 245-254.Google Scholar
  68. Mayer A M and Harel E 1979 Polyphenol oxidases in plants. Phytochem. 18, 193-215.Google Scholar
  69. Michelsen A, Schmidt I K, Jonasson S, Quarmby C and Sleep D 1996 Leaf 15N abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non-and arbuscular mycorrhizal species access different sources of soil nitrogen. Oecologia 105, 53-63.Google Scholar
  70. Miki K, Renganathan V and Gold M 1986 Mechanisms of β-aryl ether dimeric lignin model compound oxidation by lignin peroxidase of Phanerochaete chrysosporium. Biochem. 25, 4790-4796.Google Scholar
  71. Mitchell D T, Sweeney M and Kennedy A 1992 Chitin degradation by Hymenoscyphus ericae and the influence of H. ericae on the growth of ectomycorrhizal fungi. In Mycorrhizas in ecosystems, Eds. I J Alexander, A H Fitter, D H Lewis and D J Read. pp 246-251, CAB International, London.Google Scholar
  72. Mitchell D T and Read D J 1981 Utilization of inorganic and organic phosphates by the mycorrhizal endophytes of Vaccinium macrocarpon and Rhododendron ponticum. Trans. Br. Mycol. Soc. 76, 255-260.Google Scholar
  73. Myers M D and Leake J R 1996 Phosphodiesters as mycorrhizal P sources. II. Ericoid mycorrhiza and the utilization of nuclei as a phosphorus source by Vaccinium macrocarpon. New Phytol. 132, 445-451.Google Scholar
  74. Ono K, Shintani K, Shigati S and Oka S 1988 Various molecular species of glucoamylase from Aspergillus niger. Agric. Biol. Chem. 52, 1689-1698.Google Scholar
  75. Pearson V and Read, D J 1975 The physiology of the mycorrhizal endophyte of Calluna vulgaris. Trans. Br. Mycol. Soc. 64, 1-7.Google Scholar
  76. Perotto S, Actis-Perino E, Perugini J and Bonfante P 1996 Molecular diversity of fungi from ericoid mycorrhizal roots. Molec. Ecol. 5, 123-131.Google Scholar
  77. Perotto S, Coisson J D, Perugini I, Cometti V and Bonfante P 1997 Production of pectin-degrading enzymes by ericoid mycorrhizal fungi. New Phytol. 135, 151-162.Google Scholar
  78. Perotto S, Peretto R, Faccio A, Schubert A, Varma A and Bonfante P 1995 Ericoid mycorrhizal fungi: cellular and molecular bases of their interactions with the host plant. Can. J. Bot. 73Suppl. 2, S557-S568.Google Scholar
  79. Perotto S, Peretto R, Moré D and Bonfante P 1990 Ericoid fungal strains from an alpine zone: their cytological and cell surface characteristics. Symbiosis 9, 167-172.Google Scholar
  80. Puls J and Schuseil J 1993 Chemistry of hemicelluloses: relationship between hemicellulose structure and the enzymes required for hydrolysis. In Hemicelluloses and hemicellulases, Eds. M P Coughlan and G P Hazelwood. pp 1-28. Portland Press, London.Google Scholar
  81. Read D J 1991 Mycorrhizas in ecosystems. Experientia 47, 376-390.Google Scholar
  82. Read D J 1992 The mycorrhizal mycelium. In Mycorrhizal functioning, Ed. M F Allen. pp 102-133. Chapman and Hall, New York.Google Scholar
  83. Read D J, Leake J R and Langdale A R 1989 The nitrogen nutrition of mycorrhizal fungi and their host plants. In Nitrogen, phosphorus and sulphur utilization by fungi, Eds. L Boddy, R Marchant and D J Read. pp 181-204. Cambridge University Press, Cambridge.Google Scholar
  84. Renganathan V and Gold M H 1986 Spectral characterization of the oxidised ststes of lignin peroxidase, an extracellular heme enzyme from the white rot basidiomycete Phanerochaete chrysosporium. Biochem. 25, 1626-1631.Google Scholar
  85. Shaw G and Read D J 1989 The biology of mycorrhiza in the Ericaceae. XIV. Effects of iron and aluminium on the activity of acid phosphatase in the ericoid endophyte Hymenoscyphus ericae (Read) Korf and Kernan. New Phytol. 113, 529-533.Google Scholar
  86. Sjoblad R D, Bollag J-M 1981 Oxidative coupling of aromatic compounds by enzymes from soil microorganisms. In Soil biochemistry volume 5, Eds. E A Paul and J N Ladd. pp 113-152. Marcel Dekker, New York.Google Scholar
  87. Smith S E and Read D J 1997 Mycorrhizal symbiosis. Academic Press, London.Google Scholar
  88. Specht R L and Rundel P W 1990 Sclerophylly and foliar nutrient status of mediterranean-climate plant communities in southern Australia. Aust. J. Bot. 38, 459-474.Google Scholar
  89. Steinke E, Williams P G and Ashford A E 1996 The structure and fungal associates of mycorrhizas in Leucopogon parviflorus (Andr.) Lindl. Ann. Bot. 77, 413-419.Google Scholar
  90. Stoyke G and Currah R S 1991 Endophytic fungi from the mycorrhizae of alpine eicoid plants. Can. J. Bot. 69, 347-352.Google Scholar
  91. Straker C J 1996 Ericoid mycorrhiza: ecological and host specificity. Mycorrhiza 6, 215-225.Google Scholar
  92. Straker C J, Gianinazzi-Pearson V, Gianinazzi S, Cleyet-Marel J-C and Bousquet N 1989 Electrophoretic and immunological studies on acid phosphatase from a mycorrhizal fungus Erica hispidula L. New Phytol. 111, 215-221.Google Scholar
  93. Straker C J and Mitchell D T 1986 The activity and characterization of acid phosphatase in endomycorrhizal fungi of the Ericaceae. New Phytol. 104, 243-256.Google Scholar
  94. Straker C J, Schnippenkoetter W H and Lemoine M-C 1992 Analysis of acid invertase and comparison with acid phosphatase in the ericoid mycorrhizal fungus Hymenoscyphus ericae (Read) Korf and Kernan. Mycorrhiza 2, 63-67.Google Scholar
  95. Suominen P and Reinikainen T 1993 Trichoderma reesii cellulases and other hydrolases. Foundation for Biotechnical and Industrial Fermentation Reseach, Helsinki.Google Scholar
  96. Suurnäkki A, Tenkanen M, Buchert J and Viikari L 1997 Hemicellulases in the bleaching of chemical pulps. In Advances in biochemical engineering biotechnology Vol. 57. Biotechnology in the pulp and paper industry. Ed. K-E L Eriksson. pp 261-287. Springer, Berlin.Google Scholar
  97. Varma A and Bonfante P 1994 Utilization of cell-wall related carbohydrates by ericoid mycorrhizal endophytes. Symbiosis 16, 301-313.Google Scholar
  98. Wariishi H, Dunford H B, Macdonald I D and Gold M H 1989 Manganese peroxidase from the lignin-degrading basidiomycete Phanerochaete chrysosporium: transient state kinetics and rection mechanism. J. Biol. Chem. 264, 3335-3340.Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • J.W.G. Cairney
    • 1
  • R. M. Burke
    • 2
  1. 1.Mycorrhiza Research Group, School of ScienceUniversity of Western SydneyKingswoodAustralia
  2. 2.Department of Biomolecular SciencesUMISTManchesterUK

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