Ectomycorrhizal fungal hyphae communities vary more along a pH and nitrogen gradient than between decayed wood and mineral soil microsites

Botany

Volumn 92, Issue 6, 2014, Pages 453-463

  Walker, Jennifer K M ^a,b   Phillips, Lori A ^a,c   Jones, Melanie D ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b WESTERN SYDNEY UNIVERSITY   (Australia)

^c LA TROBE UNIVERSITY   (Australia)

Author keywords

Ectomycorrhizal ecology; Forest soil; Fungal hyphae; Next generation sequencing; Picea engelmannii

Indexed keywords

COMMUNITY COMPOSITION; FOREST SOIL; FUNGUS; MINERAL; NITROGEN; NUTRIENT CYCLING; PH; SPECIALIZATION;

BRITISH COLUMBIA; CANADA;

EID: 84901437586     PISSN: 19162804     EISSN: None     Source Type: Journal    
DOI: 10.1139/cjb-2013-0239     Document Type: Article

References (99)

1. Agerer, R. 2001. Exploration types of ectomycorrhizae: a proposal to classify ectomycorrhizal mycelial systems according to their pattern of differentiation and putative ecological importance. Mycorrhiza, 11(2): 107-114. doi:10. 1007/s005720100108.
2. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J.H., Zhang, Z., Miller, W., and Lipman, D.J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25(17): 3389-3402. doi:10.1093/ nar/25.17.3389. PMID:9254694.
3. Amend, A.S., Seifert, K.A., and Bruns, T.D. 2010. Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol. Ecol. 19(24): 5555-5565. doi:10.1111/j.1365-294X.2010.04898.x. PMID:21050295.
4. Anderson, I.C., and Cairney, J.W.G. 2007. Ectomycorrhizal fungi: exploring the mycelial frontier. FEMS Microbiol. Rev. 31(4): 388-406. doi:10.1111/j.1574-6976. 2007.00073.x. PMID:17466031.
5. Arocena, J.M., Glowa, K.R., Massicotte, H.B., and Lavkulich, L. 1999. Chemical and mineral composition of ectomycorrhizosphere soils of subalpine fir (Abies lasiocarpa (Hook.) Nutt.) in the Ae horizon of a Luvisol. Can. J. Soil Sci. 79(1): 25-35. doi:10.4141/S98-037.
6. Arocena, J.M., Glowa, K.R., and Massicotte, H.B. 2001. Calcium-rich hypha encrustations on Piloderma. Mycorrhiza, 10(5): 209-215. doi:10.1007/s005720000082.
7. Avis, P.G., and Charvat, I. 2005. The response of ectomycorrhizal fungal inoculum to long-term increases in nitrogen supply. Mycologia, 97(2): 329-337. doi:10.3852/mycologia.97.2.329. PMID:16396340.
8. Baier, R., Ingenhaag, J., Blaschke, H., Göttlein, A., and Agerer, R. 2006. Vertical distribution of an ectomycorrhizal community in upper soil horizons of a young Norway spruce (Picea abies [L.] Karst.) stand of the Bavarian Limestone Alps. Mycorrhiza, 16(3): 197-206. doi:10.1007/s00572-006-0035-z.
9. Blackwell, M. 2011. The fungi: 1, 2, 3. 5.1 million species? Am. J. Bot. 98(3): 426-438. doi:10.3732/ajb.1000298. PMID:21613136.
10. Bruns, T.D. 1995. Thoughts on the processes that maintain local species diversity of ectomycorrhizal fungi. Plant Soil, 170: 63-73. doi:10.1007/BF02183055.
11. Buée, M., Courty, P.-E., Mignot, D., and Garbaye, J. 2007. Soil niche effect on species diversity and catabolic activities in an ectomycorrhizal fungal community. Soil Biol. Biochem. 39(8): 1947-1955. doi:10.1016/j.soilbio.2007.02.016.
12. Buée, M., Reich, M., Murat, C., Morin, E., Nilsson, R.H., Uroz, S., and Martin, F. 2009. 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol. 184: 449-456. doi:10.1111/j.1469-8137.2009. 03003.x. PMID:19703112.
