The importance of individuals: Intraspecific diversity of mycorrhizal plants and fungi in ecosystems

New Phytologist

Volumn 194, Issue 3, 2012, Pages 614-628

  Johnson, David ^a   Martin, Francis ^b   Cairney, John W G ^c   Anderson, Ian C ^c  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITÉ DE LORRAINE   (France)

^c WESTERN SYDNEY UNIVERSITY   (Australia)

Author keywords

Arbuscular mycorrhiza (AM); Biodiversity; Ectomycorrhiza (ECM); Ericoid mycorrhiza (ERM); Evolution; Genetic diversity; Genotypic diversity; Phenotypic variation

Indexed keywords

ABUNDANCE; ARBUSCULAR MYCORRHIZA; BIODIVERSITY; ECTOMYCORRHIZA; ENVIRONMENTAL FACTOR; FUNGUS; GENETIC VARIATION; GENOTYPE; INTRASPECIFIC VARIATION; PHENOTYPIC PLASTICITY; SPECIES EVENNESS; SPECIES RICHNESS; SYMBIOSIS;

BIODIVERSITY; ECOSYSTEM; EVOLUTION; GENETIC VARIABILITY; GENETICS; GENOMICS; GENOTYPE; MYCORRHIZA; PHENOTYPE; PHYSIOLOGY; PLANT; PLANT PHYSIOLOGY; POPULATION GENETICS; REVIEW; SYMBIOSIS;

BIODIVERSITY; BIOLOGICAL EVOLUTION; ECOSYSTEM; GENETIC VARIATION; GENETICS, POPULATION; GENOMICS; GENOTYPE; MYCORRHIZAE; PHENOTYPE; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS; SYMBIOSIS;

ARBUSCULAR; FUNGI;

EID: 84862828846     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2012.04087.x     Document Type: Review

References (139)

