Ectomycorrhizal fungi and interspecific competition: Species interactions, community structure, coexistence mechanisms, and future research directions

New Phytologist

Volumn 187, Issue 4, 2010, Pages 895-910

  Kennedy, Peter ^a  

^a LEWIS AND CLARK COLLEGE   (United States)

Author keywords

Community structure; Ectomycorrhizal fungi; Interspecific competition; Microbial ecology; Species coexistence; Symbiosis

Indexed keywords

COEXISTENCE; COMMUNITY STRUCTURE; ECTOMYCORRHIZA; FUNGUS; FUTURE PROSPECT; HOST SPECIFICITY; INTERSPECIFIC COMPETITION; MICROBIAL ECOLOGY; SOIL CHEMISTRY; SYMBIOSIS; TRADE-OFF;

ECOSYSTEM; FUNGUS; HOST PARASITE INTERACTION; MICROBIOLOGY; MYCORRHIZA; PLANT; PLANT ROOT; REVIEW;

ECOSYSTEM; FUNGI; HOST-PARASITE INTERACTIONS; MYCORRHIZAE; PLANT ROOTS; PLANTS;

FUNGI;

EID: 77955737297     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03399.x     Document Type: Review

References (116)

1. Abuzinadah RA, Read DJ. The role of proteins in the nitrogen nutrition of ectomycorrhizal plants I: utilization of peptides and proteins by ectomycorrhizal fungi. New Phytologist 1986, 103:481-493.
2. Agerer R. Studies on ectomycorrhizae XXIV. Ectomycorrhizae of Chroogomphus helveticus and C. rutilus (Gomphidiaceae, Basidiomycetes) and their relationship to those of Suillus and Rhizopogon. Nova Hedwiga 1990, 50:1-63.
3. Agerer R, Grote R, Raidl S. The new method 'micromapping', a means to study species-specific associations and exclusions of ectomycorrhizae. Mycological Progress 2002, 1:155-166.
4. Baar J, Horton TR, Kretzer A, Bruns TD. Mycorrhizal recolonization of Pinus muricata from resistant propagules after a stand-replacing wildfire. New Phytologist 1999, 143:409-418.
5. Bengtsson J, Fagerstrom T, Rydin H. Competition and coexistence in plant communities. Trends in Ecology and Evolution 1994, 9:246-250.
6. Bennett AE, Bever JD. Trade-offs between arbuscular mycorrhizal fungal competitive ability and host growth promotion in Plantago lanceolata. Oecologia 2009, 160:807-816.
7. Bidartondo M, Ek H, Wallander H, Soderstrom B. Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi? New Phytologist 2001, 151:543-550.
8. Bever JD, Richardson SC, Lawrence BM, Holmes J, Watson M. Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecology Letters 2009, 12:13-21.
9. Blanco AR, Sicardi M, Frioni L. Competition for nodule occupancy between introduced and native strains of Rhizobium leguminosarum biovar trifolii. Biology and Fertility of Soils 2010, 46:419-425.
10. Bledsoe C, Tennyson K, Lopushinsky W. Survival and growth of mycorrhizal Douglas-fir seedlings outplanted on burned-over sites in eastern WA. Canadian Journal of Forest Research 1982, 12:720-723.
11. Boddy L. Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiology & Ecology 2000, 31:185-194.
12. Bruns TD. Thoughts on the processes that maintain local species diversity of ectomycorrhizal fungi. Plant and Soil 1995, 170:63-73.
13. Bruns TD, Kennedy PG. Individuals, populations, communities and function: the growing field of mycorrhizal ecology. New Phytologist 2009, 182:12-14.
14. Bruns T, Peay K, Boynton P, Grubisha L, Hynson N, Nguyen N, Rosenstock N. Inoculum potential of Rhizopogon spores increases with time over the first four years of a 99-year spore burial experiment. New Phytologist 2009, 181:463-470.
15. Callaway R, Brooker R, Choler P, Kikvidze Z, Lortie C, Michalet R, Paolini L, Pugnaire F, Newingham B, Aschehoug E. Positive interactions among alpine plants increase with stress. Nature 2002, 417:844-848.
16. Cavender-Bares J, Kozak K, Fine P, Kembel S. The merging of community ecology and phylogenetic biology. Ecology Letters 2009, 12:693-715.
17. Chesson P. Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 2000, 31:343-366.
18. Chesson P, Warner R. Environmental variability promotes coexistence in lottery competitive systems. American Naturalist 1981, 117:923-943.
19. Connell JH. On the prevalence and relative importance of interspecific competition: evidence from field experiments. American Naturalist 1983, 122:661-696.