13. Carlile, M.J., Watkinson, S.C., and Gooday, G.W. 2001. The fungi. 2nd ed. Academic Press, London.
14. Christy, E.J., Sollins, P., and Trappe, J.M. 1982. First-year survival of Tsuga heterophylla without mycorrhizae and subsequent ectomycorrhizal development on decaying logs and mineral soil. Can. J. Bot. 60(9): 1601-1605. doi:10. 1139/b82-206.
15. Clemmensen, K.E., Bahr, A., Ovaskainen, O., Dahlberg, A., Ekblad, A., Wallander, H., Stenlid, J., Finlay, R.D., Wardle, D.A., and Lindahl, B.D. 2013. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science, 339(6127): 1615-1618. doi:10.1126/science.1231923. PMID: 23539604.
16. Cox, F., Barsoum, N., Lilleskov, E.A., and Bidartondo, M.I. 2010. Nitrogen availability is a primary determinant of conifer mycorrhizas across complex environmental gradients. Ecol. Lett. 13(9): 1103-1113. doi:10.1111/j.1461-0248.2010. 01494.x. PMID:20545731.
17. Craig, V.J., Klenner, W., Feller, M.C., and Sullivan, T.P. 2006. Relationships between deer mice and downed wood in managed forests of southern British Columbia. Can. J. For. Res. 36(9): 2189-2203. doi:10.1139/x06-118.
18. Cullings, K., and Courty, P.-E. 2009. Saprotrophic capabilities as functional traits to study functional diversity and resilience of ectomycorrhizal community. Oecologia, 161(4): 661-664. doi:10.1007/s00442-009-1434-6.
19. Dahlberg, A. 2001. Community ecology of ectomycorhizal fungi: an advancing interdisciplinary field. New Phytol. 150(3): 552-562. doi:10.1046/j.1469-8137. 2001.00142.x.
20. Day, M.J., and Currah, R.S. 2011. Role of selected dark septate endophyte species and other hyphomycetes as saprobes on moss gametophytes. Botany, 89(5): 349-359. doi:10.1139/b11-023.
21. Dickie, I.A. 2007. Host preference, niches, and fungal diversity. New Phytol. 174(2): 230-233. doi:10.1111/j.1469-8137.2007.02055.x.
22. Dickie, I.A. 2010. Insidious effects of sequencing errors on perceived diversity in molecular surveys. New Phytol. 188(4): 916-918. doi:10.1111/j.1469-8137.2010. 03473.x. PMID:20854395.
23. Elliott, J.C., Smith, J.E., Cromack, K., Jr., Chen, H., and McKay, D. 2007. Chemistry and ectomycorrhizal communities of coarse wood in young and old-growth forests in the Cascade Range of Oregon. Can. J. For. Res. 37(10): 2041-2051. doi:10.1139/X07-014.
24. Finlay, R.D. 2008. Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J. Exp. Bot. 59(5): 1115-1126. doi:10.1093/jxb/ern059. PMID:18349054.
25. Finlay, R.D., and Read, D.J. 1986. The structure and function of the vegetative mycelium of ectomycorrhizal plants. 1. Translocation of 14C-labelled carbon between plants interconnected by a common mycelium. New Phytol. 103(1): 143-156 doi:10.1111/j.1469-8137.1986.tb00603.x.
26. Fukami, T., Dickie, I.A., Wilkie, J.P., Paulus, B.C., Park, D., Roberts, A., Buchanan, P.K., and Allen, R.B. 2010. Assembly history dictates ecosystem functioning: evidence from wood decomposer communities. Ecol. Lett. 13(6): 675-684. doi:10.1111/j.1461-0248.2010.01465.x. PMID:20412280.
27. Gardes, M., and Bruns, T.D. 1993. ITS primers with enhanced specificity for Basidiomycetes-application to the identification of mycorrhizae and rusts. Mol. Ecol. 2(2): 113-118. doi:10.1111/j.1365-294X.1993.tb00005.x. PMID:8180733.
28. Genney, D.R., Anderson, I.C., and Alexander, I.J. 2006. Fine-scale distribution of pine ectomycorrhizas and their extramatrical mycelium. New Phytol. 170(2): 381-390. doi:10.1111/j.1469-8137.2006.01669.x. PMID:16608462.
