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Defoliation effects on enzyme activities of the ectomycorrhizal fungus Suillus granulatus in a Pinus contorta (lodgepole pine) stand in Yellowstone National Park

  • Ecosystem Ecology - Original Paper
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Abstract

Ectomycorrhizal (EM) basidiomycete fungi are obligate mutualists of pines and hardwoods that receive fixed C from the host tree. Though they often share most recent common ancestors with wood-rotting fungi, it is unclear to what extent EM fungi retain the ability to express enzymes that break down woody substrates. In this study, we tested the hypothesis that the dominant EM fungus in a pure pine system retains the ability to produce enzymes that break down woody substrates in a natural setting, and that this ability is inducible by reduction of host photosynthetic potential via partial defoliation. To achieve this, pines in replicate blocks were defoliated 50% by needle removal, and enzyme activities were measured in individual EM root tips that had been treated with antibiotics to prevent possible bacterial activity. Results indicate that the dominant EM fungal species (Suillus granulatus) expressed all enzymes tested (endocellulase D-glucosidase, laccase, manganese peroxidase, lignin peroxidase, phosphatase and protease), and that activities of these enzymes increased significantly (P < 0.001) in response to defoliation. Thus, this EM fungus (one of the more specialized mutualists of pine) has the potential to play a significant role in C, N and P cycling in this forested ecosystem. Therefore, many above-ground factors that reduce photosynthetic potential or divert fixed C from roots may have wide-reaching ecosystem effects.

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References

  • Agerer R, Schloter M, Hahn C (2000) Fungal enzymatic activity in fruitbodies. Nova Hedwigia 71:315–336

    Google Scholar 

  • Antibus RK, Sinsabaugh RL, Linkins AE (1992) Phosphatase activities and phosphorous uptake from inositol phosphate by ectomycorrhizal fungi. Can J Bot 70:794–801

    CAS  Google Scholar 

  • Bendig GD, Read DJ (1995) The structure and function of the vegetative mycelium of ectomycorrhizal plants. V. Foraging behavior and translocation of nutrients from exploited litter. New Phytol 130:401–409

    Article  Google Scholar 

  • Bendig GD, Read DJ (1997) Lignin and soluble phenolic degredation by ectomycorrhizal and ericoid mycorrhizal fungi. Mycol Res 101:1348–1354

    Article  Google Scholar 

  • Berntson GM, Bazzaz FA (1997) Regenerating temperate forest mesocosms in elevated CO2: belowground growth and nitrogen cycling. Oecologia 113:115–125

    Article  Google Scholar 

  • Bonello P, Pearce RB (1993) Biochemical defense responses in primary roots of Scots pine challenged in vitro with Cylindrocarpon destructans. Plant Pathol 42:203–211

    Article  CAS  Google Scholar 

  • Brandrud TE (1995) The effects of experimental nitrogen addition on the ectomycorrhizal fungus flora in an oligotrophic spruce forest at Gardsjon, Sweden. For Ecol Manage 71:111–122

    Article  Google Scholar 

  • Burke RM, Carney JWG (2002) Laccases and other polyphenol oxidases in ecto- and ericoid mycorrhizal fungi. Mycorrhiza 12:105–116

    PubMed  CAS  Google Scholar 

  • Chalot M, Brun A (1998) Physiology of organic nitrogen acquisitioin by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol Rev 22:21–44

    Article  PubMed  CAS  Google Scholar 

  • Colpaert JV, Van Laere A (1996) A comparison of the extracellular enzyme activities of two ectomycorrhizal and a leaf-saprophytic basidiomycetes colonizing beech leaf litter. New Phytol 133:133–141

    Article  Google Scholar 

  • Colpaert JW, Van Tichelen KK (1996) Decomposition, nitrogen and phosphorous mineralization from beech leaf litter colonized by ectomycorrhizal or litter-decomposing basidiomycetes. New Phytol 134:123–132

    Article  Google Scholar 

  • Conn C, Dighton J (2000) Litter quality influences on decomposition, ectomycorrhizal community structure and mycorrhizal root surface acid phosphatase activity. Soil Biol Biochem 32:489–496

    Article  CAS  Google Scholar 

  • Courty P-E, Breda N, Garbaye J (2007) Relation between oak tree phenology and the secretion of organic matter degrading enzymes by Lactarius quietus ectomycorrhzas before and during bud break. Soil Biol Biochem 39:1655–1663

    Article  CAS  Google Scholar 

  • Cullings KW, Szaro TM, Bruns TD (1996) Evolution of extreme specialization within a lineage of ectomycorrhizal epiparasites. Nature 379:63–66