1. Akiyama K, Matsuzaki K, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824-827.
2. Anderson IC, Cairney JWG. 2004. Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Environmental Microbiology 6: 769-779.
3. Anderson IC, Chambers SM, Cairney JWG. 2001. Distribution and persistence of Australian Pisolithus species genets at native sclerophyll forest field sites. Mycological Research 105: 971-976.
4. Angelard C, Colard A, Niculita-Hirzel H, Croll D, Sanders IR. 2010. Segregation in a mycorrhizal fungus alters rice growth and symbiosis-specific gene transcription. Current Biology 20: 1216-1221.
5. Antonovics J. 1976. The input from population genetics: 'the new ecological genetics'. Systematic Botany 1: 233-245.
6. Avio L, Pellegrino E, Bonari E, Giovannetti M. 2006. Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelial networks. New Phytologist 172: 347-357.
7. Bangert RK, Turek RJ, Martinsen GD, Wimp GM, Bailey JK, Whitham TG. 2005. Benefits of conservation of plant genetic diversity to arthropod diversity. Conservation Biology 19: 379-390.
8. Beiler KJ, Durall DM, Simard SW, Maxwell SA, Kretzer AM. 2010. Architecture of the wood-wide web: Rhizopogon spp. genets link multiple Douglas-fir cohorts. New Phytologist 185: 543-553.
9. Bever JD. 2002. Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proceedings of the Royal Society of London Series B-Biological Sciences 269: 2595-2601.
10. Bever JD. 2003. Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytologist 157: 465-473.
11. Bever JD, Richardson SC, Lawrence BM, Holmes J, Watson M. 2009. Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecology Letters 12: 13-21.
12. Bever JD, Westover KM, Antonovics J. 1997. Incorporating the soil community into plant population dynamics: the utility of the feedback approach. Journal of Ecology 85: 561-573.
13. Bilton MC, Whitlock R, Grime JP, Marion G, Pakeman RJ. 2010. Intraspecific trait variation in grassland plant species reveals fine-scale strategy trade-offs and size differentiation that underpins performance in ecological communities. Botany 11: 939-952.
14. Bolnick DI, Svanback R, Araujo MS, Persson L. 2007. Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proceedings of the National Academy of Sciences, USA 104: 10075-10079.
15. Bonello P, Bruns TD, Gardes M. 1998. Genetic structure of a natural population of the ectomycorrhizal fungus Suillus pungens. New Phytologist 138: 533-542.
16. Booth RE, Grime JP. 2003. Effects of genetic impoverishment on plant community diversity. Journal of Ecology 91: 721-730.
17. Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH, Pretorius IS, Egholm M, Chambers PJ. 2011. Whole-genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genetics 7: e1001287.
18. Bown JL, Pachepsky E, Eberst A, Bausenwein U, Millard P, Squire GR, Crawford JW. 2007. Consequences of intraspecific variation for the structure and function of ecological communities: part 1. Model development and predicted patterns of diversity. Ecological Modelling 207: 264-276.
19. Brooker RW, Travis JMJ, Clark EJ, Dytham C. 2007. Modelling species' range shifts in a changing climate: the impacts of biotic interactions, dispersal distance and the rate of climate change. Journal of Theoretical Biology 245: 59-65.
20. Bruederle LP, Hugan MS, Dignan JM, Vorsa N. 1996. Genetic variation in natural populations of the large cranberry, Vaccinium macrocarpon Ait (Ericaceae). Bulletin of the Torrey Botanical Club 123: 41-47.
21. Cairney JWG. 1999. Intraspecific physiological variation: implications for understanding functional diversity in ectomycorrhizal fungi. Mycorrhiza 9: 125-135.
22. Clark JS. 2010. Individuals and the variation needed for high species diversity in forest trees. Science 327: 1129-1132.
23. Coleman MD, Bledsoe CS, Lopushinsky W. 1989. Pure culture response of ectomycorrhizal fungi to imposed water-stress. Canadian Journal of Botany-Revue Canadienne De Botanique 67: 29-39.
24. Courty PE, Labbé J, Kohler A, Marçais B, Bastien C, Churin JL, Garbaye J, Le Tacon F. 2010. Effect of poplar genotypes on mycorrhizal infection and secreted enzyme activities in mycorrhizal and non-mycorrhizal roots. Journal of Experimental Botany 62: 249-260.