29. Goodman, D.M., and Trofymow, J.A. 1998. Distribution of ectomycorrhizas in microhabitats in mature and old-growth stands of Douglas-fir on southeastern Vancouver Island. Soil Biol. Biochem. 30(14): 2127-2138. doi:10.1016/S0038-0717(98)00094-7.
30. Grelet, G.-A., Johnson, D., Vrålstad, T., Alexander, I.J., and Anderson, I.C. 2010. New insights into the mycorrhizal Rhizoscyphus ericae aggregate: spatial structure and co-colonization of ectomycorrhizal and ericoid roots. New Phytol. 188(1): 210-222. doi:10.1111/j.1469-8137.2010.03353.x. PMID:20618909.
31. Hartmann, M., Howes, C.G., VanInsberghe, D., Yu, H., Bachar, D., Christen, R., Nilsson, R.E., Hallam, S.J., and Mohn, W.W. 2012. Significant and persistent impact of timber harvesting on soil microbial communities in Northern coniferous forests. ISME J. 6(12): 2199-2218. doi:10.1038/ismej.2012.84. PMID: 22855212.
32. Harvey, A.E., Larsen, M.J., and Jurgensen, M.F. 1979. Comparative distribution of ectomycorrhizae in soils of three western Montana forest habitat types. For. Sci. 25(2): 350-358.
33. Hibbett, D.S., Ohman, A., and Kirk, P.M. 2009. Fungal ecology catches fire. New Phytol. 184(2): 279-282. doi:10.1111/j.1469-8137.2009.03042.x. PMID:19796334.
34. Hoffland, E., Kuyper, T.W., Wallander, H., Plassard, C., Gorbushina, A.A., Haselwandter, K., Holmström, S., Landeweert, R., Lundström, U.S., Rosling, A., Sen, R., Smits, M.M., van Hees, P.A.W., and van Breemen, N. 2004. The role of fungi in weathering. Front. Ecol. Environ. 2(5): 258-264. doi:10. 1890/1540-9295(2004)002[0258:TROFIW]2.0.CO;2.
35. Hollstedt, C., and Vyse, A. (Editors). 1997. Sicamous Creek Silvicultural Systems Project: Workshop Proceedings, April 24-25, 1996. Kamloops, British Columbia. Work Pap. 24/1997. Res. Br., B.C. Min. For., Victoria, B.C., Canada.
36. Hortal, S., Trocha, L.K., Murat, C., Chybicki, I.J., Buée, M., Trojankiewicz, M., Burczyk, J., and Martin, F. 2012. Beech roots are simultaneously colonized by multiple genets of the ectomycorrhizal fungus Laccaria amethystina clustered in two genetic groups. Mol. Ecol. 21(9): 2116-2129. doi:10.1111/j.1365-294X.2012. 05515.x. PMID:22429247.
37. Horton, T.R., and Bruns, T.D. 2001. The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Mol. Ecol. 10(8): 1855-1871. doi:10.1046/ j.0962-1083.2001.01333.x.
38. Huson, D.H., Auch, A.F., Qi, J., and Schuster, S.C. 2007. MEGAN analysis of metagenomic data. Genome Res. 17: 377-386. doi:10.1101/gr.5969107. PMID: 17255551.
39. Iwański, M., and Rudawska, M. 2007. Ectomycorrhizal colonization of naturally regenerating Pinus sylvestris L. seedlings growing in micro-habitats in boreal forests. Mycorrhiza, 17(5): 461-467. doi:10.1007/s00572-007-0132-7. PMID: 17503091.
40. Izzo, A., Agbowo, J.A., and Bruns, T.D. 2005. Detection of plot-level changes in ectomycorrhizal communities across years in an old-growth mixed-conifer forest. New Phytol. 166(2): 619-630. doi:10.1111/j.1469-8137.2005.01354.x. PMID:15819924.
41. Izzo, A., Nguyen, D.T., and Bruns, T.D. 2006. Spatial structure and richness of ectomycorrhizal fungi colonizing bioassay seedlings from resistant propagules in a Sierra Nevada forest: comparisons using two hosts that exhibit different seedling establishment patterns. Mycologia, 98(3): 374-383. doi:10. 3852/mycologia.98.3.374. PMID:17040066.