20. Courty P, Pritsch K, Schloter M, Hartmann A, Garbaye J. Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytologist 2005, 167:309-319.
21. Dahlberg A, Jonsson L, Nylund J-E. Species diversity and distribution of biomass above and below ground among ectomycorrhizal fungi in an old-growth Norway spruce forest in south Sweden. Canadian Journal of Botany 1997, 75:1323-1335.
22. Deacon J, Fleming L. Interactions of ectomycorrhizal fungi. Mycorrhizal functioning 1992, 249-300. Allen M, New York, NY, USA, Chapman & Hall
23. Debaud JC, Marmeisse R, Gay G. Intraspecific genetic variation and populations of ectomycorrhizal fungi. Mycorrhiza 1999, 75-110. Varma A, Hock B.S, Berlin, Germany, Springer Verlag
24. Denno RF, McClure MS, Ott JR. Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annual Review of Entomology 1995, 40:297-331.
25. Diamond J. Assembly of species communities. Ecology and evolution of communities 1975, 342-444. Diamond JCody M.s, Cambridge, MA, USA, Harvard University Press
26. Dickie IA, Moyersoen B. Towards a global view of ectomycorrhizal ecology. New Phytologist 2008, 180:263-265.
27. Duchesne L, Peterson RL, Ellis BE. Pine root exudate stimulates the synthesis of antifungal compounds by the ectomycorrhizal fungus Paxillus involutus. New Phytologist 1988, 108:471-476.
28. Dumont M, Murrell J. Stable isotope probing - linking microbial identity to function. Nature Reviews Microbiology 2005, 3:499-504.
29. Erland S, Finlay R. Effects of temperature and incubation time on the ability of three ectomycorrhizal fungi to colonize Pinus sylvestris roots. Mycological Research 1992, 96:270-272.
30. Erland S, Soderstrom B, Andersson S. Effects of liming on ectomycorrhizal fungi infecting Pinus sylvestris L. II. Growth rates in pure symbiosis with the host plant. New Phytologist 1990, 115:683-688.
31. Erland S, Taylor AFS. Diversity of ecto-mycorrhizal fungal communities in relation to the abiotic environment. Mycorrhizal ecology 2002, 163-200. van der Heijden MGA, Sanders IR.s, Berlin, Germany, Springer-Verlag
32. Fries N, Swedjemark G. Sporophagy in Hymenomycetes. Experimental Mycology 1985, 9:74-79.
33. Garbaye J. First results of research on the competitivity of ectomycorrhizal fungi. Plant and Soil 1983, 71:303-308.
34. Gardes M, Bruns TD. Community structure of ectomycorrhizal fungi in a Pinus muricata forest: above- and below-ground views. Canadian Journal of Botany 1996, 74:1572-1583.
35. Garrett SD. Biology of root-infecting fungi 1956, New York, NY, USA, Cambridge University Press
36. Garrett SD. Pathogenic root-infecting fungi 1970, New York, NY, USA, Cambridge University Press
37. Gaul D, Hertel D, Leuschner C. Estimating fine root longetivity in a temperate Norway spruce forest using three independent methods. Functional Plant Biology 2009, 36:11-19.
38. Goldberg D. Components of competition in plant communities. Perspectives on plant competition 1990, 27-49. Grace JTilman D.s, San Diego, CA, USA, Academic Press
39. Goldberg DE, Barton AM. Patterns and consequences of interspecific competition in natural communities: a review of field experiments with plants. American Naturalist 1992, 139:771-801.
40. Gotelli N, McCabe D. Species co-occurrence: a meta-analysis of J.M. Diamond's Assembly rules model. Ecology 2002, 83:2091-2096.
41. Grace J, Tilman D. Perspectives on plant competition 1990, San Diego, CA, USA, Academic Press
42. Hibbing ME, Fuqua C, Parsek MR, Peterson SR. Bacterial competition: surviving and thriving in the microbial jungle. Nature Reviews Microbiology 2009, 8:15-25.
43. Hobbie E. Using isotopic tracers to follow carbon and nitrogen cycling of fungi. The fungal community: its organization and role in the ecosystem 2005, 361-381. Dighton JOudemans PWhite J.s, Marc Dekker, New York, NY, USA
44. Hoeksema JD, Kummel M. Ecological persistence of the plant-mycorrhizal mutualism: a hypothesis from species coexistence theory. American Naturalist 2003, 162:S40-S45.