25. Croll D, Sanders IR. 2009. Recombination in Glomus intraradices, a supposed ancient asexual arbuscular mycorrhizal fungus. BMC Evolutionary Biology 9: 13.
26. Croll D, Wille L, Gamper HA, Mathimaran N, Lammers PJ, Corradi N, Sanders IR. 2008. Genetic diversity and host plant preferences revealed by simple sequence repeat and mitochondrial markers in a population of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist 178: 672-687.
27. Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ. 2006. Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313: 966-968.
28. Curlevski NJA, Chambers SM, Anderson IC, Cairney JWG. 2009. Identical genotypes of an ericoid mycorrhiza-forming fungus occur in roots of Epacris pulchella (Ericaceae) and Leptospermum polygalifolium (Myrtaceae) in an Australian sclerophyll forest. FEMS Microbiology Ecology 67: 411-420.
29. De Deyn GB, Cornelissen JHC, Bardgett RD. 2008. Plant functional traits and soil carbon sequestration in contrasting biomes. Ecology Letters 11: 516-531.
30. Debuchy R, Berteaux-Lecellier V, Silar P. 2010. Mating systems and sexual morphogenesis in Ascomycetes. In: Borkowich KA, Ebbole DJ, eds. Cellular and molecular biology of filamentous fungi. Washington, DC, USA: ASM press, 501-535.
31. Dietz S, Von Bulow J, Beitz E, Nehls U. 2011. The aquaporin gene family of the ectomycorrhizal fungus Laccaria bicolor: lessons for symbiotic functions. New Phytologist 190: 927-940.
32. Douhan GA, Vincenot L, Gryta H, Selosse MA. 2011. Population genetics of ectomycorrhizal fungi: from current knowledge to emerging directions. Fungal Biology 115: 569-597.
33. Duddridge JA, Malibari A, Read DJ. 1980. Structure and function of mycorrhizal rhizomorphs with special reference to their role in water transport. Nature 287: 834-836.
34. Duffy JE, Cardinale BJ, France KE, McIntyre PB, Thebault E, Loreau M. 2007. The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecology Letters 10: 522-538.
35. Duplessis S, Cuomo CA, Lin Y-C, Aerts A, Tisserant E, Veneault-Fourrey C, Joly DL, Hacquard S, Amselem J, Cantarel B et al. 2011. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proceedings of the National Academy of Sciences, USA 108: 9166-9171.
36. Eastwood DC, Floudas D, Binder M, Majcherczyk A, Schneider P, Aerts A, Asiegbu FO, Baker SE, Barry K, Bendiksby M et al. 2011. The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science 333: 762-765.
37. Ehinger M, Koch AM, Sanders IR. 2009. Changes in arbuscular mycorrhizal fungal phenotypes and genotypes in response to plant species identity and phosphorus concentration. New Phytologist 184: 412-423.
38. Ehlers A, Worm B, Reusch TBH. 2008. Importance of genetic diversity in eelgrass Zostera marina for its resilience to global warming. Marine Ecology-Progress Series 355: 1-7.
39. Ellison CE, Hall C, Kowbel D, Welch J, Brem RB, Glass NL, Taylor JW. 2011. Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proceedings of the National Academy of Sciences, USA 108: 2831-2836.
40. Fiore AM, Martin F. 2001. Populations of ectomycorrhizal Laccaria amethystina and Xerocomus spp. show contrasting colonization patterns in a mixed forest. New Phytologist 152: 533-542.
41. Fridley JD, Grime JP, Bilton M. 2007. Genetic identity of interspecific neighbours mediates plant responses to competition and environmental variation in a species-rich grassland. Journal of Ecology 95: 908-915.
42. Garnier E, Laurent G, Bellmann A, Debain S, Berthelier P, Ducout B, Roumet C, Navas ML. 2001. Consistency of species ranking based on functional leaf traits. New Phytologist 152: 69-83.
43. Genney DR, Anderson IC, Alexander IJ. 2006. Fine scale distribution of pine ectomycorrhizas and their extramatrical mycelium. New Phytologist 170: 381-390.
44. Giovannetti M, Azzolini D, Citernesi AS. 1999. Anastomosis formation and nuclear and protoplasmic exchange in arbuscular mycorrhizal fungi. Applied and Environmental Microbiology 65: 5571-5575.