    Article  CAS  Google Scholar 

  • Cullings KW, Vogler DR, Parker VT, Makhija S (2001) Defoliation effects on the ectomycorrhizal community of a mixed Pinus contorta/Picea engelmannii stand in Yellowstone Park. Oecologia 127:533–539

    Article  Google Scholar 

  • Cullings KW, New MH, Makhija S, Parker VT (2003) Effects of litter addition on the ectomycorrhizal associates of a lodgepole pine (Pinus contorta) stand in Yellowstone National Park. Appl Environ Microbiol 69:3772–3776

    Article  PubMed  CAS  Google Scholar 

  • Cullings KW, Raleigh C, Vogler DR (2005) Effects of severe dwarf mistletoe infection on the ectomycorrhizal community of lodgepole pine in Yellowstone Park. Can J Bot 83:1174–1180

    Article  Google Scholar 

  • Cumming JR (1996) Phosphate-limitation physiology in ectomycorrhizal pitch pine (Pinus rigida) seedlings. Tree Physiol 16:977–983

    PubMed  Google Scholar 

  • Dass SB, Dosoretz CG, Reddy CA, Grethlein HE (1995) Extracellular proteases produced by the wood-degrading fungus Phanerochaete chrysosporium under ligninolytic and non-ligninolytic conditions. Arch Microbiol 163:254–258

    Article  PubMed  CAS  Google Scholar 

  • De Souza CGM, Tychanowicz GV, De Souza F, Peralta RM (2004) Production of laccase isoforms by Pleurotus pulmonarius in response to presence of phenolic and aromatic compounds. J Basic Microbiol 44:129–136

    Article  PubMed  CAS  Google Scholar 

  • Del Vecchio TA, Gehring CA, Cobb NS, Whitham TG (1993) Negative effects of scale insect herbivory on the ectomycorrhizae of juvenile Pinyon pine. Ecology 74:2297–2302

    Article  Google Scholar 

  • Durrall DM, Todd AW, Trappe JM (1994) Decomposition of 14C-labeled substrates by ectomycorrhizal fungi in association with Douglas-fir. New Phytol 127:725–729

    Article  Google Scholar 

  • Entry JA, Donnelley PK, Cromack K (1991) Influence of ectomycorrhizal mat soils on lignin and cellulose degradation. Biol Fertil Soils 11:75–78

    Article  CAS  Google Scholar 

  • Fields R (1972) The rapid determination of amino groups with TNBS. Methods Enzymol 25:464–468

    Article  CAS  Google Scholar 

  • Gehring CA, Whitham TG (1994) Comparisons of ectomycorrhizae on pinyon pines (Pinus edulis; Pinaceae) across extremes of soil type and herbivory. Am J Bot 81:1509–1516

    Article  Google Scholar 

  • Gehring CA, Whitham TG (1995) Duration of herbivore removal and environmental stress affect the ectomycorrhizae of Pinyon pines. Ecology 76(7):2118–2123

    Article  Google Scholar 

  • Godbold D, Berntson GM, Bazzaz FA (1997) Growth and mycorrhizal colonization of three North American tree species under elevated atmospheric CO2. New Phytol 137:433–440

    Article  CAS  Google Scholar 

  • Gold MH, Alic M (1993) Molecular biology of the lignin-degrading basidiomycetes Phanerochaete chrysosporium. Microbiol Rev 57:605–622

    PubMed  CAS  Google Scholar 

  • Gramss G, Günther TH, Fritsche W (1998) Spot tests for oxidative enzymes in ectomycorrhizal, wood and litter decaying fungi. Mycol Res 102:67–72

    Article  CAS  Google Scholar 

  • Günther TH, Perner B, Gramss G (1998) Activities of phenol oxidizing enzymes of ectomycorrhizal fungi in axenic culture and in symbiosis with Scots pine (Pinus sylvestris L.). J Basic Microbiol 38:197–206

    Article  Google Scholar 

  • Haselwandter K, Bobleter O, Read DJ (1990) Degredation of 14C-labeled lignin and dehydropolymer of coniferyl alcohol by ericoid and ectomycorrhizal fungi. Arch Microbiol 153:352–354

    Article  CAS  Google Scholar 

  • Hering TF (1982) Decomposing activity of basidiomycetes in forest litter. In: Frankland JC, Hedger JN, Swift MJ (eds) Decomposer basidiomycetes: their biology and ecology. Cambridge University Press, Cambridge, pp 213–225

    Google Scholar 

  • Hibbett DS, Gilbert L-B, Donoghue MJ (2000) Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407:506–508

    Article  PubMed  CAS  Google Scholar 

  • Hummell KM, Inselman A, Ramos ER, Gathman AC, Lilly WW (1998) Extracellular protease production by submerged cultures of Schizophyllmu commune. Mycologia 90:883–889

