Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales

New Phytologist

Volumn 185, Issue 3, 2010, Pages 631-647

  Johnson, Nancy Collins ^a  

^a NORTHERN ARIZONA UNIVERSITY   (United States)

Author keywords

Arbuscular mycorrhizas; Co adaptation; Ecological stoichiometry; Functional equilibrium; Nitrogen; Phosphorus; Thresholds; Trade balance

Indexed keywords

ADAPTATION; HOST-SYMBIONT INTERACTION; HUMAN ACTIVITY; MYCORRHIZA; NITROGEN; PHOSPHORUS; PLANT COMMUNITY; RESOURCE ALLOCATION; SOIL ECOSYSTEM; STOICHIOMETRY; TRADE-OFF;

ADAPTATION; BIOLOGICAL MODEL; ECOSYSTEM; EVOLUTION; METABOLISM; MYCORRHIZA; REVIEW; SYMBIOSIS;

ADAPTATION, PHYSIOLOGICAL; ECOSYSTEM; EVOLUTION; MODELS, BIOLOGICAL; MYCORRHIZAE; SYMBIOSIS;

ARBUSCULAR; FUNGI;

EID: 74549131772     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2009.03110.x     Document Type: Review

References (160)

1. Abbott LK, Robson AD. 1981. Infectivity and effectiveness of five endomycorrhizal fungi: competition with indigenous fungi in field soils. Australian Journal of Agricultural Research 32 : 621 630.
2. Abbott LK, Robson AD. 1991. Field management of VA mycorrhizal fungi. In : Keister DL, Cregan PB, eds. The rhizosphere and plant growth. Amsterdam, The Netherlands : Kluwer Academic Publishers, 355 362
3. Aerts R. 2002. The role of various types of mycorrhizal fungi in nutrient cycling and plant competition. In : van der Heijden MGA, Sanders I, eds. Mycorrhizal ecology. Berlin Heidelberg, Germany : Springer-Verlag, 117 133.
4. Allen EB, Allen MF. 1990. The mediation of competition by mycorrhizae in successional and patchy environments. In : Grace JB, Tilman D, eds. Perspectives on plant competition. San Diego, CA, USA : Academic Press, 367 385.
5. Allen MF, Boosalis MG. 1983. Effects of two species of vesicular arbuscular fungi on drought tolerance of winter wheat. New Phytologist 93 : 67 76.
6. Allen MF, Swenson W, Querejeta JI, Egerton-Warburton LM, Treseder KK. 2003. Ecology of mycorrhizae: a conceptual framework for complex interactions among plants and fungi. Annual Review of Phytopathology 41 : 271 303.
7. 2 in a chaparral ecosystem. Ecological Applications 15 : 1701 1711.
8. Antoninka A, Wolf J, Bowker MA, Classen AT, Johnson NC. 2009. Linking above- and belowground responses to global change at community and ecosystem scales. Global Change Biology 15 : 914 929.
9. Auge RM. 2001. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11 : 3 42.
10. Azcón R, Ocampo JA. 1981. Factors affecting the vesicular-arbuscular infection and mycorrhizal dependency of thirteen wheat cultivars. New Phytologist 87 : 677 685.
11. Azcón R, Ambrosano E, Charest C. 2003. Nutrient acquisition in mycorrhizal lettuce plants under different phosphorus and nitrogen concentration. Plant Science 165 : 1137 1145.
12. Bååth E, Spokes J. 1989. The effect of added nitrogen and phophorus on mycorrhizal growth response and infection in Allium schoenoprasum. Canadian Journal of Botany 67 : 3227 3232.
13. Bardgett RD, Bowman WD, Kaufman R, Schmidt SK. 2005. A temporal approach to linking aboveground and belowground ecology. Trends in Ecology & Evolution 20 : 634 641.
14. Bardgett RD, Freeman C, Ostle NJ. 2008. Microbial contributions to climate change through carbon cycle feedbacks. International Society for Microbial Ecology Journal 2 : 805 814.
15. Baylis GTS. 1975. The magnolioid mycorrhiza and mycotrophy in root systems derived from it. In : Sanders F, Mosse B, Tinker P, eds. Endomycorrhizas. London, UK : Academic Press, 373 389.
16. Berendse F, Aerts R, Bobbink R. 1993. Atmospheric nitrogen deposition and its impact on terrestrial ecosystems. In : Vos CC, Opdam P, eds. Landscape ecology of a stressed environment. London, UK : Chapman and Hall, 104 121.
17. Bever JD. 2002. Soil community feedback and the coexistence of competitiors: conceptual frameworks and empirical tests. New Phytologist 157 : 465 473.