45. Giovannetti M, Fortuna P, Citernesi AS, Morini S, Nuti MP. 2001. The occurrence of anastomosis formation and nuclear exchange in intact arbuscular mycorrhizal networks. New Phytologist 151: 717-724.
46. Grelet G-A, Johnson D, Vrålstad T, Alexander IJ, Anderson IC. 2010. New insights into the mycorrhizal Rhizoscyphus ericae aggregate: spatial structure and co-colonization of ectomycorrhizal and ericoid roots. New Phytologist 188: 210-222.
47. 13C within the structure of an upland grassland soil. Soil Biology and Biochemistry 38: 229-234.
48. Grigoriev IV, Cullen D, Goodwin SB, Hibbett D, Jeffries TW, Kubicek CP, Kuske C, Magnuson JK, Martin F, Spatafora JW et al. 2011. Fueling the future with fungal genomics. Mycology 2: 192-209.
49. Grime JP. 2002. Declining plant diversity: empty niches or functional shifts? Journal of Vegetation Science 13: 457-460.
50. Gryta H, Debaud JC, Effosse A, Gay G, Marmeisse R. 1997. Fine-scale structure of populations of the ectomycorrhizal fungus Hebeloma cylindrosporum in coastal sand dune forest ecosystems. Molecular Ecology 6: 353-364.
51. Guidot A, Lumini E, Debaud JC, Marmeisse R. 1999. The nuclear ribosomal DNA intergenic spacer as a target sequence to study intraspecific diversity of the ectomycorrhizal basidiomycete Hebeloma cylindrosporum directly on Pinus root systems. Applied and Environmental Microbiology 65: 903-909.
52. Hambleton S, Sigler L. 2005. Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (≡Hymenoscyphus ericae), Leotiomycetes. Studies in Mycology 53: 1-27.
53. He TH, Lamont BB. 2010. Species versus genotypic diversity of a nitrogen-fixing plant functional group in a metacommunity. Population Ecology 52: 337-345.
54. Hillebrand H, Bennett DM, Cadotte MW. 2008. Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89: 1510-1520.
55. Hoeksema JD. 2010. Ongoing coevolution in mycorrhizal interactions. New Phytologist 187: 276-300.
56. Horton TR, Bruns TD. 2001. The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Molecular Ecology 10: 1855-1871.
57. Hughes AR, Inouye BD, Johnson MTJ, Underwood VM. 2008. Ecological consequences of genetic diversity. Ecology Letters 11: 609-623.
58. Huston MA. 1997. Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110: 449-460.
59. Jany JL, Martin F, Garbaye J. 2003. Respiration activity of ectomycorrhizas from Cenococcum geophilum and Lactarius sp. in relation to soil water potential in five beech forests. Plant and Soil 255: 487-494.
60. Johnson D, Anderson IC, Williams A, Whitlock R, Grime JP. 2010a. Plant genotypic diversity does not beget root-fungal species diversity. Plant and Soil 336: 107-111.
61. Johnson D, Phoenix GK, Grime JP. 2008. Plant community composition regulates soil respiration in grasslands. Biology Letters 4: 345-348.
62. Johnson D, Vandenkoornhuyse PJ, Leake JR, Gilbert LA, Booth RE, Grime JP, Young JPW, Read DJ. 2004. Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytologist 161: 503-516.
63. Johnson NC. 2010. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist 185: 631-647.
64. Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM. 2010b. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proceedings of the National Academy of Sciences, USA 107: 2093-2098.
65. Jonsson LM, Nilsson MC, Wardle DA, Zackrisson O. 2001. Context dependent effects of ectomycorrhizal species richness on tree seedling productivity. Oikos 93: 353-364.
66. Jump AS, Hunt JM, Martínez-Izquierdo JA, Peñuelas J. 2006. Natural selection and climate change: temperature-linked spatial and temporal trends in gene frequency in Fagus sylvatica. Molecular Ecology 15: 3469-3480.
67. Jump AS, Marchant R, Peñuelas J. 2009. Environmental change and the option value of genetic diversity. Trends in Plant Science 14: 51-58.
68. Jump AS, Peñuelas J, Rico L, Ramallo E, Estiarte M, Martínez-Izquierdo JA, Lloret F. 2008. Simulated climate change provokes rapid genetic change in the Mediterranean shrub Fumana thymifolia. Global Change Biology 14: 637-643.
69. Jung V, Violle C, Mondy C, Hoffmann L, Muller S. 2010. Intraspecific variability and trait-based community assembly. Journal of Ecology 98: 1134-1140.