    Article  Google Scholar 

  • Kjöller A (2006) Disproportionate abundance between ectomycorrhizal root tips and their associated mycelia. FEMS Microbiol Ecol 58:214–224

    Article  PubMed  CAS  Google Scholar 

  • Kjöller A, Struwe S (2002) Enzymes in the environment. Activity, ecology and applications. Dekker, New York

    Google Scholar 

  • Luis P, Walther G, Kellner H, Martin F, Buscot F (2004) Diversity of laccase genes from basidiomycetes in a forest soil. Soil Biol Biochem 36:1025–1036

    Article  CAS  Google Scholar 

  • Markkola AM (1996) Effect of artificial defoliation on biomass allocation ectomycorrhizal Pinus sylvestris seedlings. Can J For 26:899–904

    Google Scholar 

  • Martin F, Delaruelle C, Hilbert JL (1990) An improved ergosterol assay to estimate fungal biomass in ectomycorrhizas. Mycol Res 94:1059–1064

    Article  Google Scholar 

  • Molina R, Massicotte J, Trappe JM (1992) Specificity phenomena in mycorrhizal symbioses: Community ecological consequences and practical applications. In: Allen A (ed) Mycorrhizal functioning. Chapman and Hall, New York, pp 357–420

    Google Scholar 

  • Moorhead DL, Linkins AE (1997) Elevated CO2 alters belowground exoenzyme activities in tussock tundra. Plant Soil 189:321–329

    Article  CAS  Google Scholar 

  • Pritsch KS, Raidl E, Markensteiner H, Blashcke Agerer R, Schloter M, Hartmann A (2004) A rapid and highly sensitive method for measuring enzyme activities in single mycorrhizal tips using 4-methylumbelliferone-labeled fluorogenic substrates in a mciroplate system. J Microbiol Methods 58:233–241

    Article  PubMed  CAS  Google Scholar 

  • Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391

    Article  Google Scholar 

  • Redlak KH, Dahm H, Ciesielska A, Strezelczyk E (2001) Enzymatic activity of ectendomycorrhizal fungi. Biol Fertil Soils 33:83–90

    Article  CAS  Google Scholar 

  • Rossow LJ, Bryant JP, Kielland K (1997) Effects of above-ground browsing by mammals on mycorrhizal infection in an early sucessional taiga ecosystem. Oecologia 110:94–98

    Article  Google Scholar 

  • Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R (1998) Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579–582

    Article  CAS  Google Scholar 

  • Sinsabaugh R, Antibus R, Linkins A, McClaugherty AC, Rayburn L, Repert D, Weiland T (1993) Wood decomposition: nitrogen and phosphorus dynamics in relation to extracellular enzyme activity. Ecology 74:1586–1593

    Article  CAS  Google Scholar 

  • Sundari SK, Adholeya A (2000) Retention of enzyme activity following freeze-drying the mycelium of ectomycorrhizal isolates. Part II. Enzymes acting upon carbon compounds. World J Microbiol 16:865–868

    Article  CAS  Google Scholar 

  • Tabatabai MA, Bremner JM (1969) Use of p-nitrophenol phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

    Article  CAS  Google Scholar 

  • Taylor TN, Taylor EL (1997) The distribution and interactions of some Paleozoic fungi. Rev Paleobot Palynol 95:83–94

    Article  Google Scholar 

  • Tibbett M, Sanders FE, Cairney JWG, Leake JR (1999) Temperature regulation of extracellular proteases in ectomycorrhizal fungi (Hebeloma spp.) grown in axenic culture. Mycol Res 103:707–714

    Article  Google Scholar 

  • Timonen S, Sen R (1998) Heterogeneity of fungal and plant enzyme expression in intact Scots pine-Suillus bovines and–Paxillus involutus mycorrhizaospheres developed in natural forest humus. New Phytol 138:355–366

    Article  Google Scholar 

  • Walker RF, Geisinger DR, Johnson DW, Ball JT (1997) Elevated atmospheric CO2 and soil N fertility effects on growth, mycorrhizal colonization, and xylem water potential of juvenile ponderosa pine in a field soil. Plant Soil 195:25–36

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by an NSF grant to Henson and Cullings (NSF Ecology 0211848). We thank the Yellowstone Center for Resources for logistical support.

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Correspondence to Ken Cullings.

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Communicated by Zoe Cardon.

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Cullings, K., Ishkhanova, G. & Henson, J. Defoliation effects on enzyme activities of the ectomycorrhizal fungus Suillus granulatus in a Pinus contorta (lodgepole pine) stand in Yellowstone National Park. Oecologia 158, 77–83 (2008). https://doi.org/10.1007/s00442-008-1119-6

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