45. Hortal S, Pera J, Parlade J. Tracking mycorrhizas and extraradical mycelium of the edible fungus Lactarius delicious under field competition with Rhizopogon spp. Mycorrhiza 2008, 18:69-77.
46. Horton TR, Bruns TD. The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Molecular Ecology 2001, 10:1855-1871.
47. Horton TR, Cazares E, Bruns TD. Ectomycorrhizal, vesicular-arbuscular and dark septate fungal colonization of bishop pine (Pinus muricata) seedlings in the first five months of growth after wildfire. Mycorrhiza 1998, 8:11-18.
48. Hutchison GE. The paradox of the plankton. American Naturalist 1961, 93:145-159.
49. Inderjit, Del Moral R. Is separating resource competition from allelopathy realistic? The Botanical Review 1997, 63:22-232.
50. Ishida T, Nara K, Hogetsu T. Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer-broadleaf forests. New Phytologist 2007, 174:430-440.
51. Ishida T, Nara K, Kazuhide T, Tanaka M, Kinoshita A, Hogetsu T. Germination and infectivity of ectomycorrhizal fungal spores in relation to their ecological traits during primary succession. New Phytologist 2008, 180:491-500.
52. Izzo A, Nguyen DT, Bruns TD. Spatial structure and richness of ectomycorrhizal fungi colonizing bioassay seedlings from resistant propagules in a Sierra Nevada forest: comparisons using two host that exhibit different seedling establishment patterns. Mycologia 2006, 98:374-383.
53. Kaplan I, Denno RF. Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecology Letters 2007, 10:977-994.
54. Keddy PA. Competition 2001, Dordrecht, the Netherlands, Kluwer
55. Kennedy P, Bergemann S, Hortal S, Bruns T. Determining the outcome of field-based competition between two Rhizopogon species using real-time PCR. Molecular Ecology 2007a, 16:881-890.
56. Kennedy P, Bruns T. Priority effects determine the outcome of ectomycorrhizal competition between two Rhizopogon species colonizing Pinus muricata seedlings. New Phytologist 2005, 166:631-638.
57. Kennedy P, Hortal S, Bergemann S, Bruns T. Competitive interactions three ectomycorrhizal and their relation to host plant performance. Journal of Ecology 2007b, 95:1338-1345.
58. Kennedy PG, Bruns TD. Mycorrhizas take root at the Ecological Society of America. New Phytologist 2007, 176:745-748.
59. Kennedy PG, Peay K, Bruns TD. Root tip competition among ectomycorrhizal fungi: are priority effects a rule or an exception? Ecology 2009, 90:2098-2107.
60. Koide R, Xu B, Sharda J, Lekberg Y, Ositguy N. Evidence of species interactions within an ectomycorrhizal fungal community. New Phytologist 2005, 165:305-316.
61. Kraft N, Ackerly D. Functional trait and phylogenetic tests of community assembly across spatial scales in an Amazonian forest. Ecology 2010, http://dx.doi.org/10.1890/09-1672, doi: 10.1890/09-1672
62. Kraft N, Cornwell W, Webb C, Ackerly D. Trait evolution, community assembly, and the phylogenetic structure of ecological communities. American Naturalist 2007, 170:217-283.
63. Krywolap G. Cenococcum graniforme 1964, Antibiotics elaboration in pure culture and during mycorrhizal association. PhD thesis, Pennsylvania State University, University Park, PA, USA
64. Kummel M, Salant S. The economics of mutualisms: optimal utilization of mycorrhizal mutualistic partners by plants. Ecology 2006, 87:892-902.
65. Landeweert R, Veenman C, Kuyper TW, Fritze H, Wernars K, Smit E. Quantification of ectomycorrhizal mycelium in soil by real-time PCR compared to conventional quantification techniques. FEMS Microbiology & Ecology 2003, 45:283-292.
66. Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read D. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Canadian Journal of Botany 2004, 82:1016-1045.
67. Lekberg Y, Koide R, Rohr JR, Aldrich-Wolfe L, Morton JB. Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. Journal of Ecology 2007, 95:95-105.
68. Lian C, Marimatsu M, Nara K, Hogetsu T. Tricholoma matsutake in a natural Pinus densiflora forest: correspondence between above- and below-ground genets, association with multiple host trees and alteration of existing ectomycorrhizal communities. New Phytologist 2006, 171:825-836.