70. Kennedy PG, Peay KG. 2007. Different soil moisture conditions change the outcome of the ectomycorrhizal symbiosis between Rhizopogon species and Pinus muricata. Plant and Soil 291: 155-165.
71. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A et al. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333: 880-882.
72. Koch AM, Croll D, Sanders IR. 2006. Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth. Ecology Letters 9: 103-110.
73. Koch AM, Kuhn G, Fontanillas P, Fumagalli L, Goudet J, Sanders IR. 2004. High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi. Proceedings of the National Academy of Sciences, USA 101: 2369-2374.
74. Koide RT, Xu B, Sharda J. 2005. Contrasting below-ground views of an ectomycorrhizal fungal community. New Phytologist 166: 251-262.
75. Korkama T, Pakkanen A, Pennanen T. 2006. Ectomycorrhizal community structure varies among Norway spruce (Picea abies) clones. New Phytologist 171: 815-824.
76. Kretzer AM, Dunham S, Molina R, Spatafora JW. 2003. Microsatellite markers reveal the below ground distribution of genets in two species of Rhizopogon forming tuberculate ectomycorrhizas on Douglas fir. New Phytologist 161: 313-320.
77. Kuhn G, Hijri M, Sanders IR. 2001. Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414: 745-748.
78. Labbé J, Jorge V, Kohler A, Vion P, Marcais B, Basten C, Tuskan GA, Martin F, Le Tacon F. 2011a. Identification of quantitative trait loci affecting ectomycorrhizal symbiosis in an interspecific F(1) poplar cross and differential expression of genes in ectomycorrhizas of the two parents: Populus deltoides and Populus trichocarpa. Tree Genetics and Genomes 7: 617-627.
79. Labbé J, Murat C, Morin E, Le Tacon F, Martin F. 2011b. Survey and analysis of simple sequence repeats in the Laccaria bicolor genome, with development of microsatellite markers. Current Genetics 57: 75-88.
80. Lam HM, Xu X, Liu X, Chen WB, Yang GH, Wong FL, Li MW, He WM, Qin N, Wang B et al. 2010. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nature Genetics 42: 1053-1059.
81. Lankau RA, Strauss SY. 2007. Mutual feedbacks maintain both genetic and species diversity in a plant community. Science 317: 1561-1563.
82. Leake JR. 2004. The biology of myco-heterotrophic (saprophytic) plants. New Phytologist 127: 171-216.
83. Lian CL, Narimatsu M, Nara K, Hogetsu T. 2006. 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 171: 825-836.
84. Loreau M, Hector A. 2001. Partitioning selection and complementarity in biodiversity experiments. Nature 412: 72-76.
85. Malik M, Vilgalys R. 1999. Somatic incompatibility in fungi. In: Worrall JJ, ed. Structure and dynamics of fungal populations. Dordrecht, the Netherlands: Kluwer, 123-138.
86. Martin F, Aerts A, Ahrén D, Brun A, Danchin EGJ, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V et al. 2008. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452: 88-92.
87. Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R et al. 2010. Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464: 1033-1038.
88. Martin F, Selosse M-A. 2008. The Laccaria genome: a symbiont blueprint decoded. New Phytologist 180: 296-310.
89. Munkvold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I. 2004. High functional diversity within species of arbuscular mycorrhizal fungi. New Phytologist 164: 357-364.
90. Murat C, Riccioni C, Belfiori B, Cichocki N, Labbé J, Morin E, Tisserant M, Paolocci F, Rubini A, Martin F. 2011. Distribution and localization of microsatellites in the Perigord black truffle genome and identification of new molecular markers. Fungal Genetics and Biology 48: 592-601.
91. Parrent JL, Peay K, Arnold AE, Comas LH, Avis P, Tuininga A. 2010. Moving from pattern to process in fungal symbioses: linking functional traits, community ecology and phylogenetics. New Phytologist 185: 882-886.
92. Pickles BJ, Genney DR, Potts JM, Lennon JJ, Anderson IC, Alexander IJ. 2010. Spatial and temporal ecology of Scots pine ectomycorrhizas. New Phytologist 186: 755-768.