18. Bever JD, Schultz PA, Pringle A, Morton JB. 2001. Arbuscular mycorrhizal fungi: more diverse than meets the eye, and the ecological tale of why. BioScience 51 : 923 931.
19. Bever JD, Richardson SC, Lawrence BM, Holmes J, Watson M. 2009. Preferential allocation to a beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecology Letters 12 : 13 21.
20. Blanke V, Renker C, Wagner M, Fullner K, Held M, Kuhn AJ, Buscot F. 2005. Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate-polluted field site. New Phytologist 166 : 981 992.
21. Bloom AJ, Chapin FS III., Mooney HA. 1985. Resource limitation in plants: an economic analogy. Annual Review of Ecology and Systematics 16 : 363 393.
22. Bobbink R. 1991. Effects of nutrient enrichment in dutch chalk grassland. Journal of Applied Ecology 28 : 28 41.
23. Brouwer R. 1983. Functional equilibrium: sense or nonsense? Netherlands Journal of Agricultural Science 31 : 335 348.
24. Brundrett MC. 2002. Coevolution of roots and mycorrhizas of land plants. New Phytologist 154 : 275 304.
25. Bucher M. 2007. Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist 173 : 11 26.
26. Chapin FSI, Bloom AJ, Field CB, Waring RH. 1987. Plant responses to multiple environmental factors. BioScience 37 : 49 57.
27. Chaudhary VB, Lau MK, Johnson NC. 2008. Macroecology of microbes - biogeography of the Glomeromycota. In : Vama A. ed. Mycorrhiza. Berlin, Heidelberg, Germany : Springer-Verlag, 529 564.
28. Chaudhary VB, Bowker MA, O'Dell TE, Grace JB, Redman AE, Rillig MC, Johnson NC. 2009. Untangling the biological contributions to soil stability in semiarid shrublands. Ecological Applications 19 : 110 122.
29. Collins CD, Foster BL. 2009. Community-level consequences of mycorrhizae depend on phosphorus availability. Ecology 90 : 2567 2576.
30. Daft MJ, El-Giahmi AA. 1978. Effect of arbuscular mycorrhiza on plant growth. VIII. Effects of defoliation and light on selected hosts. New Phytologist 80 : 365 372.
31. De Deyn GB, Van der Putten WH. 2005. Linking aboveground and belowground diversity. Trends in Ecology & Evolution 20 : 625 633.
32. Douds DD, Schenck NC. 1990. Relationship of colonization and sporulation by VA mycorrhizal fungi to plant nutrient and carbohydrate contents. New Phytologist 116 : 621 627.
33. Egerton-Warburton LM, Allen EB. 2000. Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecological Applications 10 : 484 496.
34. Egerton-Warburton L, Johnson NC, Allen EB. 2007. Mycorrhizal community dynamics following nitrogen fertilization: a cross-site test in five grasslands. Ecological Monographs 77 : 527 577.
35. Eom A-H, Harnett DC, Wilson GWT, Figge DAH. 1999. The effect of fire, mowing and fertilizer amendment on arbuscular mycorrhizas in tallgrass prairie. American Midland Naturalist 142 : 55 70.
36. Eom AH, Hartnett DC, Wilson GWT. 2000. Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122 : 435 444.
37. Ericsson T. 1995. Growth and shoot:root ratio of seedlings in relation to nutrient availability. Plant and Soil 168-169 : 205 214.
38. Fitter AH. 1991. Costs and benefits of mycorrhizas: implications for functioning under natural conditions. Experientia 47 : 350 355.
39. Fitter AH. 2006. What is the link between carbon and phosphorus fluxes in arbuscular mycorrhizas? A null hypothesis for symbiotic function. New Phytologist 172 : 3 6.
40. Garraway MO, Evans RC. 1984. Fungal nutrition and physiology. New York, NY, USA : Wiley & Sons, 401.
41. Gehring CA. 2003. Growth responses to arbuscular mycorrhizae by rain forest seedlings vary with light intensity and tree species. Plant Ecology 167 : 127 139.
42. George E, Romheld V, Marschner H. 1994. Contribution of mycorrhizal fungi to micronutrient uptake by plants. In : Manthey JA, Crowley DE, Luster DG, eds. Biochemistry of metal micronutrients in the rhizosphere. Boca Raton, FL, USA : Lewis Publishers, 93 109.