69. Lilleskov EA, Bruns TD. Root colonization dynamics of two ectomycorrhizal fungi of contrasting life history strategies are mediated by addition of organic nutrient patches. New Phytologist 2003, 159:141-151.
70. Lockwood J. Exploitation competition fungi. Mycological Progress 1981, 2:319-349.
71. Mahmood S. Colonisation of spruce roots by two interacting ectomycorrhizal fungi in wood ash amended substrates. FEMS Microbiology Letters 2003, 221:881-887.
72. Mamoun M, Olivier J. Competition between Tuber melanosporum and other ectomycorrhizal fungi under two irrigation regimes. I. Competition with Tuber brunale. Plant and Soil 1993, 149:211-218.
73. McAfee B, Fortin J. Competitive interactions of ectomycorrhizal mycobionts under field conditions. Canadian Journal of Botany 1986, 64:848-852.
74. Molina R, Massicotte HB, Trappe JM. Specificity phenomena in mycorrhizal symbioses: community-ecological consequences and practical implications. Mycorrhizal functioning 1992, 357-423. Allen M, New York, NY, USA, Chapman & Hall
75. Nara K. Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytologist 2006, 169:169-178.
76. Nehls U, Grunze N, Willman M, Reich M, Kuster H. Sugar for my honey: carbohydrate partitioning in ectomycorrhizal symbiosis. Phytochemistry 2007, 68:82-91.
77. Newell K. Interaction between two decomposer basidiomycetes and a collembolan under spruce: distribution, abundance, and selective grazing. Soil Biology and Biochemistry 1984, 16:227-233.
78. Paine R. Intertidal community structure - experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia 1974, 15:93-120.
79. Palmer TM, Stanton ML, Young TP. Competition and coexistence: exploring mechanisms that restrict and maintain diversity within mutualist guilds. American Naturalist 2003, 162:S63-S79.
80. Parkinson D, Visser S, Whittaker JB. Effects of collembolan grazing on fungal colonization on leaf litter. Soil Biology and Biochemistry 1979, 11:529-535.
81. Parlade J, Alvarez I. Coinoculation of aseptically grown Douglas fir with pairs of ectomycorrhizal fungi. Mycorrhiza 1993, 3:93-96.
82. Parlade J, Hortal S, Pera J, Galipienso L. Quantitative detection of Lactarius deliciosus extraradical soil mycelium by real-time PCR and its application in the study of fungal persistence and interspecific competition. Journal of Biotechnology 2007, 128:14-23.
83. Peay K, Bruns T, Kennedy P, Bergemann S, Garbelotto M. A strong species-area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecology Letters 2007, 10:470-480.
84. Peay K, Kennedy P, Bruns T. Fungal community ecology: a hybrid beast with a molecular master. BioScience 2008, 58:799-810.
85. Peay K, Kennedy P, Davies S, Tan S, Bruns T. Potential link between plant and fungal distributions in a dipterocarp rainforest: community phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone. New Phytologist 2010, 185:529-542.
86. Pickles BJ, Genney DR, Potts JM, Lennon J, Anderson I, Alexander I. Spatial and temporal ecology of Scots pine ectomycorrhizas. New Phytologist 2010, 186:755-768.
87. Prosser J, Bohannan B, Curtis T, Ellis R, Firestone M, Freckleton R, Green J, Green L, Killham K, Lennon J. The role of ecological theory in microbial ecology. Nature Reviews Microbiology 2007, 5:384-392.
88. Radajewski S, McDonald I, Murrell J. Stable-isotope probing of nucleic acids: a window to the function of uncultured microorganisms. Current Opinion in Biotechnology 2003, 14:296-302.
89. Raidl S, Bonfigli R, Agerer R. Calibration of quantitative real-time TaqMan PCR by correlation with hyphal biomass and ITS copies in mycelia of Piloderma croceum. Plant Biology 2005, 7:713-717.
90. Sachs J, Simms E. Pathways to mutualism breakdown. Trends in Ecology and Evolution 2006, 21:585-592.
91. Sale P. Maintenance of high diversity in coral reef fish communities. American Naturalist 1977, 111:337-359.
92. Sammul M, Oksanen L, Magi M. Regional effects on competition-productivity relationship: a set of field experiments in two distant regions. Oikos 2006, 112:138-148.