42. Jones, M.D., Durall, D.M., and Tinker, P.B. 1991. Fluxes of carbon and phosphorus between symbionts in willow ectomycorrhizas and their changes with time. New. Phytol. 119(1): 99-106. doi:10.1111/j.1469-8137.1991.tb01012.x.
43. Jones, M.D., Durall, D.M., and Cairney, J.W.G. 2003. Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging. New Phytol. 157(3): 399-422. doi:10.1046/j.1469-8137.2003.00698.x.
44. Jones, M.D., Grenon, F., Peat, H., Fitzgerald, M., Holt, L., Philip, L.J., and Bradley, R. 2009. Differences in 15N uptake amongst spruce seedlings colonized by three pioneer ectomycorrhizal fungi in the field. Fungal Ecol. 2(3): 110-120. doi:10.1016/j.funeco.2009.02.002.
45. Jones, M.D., Phillips, L.A., Treu, R., Ward, V., and Berch, S. 2012. Functional responses of ectomycorrhizal fungal communities to long-term fertilization of lodgepole pine (Pinus contorta Dougl. ex Loud. var. latifolia Engelm.) stands in central British Columbia. Appl. Soil Ecol. 60: 29-40. doi.org/10.1016/j. apsoil.2012.01.010.
46. Jumpponen, A., and Jones, K.L. 2009. Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol. 184(2): 438-448. doi:10.1111/j.1469-8137.2009.02990.x. PMID:19674337.
47. Katoh, K., Misawa, K., Kuma, K., and Miyata, T. 2002. Mafft: A novel method for rapid multiple sequence alignment based on fast fourier transform. Nucleic Acids Res. 30(14): 3059-3066. doi:10.1093/nar/gkf436. PMID:12136088.
48. Kauserud, H., Kumar, S., Brysting, A.K., Nordén, J., and Carlsen, T. 2012. High consistency between replicate 454 pyrosequencing analyses of ectomycorrhizal plant root samples. Mycorrhiza, 22(4): 309-315. doi:10.1007/s00572-011-0403-1. PMID:21779811.
49. Kjøller, R. 2006. Disproportionate abundance between ectomycorrhizal root tips and their associated mycelia. FEMS Microbiol. Ecol. 58(2): 214-224. doi:10.1111/ j.1574-6941.2006.00166.x. PMID:17064263.
50. Koide, R.T., Fernandez, C., and Petprakob, K. 2011. General principles in the community ecology of ectomycorrhizal fungi. Ann. For. Sci. 68(1): 45-55. doi:10.1007/s13595-010-0006-6.
51. Kranabetter, J.M., Durall, D.M., and MacKenzie, W.H. 2009. Diversity and species distribution of ectomycorrhizal fungi along productivity gradients of a southern boreal forest. Mycorrhiza, 19(2): 99-111. doi:10.1007/s00572-008-0208-z. PMID:18941804.
52. Kunin, V., Engelbrektson, A., Ochman, H., and Hugenholtz, P. 2010. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ. Microbiol. 12(1): 118-123. doi:10.1111/j.1462-2920. 2009.02051.x. PMID:19725865.
53. Landeweert, R., Leeflang, P., Kuyper, T.W., Hoffland, E., Rosling, A., Wernars, K., and Smit, E. 2003. Molecular identification of ectomycorrhizal mycelium in soil horizons. Appl. Environ. Microbiol. 69(1): 327-333. doi:10.1128/AEM.69.1. 327-333.2003. PMID:12514012.
54. Lilleskov, E.A., Fahey, T.J., Horton, T.R., and Lovett, G.M. 2002. Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology, 83(1): 104-115. doi:10.1890/0012-9658(2002)083[0104: BEFCCO]2.0.CO;2.
55. Lilleskov, E.A., Bruns, T.D., Horton, T.R., Taylor, D.L., and Grogan, P. 2004. Detection of forest stand-level spatial structure in ectomycorrhizal fungal communities. FEMS Microbiol. Ecol. 49(2): 319-332. doi:10.1016/j.femsec.2004.04. 004. PMID:19712424.