93. Piculell BJ, Hoeksema JD, Thompson JN. 2008. Interactions of biotic and abiotic environmental factors in an ectomycorrhizal symbiosis, and the potential for selection mosaics. BMC Biology 6: 23.
94. Plett JM, Kemppainen M, Kale SD, Kohler A, Legué V, Brun A, Tyler BM, Pardo AG, Martin F. 2011. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Current Biology 21: 1197-1203.
95. Plett JM, Martin F. 2011. Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes. Trends in Genetics 27: 14-22.
96. Podila GK, Sreedasyam A, Muratet MA. 2009. Populus rhizosphere and the ectomycorrhizal interactome. Critical Reviews in Plant Science 28: 359-367.
97. Reiss J, Bridle JR, Montoya JM, Woodward G. 2009. Emerging horizons in biodiversity and ecosystem functioning research. Trends in Ecology and Evolution 24: 505-514.
98. Reusch TBH, Ehlers A, Hammerli A, Worm B. 2005. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proceedings of the National Academy of Sciences, USA 102: 2826-2831.
99. Rosendahl S. 2008. Communities, populations and individuals of arbuscular mycorrhizal fungi. New Phytologist 178: 253-266.
100. Rosendahl S, Matzen HB. 2008. Genetic structure of arbuscular mycorrhizal populations in fallow and cultivated soils. New Phytologist 179: 1154-1161.
101. Rosling A, Cox F, Cruz-Martinez K, Ihrmark K, Grelet GA, Lindahl BD, Menkis A, James TY. 2011. Archaeorhizomycetes: unearthing an ancient class of ubiquitous soil fungi. Science 333: 876-879.
102. Roumet C, Lafont F, Sari M, Warembourg F, Garnier E. 2008. Root traits and taxonomic affiliation of nine herbaceous species grown in glasshouse conditions. Plant and Soil 312: 69-83.
103. Rubini A, Belfiori B, Riccioni C, Arcioni S, Martin F, Paolocci P. 2010a. Tuber melanosporum: mating type distribution in a natural plantation and dynamics of strains of different mating types on the roots of nursery-inoculated host plants. New Phytologist 189: 723-725.
104. Rubini A, Belfiori B, Riccioni C, Tisserant E, Arcioni S, Martin F, Paolocci P. 2010b. Isolation and characterization of MAT genes in the symbiotic ascomycete Tuber melanosporum. New Phytologist 189: 710-722.
105. Selosse MA, Dubois MP, Alvarez N. 2009. Do Sebacinales commonly associate with plant roots as endophytes? Mycological Research 113: 1062-1069.
106. Selosse MA, Martin F, Le Tacon F. 2001. Intraspecific variation in fruiting phenology in an ectomycorrhizal Laccaria population under Douglas fir. Mycological Research 105: 524-531.
107. Selosse MA, Setaro S, Glatard F, Richard F, Urcelay C, Weiss M. 2007. Sebacinales are common mycorrhizal associates of Ericaceae. New Phytologist 174: 864-878.
108. Selosse MA, Weiss M, Jany JL, Tillier A. 2002. Communities and populations of sebacinoid basidiomycetes associated with the achlorophyllous orchid Neottia nidus-avis (L.) LCM Rich. and neighbouring tree ectomycorrhizae. Molecular Ecology 11: 1831-1844.
109. Silander JA, Antonovics J. 1979. Genetic-basis of the ecological amplitude of Spartina patens. 1. Morphometric and physiological traits. Evolution 33: 1114-1127.
110. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis, 3rd edn New York, NY, USA: Academic Press.
111. Spanu PD, Abbott JC, Amselem J, Burgiss TA, Soanes DM, Stuber K, van Themaat EVL, Brown JKM, Butcher SA, Gurr SJ et al. 2010. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330: 1543-1546.
112. Steltzer H, Hufbauer RA, Welker JM, Casalis M, Sullivan PF, Chimner R. 2008. Frequent sexual reproduction and high intraspecific variation in Salix arctica: implications for a terrestrial feedback to climate change in the High Arctic. Journal of Geophysical Research-Biogeosciences 113: G03S10.
113. Sthultz CM, Whitham TG, Kennedy K, Deckert R, Gehring CA. 2009. Genetically based susceptibility to herbivory influences the ectomycorrhizal fungal communities of a foundation tree species. New Phytologist 184: 657-667.
114. Stukenbrock EH, Rosendahl S. 2005. Clonal diversity and population genetic structure of arbuscular mycorrhizal fungi (Glomus spp.) studied by multilocus genotyping of single spores. Molecular Ecology 14: 743-752.