93. Schoener TW. Field experiments on interspecific competition. American Naturalist 1983, 122:240-285.
94. Schubert R, Raidl S, Funk R, Bahnweg G, Muller-Starck G, Agerer R. Quantitative detection of agar-cultivated and rhizotron-grown Piloderma croceum Erikss. & Hjortst. by ITS1-based fluorescent PCR. Mycorrhiza 2003, 13:159-165.
95. Shearer C. Fungal competition. Canadian Journal of Botany 1995, 73:S1259-S1264.
96. Smith M, Douhan G, Kremier A, Rizzo D. Are true multihost fungi the exception or the rule? Dominant ectomycorrhizal fungi on Pinus sabinia differ from those on co-occurring Quercus species. New Phytologist 2009, 182:295-299.
97. Smith C, Osborn A. Advantages and limitations of quantitative PCR (Q-PCR)-based approaches in microbial ecology. FEMS Microbiology & Ecology 2009, 67:6-20.
98. Smith SE, Read DJ. Mycorrhizal Symbiosis 2008, 3rd edition, New York, USA, Academic Press
99. Stachowicz JJ. Mutualism, facilitation and the structure of ecological communities. BioScience 2001, 51:235-246.
100. Stone L, Roberts A. The checkerboard score and species distributions. Oecologia 1990, 85:74-79.
101. Taylor DL, Bruns TD. Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the mature forest and resistant propagule communities. Molecular Ecology 1999, 8:1837-1850.
102. Tedersoo L, Jairus T, Horton B, Abarenkov K, Suvi T, Saar I, Koljalg U. Strong host preference of ectomycorrhizal fungi in a Tasmanian wet sclerophyll forest as revealed by DNA barcoding and taxon-specific primers. New Phytologist 2008, 180:479-490.
103. Tilman D. Competition and biodiversity in spatially structured habitats. Ecology 1994, 75:2-16.
104. Timonen S, Tammi H, Sen R. Outcome of interactions between genets of two Suillus spp. and different Pinus sylvestris genotype combinations: identity and distribution of ectomycorrhizas and effects on early seedling growth in N-limited nursery soil. New Phytologist 1997, 137:691-702.
105. Townsend C, Begon M, Harper J. Essentials of ecology 2008, Malden, MA, USA, Wiley-Blackwell
106. Tuininga AR. Interspecific interaction terminology: from mycology to general ecology. The fungal community: its organization and role in the ecosystem 2005, 265-286. Dighton JWhite JOudemans P.s, Boca Raton, FL, USA, CRC Press
107. Vandenkoornhuyse P, Mahe S, Ineson P, Staddon P, Ostle N, Cliquet J, Francez A, Fitter A, Young J. Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA. Proceedings in the National Academy of Sciences, USA 2007, 104:16970-16975.
108. Villeneuve N, Le Tacon F, Bouchard D. Survival of inoculated Laccaria bicolor in competition with native ectomycorrhizal fungi and effects on the growth of outplanted Douglas-fir seedlings. Plant and Soil 1991, 135:95-107.
109. Warner R, Chesson P. Coexistence mediated by recruitment fluctuations: a field guide to the storage effect. American Naturalist 1985, 125:769-787.
110. Webb C, Ackerly D, McPeek M, Donoghue M. Phylogenies and community ecology. Annual Review of Ecology and Systematics 2002, 33:475-505.
111. Weiner J. Asymmetric competition in plant populations. Trends in Ecology and Evolution 1990, 5:360-364.
112. Wicklow DT. Interference competition. The fungal community: its organization and role in the ecosystem 1992, 265-274. Wicklow DTCarroll GC.s, New York, NY, USA, Marcel Dekker, Inc
113. Widden P. Competition and the fungal community. The Mycota IV: environmental and microbial relationships 1997, 135-147. Wicklow GSoderstrom A.s, Berlin, Germany, Springer-Verlag
114. Williamson GB. Allelopathy, Koch's postulates, and the neck riddle. Perspectives on plant competition 1990, 143-162. Grace JTilman D.s, San Diego, CA, USA, Academic Press
115. Wolfe BE, Richard F, Cross HB, Pringle A. Distribution and abundance of the introduced ectomycorrhizal fungus Amanita phalloides in North America. New Phytologist 2010, 185:803-816.
116. Wu B, Nara K, Hogetsu T. Competition between ectomycorrhizal fungi in colonizing Pinus densiflora. Mycorrhiza 1999, 9:151-159.