56. Lindahl, B.D., Ihrmark, K., Boberg, J., Trumbore, S.E., Högberg, P., Stenlid, J., and Finlay, R.D. 2007. Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol. 173(3): 611-620. doi:10.1111/j. 1469-8137.2006.01936.x. PMID:17244056.
57. Lindahl, B.D., Nilsson, R.H., Tedersoo, L., Abarenkov, K., Carlsen, T., Kjøller, R., Kõljalg, U., Pennanen, T., Rosendahl, S., Stenlid, J., and Kauserud, H. 2013. Fungal community analysis by high-throughput sequencing of amplified markers: a user's guide. New Phytol. 199(1): 288-299. doi:10.1111/nph.12243. PMID:23534863.
58. Lloyd, D., and Inselberg, A. 1997. Ecosystem mapping for the Sicamous Creek Silvicultural System Research Site. In Sicamous Creek Silvicultural Systems Project: Workshop Proceedings, April 24-25, 1996, Kamloops, British Columbia. Work. Pap. 24/1997. Edited by C. Hollstedt and A. Vyse. Res. Br., B.C. Min. For., Victoria, B.C.
59. Mello, A., Napoli, C., Murat, C., Morin, E., Marceddu, G., and Bonfante, P. 2011. ITS-1 versus ITS-2 pyrosequencing: a comparison of fungal populations in truffle grounds. Mycologia, 103(6): 1184-1193. doi:10.3852/11-027. PMID: 21700633.
60. Nilsson, L.O., Giesler, R., Bååth, E., and Wallander, H. 2005. Growth and biomass of mycorrhizal mycelia in coniferous forests along short natural nutrient gradients. New Phytol. 165(2): 613-622. doi:10.1111/j.1469-8137.2004.01223.x. PMID:15720671.
61. Nilsson, R.H., Ryberg, M., Kristiansson, E., Abarenkov, K., Larsson, K.-H., and Kõljalg, U. 2006. Taxonomic reliability of DNA sequences in public sequence databases: a fungal perspective. PLoS ONE, 1(1): 1-4. doi:10.1371/journal.pone. 0000059.
62. Nilsson, R.H., Bok, G., Ryberg, M., Kristiansson, E., and Hallenberg, N. 2009. A software pipeline for processing and identification of fungal ITS sequences. Source Code Biol. Med. 4(1): doi:10.1186/1751-0473-4-1. PMID:19146660.
63. Nilsson, R.H., Abarenkov, K., Veldre, V., Nylinder, S., DeWit, P., Brosché, S., Alfredsson, J.F., Ryberg, M., and Kristiansson, E. 2010a. An open source chimera checker for the fungal ITS region. Mol. Ecol. Resour. 10(6): 1076-1081. doi:10.1111/j.1755-0998.2010.02850.x. PMID:21565119.
64. Nilsson, R.H., Veldre, V., Hartmann, M., Unterseher, M., Amend, A., Bergsten, J., Kristiansson, E., Ryberg, M., Jumpponen, A., and Abarenkov, K. 2010b. An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high-throughput community assays and molecular ecology. Fungal Ecol. 3(4): 284-287. doi:10.1016/j.funeco.2010.05. 002.
65. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Henry, M., Stevens, H., and Wagner, H. 2012. vegan: Community Ecology Package. R package version 2.1. http://R-Forge.Rproject. org/projects/vegan/.
66. Ovaskainen, O., Nokso-Koivisto, J., Hottola, J., Rajala, T., Pennanen, T., Ali-Kovero, H., Miettinen, O., Oinonen, P., Auvinen, P., Paulin, L., Larsson, K.-H., and Mäkipää, R. 2010. Identifying wood-inhabiting fungi with 454 sequencing-what is the probability that BLAST gives the correct species? Fungal Ecol. 3(4): 274-283. doi:10.1016/j.funeco.2010.01.001.
67. Peay, K.G., Kennedy, P.G., and Bruns, T.D. 2008. Fungal community ecology: a hybrid beast with a molecular master. Bioscience, 58(9): 799-810. doi:10.1641/ B580907.