43. George E, Marschner H, Jakobsen I. 1995. Role of arbuscular mycorrhizal fungi in uptake of phosphorus and nitrogen from soil. Critical Reviews in Biotechnology 15 : 257 270.
44. Govindarajulu M, Pfeffer PE, Jin H, Abudaker J, Douds DD, Allen JA, Bucking H, Lammers PJ, Shachar-Hill Y. 2005. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435 : 819 823.
45. Graham JM. 2008. Scaling-up evaluation of field functioning of arbuscular mycorrhizal fungi. New Phytologist 180 : 1 2.
46. Graham JH, Abbott LK. 2000. Wheat responses to aggressive and non-aggressive arbuscular mycorrhizal fungi. Plant and Soil 220 : 207 218.
47. Graham JH, Eissenstat DM. 1994. Host genotype and the formation and function of VA mycorrhizae. Plant and Soil 159 : 179 185.
48. Graham JH, Leonard RT, Menge JA. 1981. Membrane mediated decrease in root exudation responsible for phosphorus inhibition of vesicular-arbuscular mycorrhizae formation. Plant Physiology 68 : 548 552.
49. Graham JH, Leonard RT, Menge JA. 1982. Interaction of light intensity and soil temperature with phosphorus inhibition of vesicular-arbuscular mycorrhizae formation. New Phytologist 91 : 683 690.
50. Graham JH, Eissenstat DM, Drouillard DL. 1991. On the relationship between a plant's mycorrhizal dependency and rate of vesicular-arbuscular mycorrhizal colonization. Functional Ecology 5 : 773 779.
51. Hardie K. 1985. The effect of removal of extraradical hyphae on water uptake by vesicular-arbuscular mycorrhizal plants. New Phytologist 101 : 677 684.
52. Harrison MJ. 2005. Signaling in the arbuscular mycorrhial symbiosis. Annual Review of Microbiology 59 : 19 42.
53. Hart MM, Reader RJ. 2002. Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytologist 153 : 335 344.
54. Hartnett DC, Wilson GWT. 2002. The role of mycorrhizas in plant community structure and dynamics: Lessons from grasslands. Plant and Soil 244 : 319 331.
55. Hayman DS. 1974. Plant growth responses to va mycorrhiza vi. Effect of light and temperature. New Phytologist 73 : 71 80.
56. van der Heijden MGA, Scheublin TR. 2007. Functional traits in mycorrhizal ecology: their use for predicting the impact of arbuscular mycorrhizal fungal communities on plant growth and ecosystem functioning. New Phytologist 174 : 244 250.
57. van der Heijden MGA, Bardgett RD, van Straalen NM. 2008. The unseen majority: Soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11 : 296 310.
58. Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW. 1998. Ploughing up the wood-wide web? Nature 394 : 431.
59. Hempel S, Renker C, Buscot F. 2007. Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environmental Microbiology 9 : 1930 1938.
60. Hendrix JW, Jones KJ, Nesmith WC. 1992. Control of pathogenic mycorrhizal fungi in maintenance of soil productivity by crop rotation. Journal Production Agriculture 5 : 383 386.
61. Hetrick BAD. 1991. Mycorrhizas and root architecture. Experientia 47 : 355 362.
62. Hetrick BAD, Wilson GWT, Cox TS. 1993. Mycorrhizal dependence of modern wheat cultivars and ancestors: a synthesis. Canadian Journal of Botany 71 : 512 518.
63. Hildebrandt U, Ouziad F, Marner F-J, Bothe H. 2006. The bacterium Paenibacillus validus stimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores. FEMS Microbiology Letters 254 : 258 267.
64. Hodge A, Robinson D, Fitter A. 2000. Are microorganisms more effective than plants at competing for nitrogen? Trends in Plant Science 5 : 304 308.
65. Hoeksema JD, Schwartz MW. 2003. Expanding comparative-advantage biological market models: contingency of mutualism on partners' resouces requirements and acquisition trade-offs. Proceedings of the Royal Society of London B 270 : 913 919.
66. Janos DP. 2007. Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17 : 75 91.