115. Suzuki JI, Herben T, Krahulec F, Hara T. 1999. Size and spatial pattern of Festuca rubra genets in a mountain grassland: its relevance to genet establishment and dynamics. Journal of Ecology 87: 942-954.
116. Tagu D, Bastien C, Rampant PF, Garbaye J, Vion P, Villar M, Martin F. 2005. Genetic analysis of phenotypic variation for ectomycorrhiza formation in an interspecific F1 poplar full-sib family. Mycorrhiza 15: 87-91.
117. Tagu D, Rampant PF, Lapeyrie F, Frey-Klett P, Vion P, Villar M. 2001. Variation in the ability to form ectomycorrhizas in the F1 progeny of an interspecific poplar (Populus spp.) cross. Mycorrhiza 10: 237-240.
118. Taylor DL, Bruns TD. 1997. Independent, specialized invasions of ectomycorrhizal mutualism by two nonphotosynthetic orchids. Proceedings of the National Academy of Sciences, USA 94: 4510-4515.
119. Thompson JN. 2005. The geographic mosaic of coevolution. Chicago, IL, USA: University of Chicago Press.
120. Thrall PH, Hochberg ME, Burdon JJ, Bever JD. 2007. Coevolution of symbiotic mutualists and parasites in a community context. Trends in Ecology and Evolution 22: 120-126.
121. Tilman D. 1982. Resource competition and community structure. Princeton, NJ, USA: Princeton University Press.
122. Tiunov AV, Scheu S. 2005. Facilitative interactions rather than resource partitioning drive diversity-functioning relationships in laboratory fungal communities. Ecology Letters 8: 618-625.
123. Turner TL, Bourne EC, von Wettberg EJ, Hu TT, Nuzhdin SV. 2010. Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nature Genetics 42: 260-263.
124. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604.
125. Van der Heijden MJA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69-72.
126. Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW. 2003. Co-existing grass species have distinctive arbuscular mycorrhizal communities. Molecular Ecology 12: 3085-3095.
127. Vellend M. 2006. The consequences of genetic diversity in competitive communities. Ecology 87: 304-311.
128. Vellend M. 2008. Effects of diversity on diversity: consequences of competition and facilitation. Oikos 117: 1075-1085.
129. Vellend M, Geber MA. 2005. Connections between species diversity and genetic diversity. Ecology Letters 8: 767-781.
130. Vrålstad T, Fossheim T, Schumacher T. 2000. Piceirhiza bicolorata- the ectomycorrhizal expression of the Hymenoscyphus ericae aggregate? New Phytologist 145: 549-563.
131. Vrålstad T, Myhre E, Schumacher T. 2002. Molecular diversity and phylogenetic affinities of symbiotic root-associated ascomycetes of the Helotiales in burnt and metal polluted habitats. New Phytologist 155: 131-148.
132. Whitlock R, Grime JP, Booth R, Burke T. 2007. The role of genotypic diversity in determining grassland community structure under constant environmental conditions. Journal of Ecology 95: 895-907.
133. Whitlock R, Grime JP, Burke T. 2010. Genetic variation in plant morphology contributes to the species-level structure of grassland communities. Ecology 91: 1344-1354.
134. Widén B, Cronberg N, Widén M. 1994. Genotypic diversity molecular markers and spatial distribution of genets in clonal plants, a literature survey. Folia Geobotanica and Phytotaxonomica 29: 245-263.
135. Wilkinson A, Solan M, Taylor AFS, Alexander IJ, Johnson D. 2010. Intraspecific diversity regulates fungal productivity and respiration. PLoS ONE 5: e12604.
136. Wolfe BE, Parrent JL, Koch AM, Sikes BA, Gardes M, Klironomos JN. 2009. Spatial heterogeneity in mycorrhizal populations and communities: scales and mechanisms. In: AzconAguilar C, Barea JM, Gianinazzi-Pearson V, Gianinazzi S, eds. Mycorrhizas - functional processes and ecological impact. Berlin, Germany: Springer-Verlag, 167-185.
137. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M et al. 2004. The worldwide leaf economics spectrum. Nature 428: 821-827.
138. Wu B, Nara K, Hogetsu T. 1999. Competition between ectomycorrhizal fungi colonizing Pinus densiflora. Mycorrhiza 9: 151-159.
139. Zhou ZH, Miwa M, Matsuda Y, Hogetsu T. 2001. Spatial distribution of the subterranean mycelia and ectomycorrhizae of Suillus grevillei genets. Journal of Plant Research 114: 179-185.