68. Peay, K.G., Garbelotto, M., and Bruns, T.D. 2010. Evidence of dispersal limitation in soil microorganisms: isolation reduces species richness on mycorrhizal tree islands. Ecology, 91(12): 3631-3640. doi:10.1890/09-2237.1. PMID:21302834.
69. Peay, K.G., Schubert, M.G., Nguyen, N.H., and Bruns, T.D. 2012. Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol. Ecol. 21(16): 4122-4136. doi:10.1111/j.1365-294X.2012. 05666.x. PMID:22703050.
70. Peterson, R.L., Wagg, C., and Pautler, M. 2008. Associations between microfungal endophytes and roots: do structural features indicate function? Botany, 86(5): 445-456. doi:10.1139/B08-016.
71. Phillips, L.A., Ward, V., and Jones, M.D. 2014. Ectomycorrhizal fungi contribute to soil organic matter cycling in sub-boreal forests. ISME J. 8: 699-713. doi: 10.1038/ismej.2013.195. PMID:24173458.
72. Pickles, B.J., Genney, D.R., Potts, J.M., Lennon, J.J., Anderson, I.C., and Alexander, I.J. 2010. Spatial and temporal ecology of Scots pine ectomycorrhizas. New Phytol. 186(3): 755-768. doi:10.1111/j.1469-8137.2010.03204.x. PMID:20202132.
73. R Core Team. 2012. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http:// www.R-project.org/.
74. Read, D.J., and Perez-Moreno, J. 2003. Mycorrhizas and nutrient cycling in ecosystems-a journey towards relevance? New Phytol. 157(3): 475-492. doi:10. 1046/j.1469-8137.2003.00704.x.
75. Reeder, J., and Knight, R. 2009. The 'rare biosphere': a reality check. Nat. Methods, 6: 636-637. doi:10.1038/nmeth0909-636.
76. Rosling, A., Landeweert, B.D., Lindahl, B.D., Larsson, K.-H., Kuyper, T.W., Taylor, A.F.S., and Finlay, R.D. 2003. Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytol. 159(3): 775-783. doi:10.1046/ j.1469-8137.2003.00829.x.
77. Rousk, J., Brookes, P.C., and Bååth, E. 2009. Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization Appl. Environ. Microbiol. 75(6): 1589-1596. doi:10.1128/AEM.02775-08.
78. Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., Sahl, J.W., Stres, B., Thallinger, G.G., Van Horn, D.J., and Weber, C.F. 2009. Introducing MOTHUR: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75(23): 7537-7541. doi:10.1128/AEM.01541-09. PMID:19801464.
79. Schulte, E.E., and Hopkins, B.G. 1996. Estimation of soil organic matter by weight loss-on-ignition. In Soil organic matter: analysis and interpretation. Edited by F.R. Magdiff, M.A. Tabatabai, and E.A. Hanlon. Soil Science Society of America, Madison, Wisc. pp. 21-31.
80. Siitonen, J. 2001. Forest management, coarse woody debris and saproxilic organisms: Fennoscandian boreal forests as an example. Ecol. Bull. 49: 11-41. http://www.jstor.org/stable/20113262.
81. Smith, J.E., Molina, R., Huso, M.M.P., and Larsen, M.J. 2000. Occurrence of Piloderma fallax in young, rotation-age, and old-growth stands of Douglas-fir (Pseudotsuga menziesii) in the Cascade Range of Oregon, U.S.A. Can. J. Bot. 78(8): 995-1001. doi:10.1139/b00-085.
82. Smith, S.E., and Read, D.J. 2008. Mycorrhizal symbiosis. 3rd ed. Academic Press, London.
83. Talbot, J.M., Allison, S.D., and Treseder, K.K. 2008. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct. Ecol. 22(6): 955-963. doi:10.1111/j.1365-2435.2008.01402.x.
84. Talbot, J.M., Bruns, T.D., Smith, D.P., Branco, S., Glassman, S.I., Erlandson, S., Vilgalys, R., and Peay, K.G. 2013 Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition. Soil Biol. Biochem. 57: 282-291. doi:10.1016/j.soilbio.2012.10.004
85. Tanesaka, E., Masuda, H., and Kinugawa, K. 1993. Wood degrading ability of basidiomycetes that are wood decomposers, litter decomposers, or mycorrhizal symbionts. Mycologia, 85(3): 347-354. doi:10.2307/3760693.