67. Jansa J, Mozafar A, Kuhn G, Ruh R, Sanders IR, Frossard E. 2003. Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecological Applications 13 : 1164 1176.
68. 2. New Phytologist 153 : 133 142.
69. Jin H, Pfeffer PE, Douds DD, Pitotrowski E, Lammers PJ, Shachar-Hill Y. 2005. The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytologist 168 : 687 696.
70. Johnson NC. 1993. Can fertilization of soil select less mutualistic mycorrhizae? Ecological Applications 3 : 749 757.
71. Johnson NC, Copeland PJ, Crookston RK, Pfleger FL. 1992a. Mycorrhizae: Possible explanation for yield decline with continuous corn and soybean. Agronomy Journal 84 : 387 390.
72. Johnson NC, Tilman D, Wedin D. 1992b. Plant and soil controls on mycorrhizal fungal communities. Ecology 73 : 2034 2042.
73. Johnson NC, Graham JH, Smith FA. 1997. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytologist 135 : 575 585.
74. Johnson NC, Rowland DL, Corkidi L, Egerton-Warburton L, Allen EB. 2003. Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84 : 1895 1908.
75. 2 enrichment. Global Change Biology 11 : 1156 1166.
76. Johnson NC, Hoeksema JD, Bever JD, Chaudhary VB, Gehring CA, Klironomos JN, Koide R, Miller RM, Moore J, Moutoglis P et al. 2006. From Lilliput to Brobdingnag: Extending models of mycorrhizal function across scales. BioScience 56 : 889 900.
77. Johnson NC, Rowland DL, Corkidi L, Allen EB. 2008. Characteristics of plant winners and losers in grassland eutrophication - importance of allocation plasticity and mycorrhiza function. Ecology 89 : 2868 2878.
78. Johnson NC, Wilson GWT, Bowker MA, Wilson J, Miller RM in press). Mycorrhizal mutualisms are enhanced when plant and fungal partners are in home soil. Proceedings of the National Academy of Sciences, USA.
79. Kardol P, Bezemer TM, Van der Putten WH. 2006. Temporal variation in plant-soil feedback controls succession. Ecology Letters 9 : 1080 1088.
80. Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE. 2009. Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses Soil Biology and Biochemistry 41 : 1233 1244.
81. Kaye JP, Hart SC. 1997. Competition for nitrogen between plants and soil microorganisms. Trends in Ecology & Evolution 12 : 139 143.
82. Klironomos JN. 2002. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417 : 67 70.
83. 2. New Phytologist 138 : 599 605.
84. Klironomos JN, McCune J, Hart M, Neville J. 2000. The influence of arbuscular mycorrhizae on the relationship between plant diversity and productivity. Ecology Letters 3 : 137 141.
85. 2 overestimates community response in a model plant-soil system. Nature 433 : 21 624.
86. 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.
87. Koerselman W, Meuleman AFM. 1996. The vegetation N:P ratio: A new tool to detect the nature of nutrient limitation. Journal of Applied Ecology 33 : 1441 1450.
88. Koide RT. 1991. Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytologist 117 : 365 386.
89. Koide RT, Dickie IA. 2002. Effects of mycorrhizal fungi on plant populations. Plant and Soil 244 : 307 317.
90. Koide R, Elliot G. 1989. Cost, benefit and efficiency of the vesicular-arbuscular mycorrhizal symbiosis. Functional Ecology 3 : 252 255.
91. Krüger M, Stockinger H, Kruger C, Schussler A. 2009. DNA-based species level detection of glomeromycota: One PCR primer set for all arbuscular mycorhial fungi. New Phytologist 183 : 212 223.
92. Lambers H, Raven JA, Shaver GR, Smith SE. 2008. Plant nutrient-acquisition strategies change with soil age. Trends in Ecology & Evolution 23 : 95 103.
93. Leigh J, Hodge A, Fitter AH. 2008. Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytologist 181 : 199 207.
94. Li H, Smith FA, Dickson S, Holloway RE, Smith SE. 2008. Plant growth depressions in arbuscular mycorrhizl symbioses: Not just caused by carbon drain? New Phytologist 178 : 852 862.
95. Liebig J. 1843. Chemistry in its application to agriculture and physiology. London, UK : Taylor and Walton.
96. Lilleskov EA, Parrent JL. 2007. Can we develop general predictive models of mycorrhizal fungal community - environment relationships? New Phytologist 174 : 250 256.
97. Maherali H, Klironomos JN. 2007. Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316 : 1746 1748.
98. Marschner H, Dell B. 1994. Nutrient uptake in mycorrhizal symbiosis. Plant and Soil 159 : 89 102.
99. Mengel K, Kirkby EA. 1982. Principles of plant nutrition. Warblaufen-Bern, Switzerland : International Potash Institute.
100. Miller RM. 2005. The nonmycorrhizal root - a strategy for survival in nutrient-impoverished soil. New Phytologist 165 : 655 658.
101. Miller RM, Jastrow JD. 2000. Mycorrhizal fungi influence soil structure. In : Kapulnik Y, Douds DD Jr., eds. Arbuscular mycorrhizas: physiology and function. Dordrecht, The Netherlands : Kluwer Academic Publishers, 3 18.
102. Miller RM, Kling M. 2000. The importance of integration and scale in the arbuscular mycorrhizal symbiosis. Plant and Soil 226 : 295 309.
103. Miller RM, Miller SP, Jastrow JD, Rivetta CB. 2002. Mycorrhizal mediated feedbacks influence net carbon gain and nutrient uptake in Andropogon gerardii. New Phytologist 155 : 149 162.
104. Modjo HS, Hendrix JW, Nesmith WC. 1987. Mycorrhizal fungi in relation to control of tobacco stunt disease with soil fumigants. Soil Biology and Biochemistry 19 : 289 295.
105. Mosse B. 1973. Plant growth responses to vesicular-arbuscular mycorrhizas. IV. In soil given additional phosphorus. New Phytologist 72 : 127 136.
106. 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.
107. Newsham K, Fitter A, Watkinson A. 1995. Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends in Ecology & Evolution 10 : 407 411.
108. Olsson PA, Thingstrup I, Jakobsen I, Baath E. 1999. Estimation of the biomass of arbuscular mycorrhizal fungi in a linseed field. Soil Biology and Biochemistry 31 : 1879 1887.
109. Öpik M, Metsis M, Daniell TJ, Moora M. 2009. Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a borenemoral forest. New Phytologist 184 : 424 437.
110. Parniske M. 2008. Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nature Reviews Microbiology 6 : 763 775.
111. Pfeffer PE, Douds DD, Bucking H, Schwartz DP, Shachar-Hill Y. 2004. The fungus does not transfer carbon to or between roots in an arbucsular mycorrhizal symbiosis. New Phytologist 163 : 617 627.
112. Piotrowski JS, Denich T, Klironomos JN, Graham JM, Rillig MC. 2004. The effects of arbuscular mycorrhizas on soil aggregation depend on the interaction between plant and fungal species. New Phytologist 164 : 365 373.
113. Pirozynski KA, Malloch DW. 1975. The origin of land plants: a matter of mycotrophism. Biosystems 6 : 153 164.
114. van der Ploeg RR, Böhm W, Kirkham MB. 1999. On the origin of the theory of mineral nutrition of plants and the law of the minimum. Soil Science Society of America Journal 63 : 1055 1062.
115. Porras-Alfaro A, Herrera J, Natvig DO, Sinsabaugh RL. 2007. Effect of long-term nitrogen fertilization on mycorrhizal fungi associated with a dominant grass in a semiarid grassland. Plant and Soil 296 : 65 75.
116. van der Putten WH, Van Dijk c, Peters BAM. 1993. Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362 : 53 56.
117. van der Putten WH, Vet LEM, Harvey JA, Wackers FL. 2001. Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends in Ecology & Evolution 16 : 547 554.
118. Pyke GH. 1984. Optimal foraging theory: a critical review. Annual Review of Ecology and Systematics 15 : 523 575.
119. Read DJ. 1991a. Mycorrhizas in ecosystems. Experientia 47 : 376 391.
120. Read DJ. 1991b. Mycorrhizas in ecosystems - nature's response to the "law of the minimum". In : Hawksworth DL, ed. Frontiers in mycology. Kew Surrey, UK : CAB International, 101 130.