86. Taylor, D.L., Herriott, I.C., Stone, K.E., McFarland, J.W., Booth, M.G., and Leigh, M.B. 2010. Structure and resilience of fungal communities in Alaskan boreal forest soils. Can J. For. Res. 40(7): 1288-1301. doi:10.1139/X10-081.
87. Tedersoo, L., Kõljalg, U., Hallenberg, N., and Larsson, K.-H. 2003. Fine scale distribution of ectomycorrhizal fungi and roots across substrate layers including coarse woody debris in a mixed forest. New Phytol. 159(1): 153-165. doi:10.1046/j.1469-8137.2003.00792.x.
88. Tedersoo, L., Suvi, T., Jairus, T., and Kõljalg, U. 2008. Forest microsite effects on community composition of ectomycorrhizal fungi on seedlings of Picea abies and Betula pendula. Environ. Microbiol. 10(5): 1189-1201. doi:10.1111/j.1462-2920.2007.01535.x. PMID:18266759.
89. Tedersoo, L., May, T.W., and Smith, M.E. 2010a. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza, 20(4): 217-263. doi:10.1007/s00572-009-0274-x. PMID:20191371.
90. Tedersoo, L., Nilsson, R.H., Abarenkov, K., Jairus, T., Sadam, A., Saar, I., Bahram, M., Bechem, E., Chuyong, G., and Kõljalg, U. 2010b. 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol. 188(1): 291-301. doi:10.1111/j.1469-8137.2010.03373.x. PMID:20636324.
91. Toljander, J.F., Eberhardt, U., Toljander, Y.K., Paul, L.R., and Taylor, A.F.S. 2006. Species composition of an ectomycorrhizal fungal community along a local nutrient gradient in a boreal forest. New Phytol. 170(4): 873-884. doi:10.1111/ j.1469-8137.2006.01718.x. PMID:16684245.
92. Trofymow, J.A., Preston, C.M., and Prescott, C.E. 1995. Litter quality and its potential effect on decay rates of materials from Canadian forests. Water Air Soil Pollut. 82: 215-226. doi:10.1007/BF01182835.
93. Twieg, B.D., Durall, D.M., and Simard, S.W. 2007. Ectomycorrhizal fungal succession in mixed temperate forests. New Phytol. 176(2): 437-447. doi:10.1111/ j.1469-8137.2007.02173.x. PMID:17888121.
94. van der Heijden, M.G.A., Bardgett, R.D., and van Straalen, N.M. 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11(3): 296-310. doi:10.1111/j.1461-0248.2007.01139.x.
95. Walker, J.K.M., and Jones, M.D. 2013. Little evidence for niche partitioning among ectomycorrhizal fungi on spruce seedlings planted in decayed wood versus mineral soil microsites. Oecologia, 173(4): 1499-1511. 1-13. 10.1007/ s00442-013-2713-9.
96. Walker, J.K.M., Ward, V., Paterson, C., and Jones, M.D. 2012. Coarse woody debris retention in subalpine clearcuts affects ectomycorrhizal root tip community structure within fifteen years of harvest. J. Appl. Soil Ecol. 60: 5-15. doi:10. 1016/j.apsoil.2012.02.017.
97. Wallander, H., Göransson, H., and Rosengren, U. 2004. Production, standing biomass and natural abundance of 15N and 13C in ectomycorrhizal mycelium collected at different soil depths in two forest types. Oecologia, 139(1): 89-97. doi:10.1007/s00442-003-1477-z. PMID:14727173.
98. Wallander, H., Johansson, U., Sterkenburg, E., Durling, M.B., and Lindahl, B.D. 2010. Production of ectomycorrhizal mycelium peaks during canopy closure in Norway spruce forests. New Phytol. 187(4): 1124-1134. doi:10.1111/j.1469-8137.2010.03324.x. PMID:20561206.
99. White, T.J., Bruns, T., Lee, S., and Taylor, J.W. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR protocols: a guide to methods and applications. Edited by M.A. Innis, D.H. Gelfand, J.J. Sninsky, and T.J. White. Academic Press.