121. Read DJ. 2002. Towards ecological relevance - progress and pitfalls in the path towards an understanding of mycorrhzal functions in nature. In : van der Heijden MGA, Sanders IR, eds. Mycorrhizal ecology. Berlin, Heidelberg, Germany : Springer-Verlag, 3 29.
122. Read DJ, Perez-Moreno J. 2003. Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? New Phytologist 157 : 475 492.
123. Redecker D, Kodner R, Graham LE. 2000. Glomalean fungi from the ordovician. Science 289 : 1920 1921.
124. Reinhardt D. 2007. Programming good relations - development of the arbuscular mycorrhizal symbiosis. Current Opinions in Plant Biology 10 : 98 105.
125. Reynolds HL, Packer A, Bever A, Clay K. 2003. Grassroots ecology: Plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84 : 2281 2291.
126. Reynolds HL, Hartley AE, Vogelsang KM, Bever JD, Schultz PA. 2005. Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture. New Phytologist 167 : 869 880.
127. Rillig MC. 2004. Arbuscular mycorrhize and terrestrial ecosystem processes. Ecology Letters 7 : 740 754.
128. Rillig MC, Mummey DL. 2006. Mycorrhizas and soil structure. New Phytologist 171 : 41 53.
129. 2. Plant and Soil 187 : 229 248.
130. Rosendahl S. 2008. Communities, populations and individuals of arbuscular mycorrhizal fungi. New Phytologist 178 : 253 266.
131. Sanders IR. 2002. Ecology and evolution of multigenomic arbuscular mycorrhizal fungi. American Naturalist Supplement 160 : s128 s141.
132. Sanders IR. 2004. Plant and arbuscular mycorrhizal fungal diversity - are we looking at the relevant levels of diversity and are we using the right techniques? New Phytologist 164 : 415 418.
133. Sanders IR, Fitter A. 1992. Evidence for differential responses between host-fungus combinations of vesicular-arbuscular mycorrhizas from a grassland. Mycological Research 96 : 415 419.
134. 2 enrichment. Oecologia 117 : 496 503.
135. Schenck NC, Kinloch RA. 1980. Incidence of mycorrhizal fungi on six field crops in monoculture on a newly cleared woodland site. Mycologia 72 : 445 456.
136. Schroeder MS, Janos DP. 2004. Phosphorus and intraspecific density alter plant responses to arbuscular mycorrhizas. Plant and Soil 264 : 335 348.
137. Schultz PA, Miller RM, Jastrow JD, Rivetta CV, Bever JD. 2001. Evidence of a mycorrhizal mechanism for the adaptation of Andropogon gerardii (poaceae) to high- and low-nutrient prairies. American Journal of Botany 88 : 1650 1656.
138. Schwartz M, Hoeksema J. 1998. Specialization and resource trade: Biological markets as a model of mutualisms. Ecology 79 : 1029 1038.
139. Schweiger P, Robson AD, Barrow NJ. 1995. Root hair length determines beneficial effect of a Glomus species on shoot growth of some pasture species. New Phytologist 131 : 247 254.
140. Shachar-Hill Y. 2007. Quantifying flows through metabolic networks and the prospects for fluxomic studies of mycorrhizas. New Phytologist 174 : 235 240.
141. Smith VH, Holt RD. 1996. Resource competition and within-host disease dynamics. Trends in Ecology & Evolution 11 : 386 389.
142. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. New York, NY, USA : Academic Press.
143. Smith FA, Grace EJ, Smith SE. 2009. More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytologist 182 : 347 358.
144. Staddon P, Fitter A. 1998. Does elevated atmospheric carbon dioxide affect arbuscular mycorrhizas? Trends in Ecology & Evolution 13 : 455 458.
145. Sterner RW, Elser JJ. 2002. Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton, NJ, USA : Princeton University Press.
146. Stubblefield SP, Taylor TN, Trappe JM. 1987. Fossil mycorrhizae: a case for symbiosis. Science 237 : 59 60.
147. Sylvia DM, Neal LH. 1990. Nitrogen affects the phosphorus response of va mycorrhiza. New Phytologist 115 : 303 310.
148. Thompson JP. 1990. Soil sterilization methods to show VA-mycorrhizae aid P and Zn nutrition of wheat in vertisols. Soil Biology and Biochemistry 22 : 229 240.
149. Thrall PH, Hochbert ME, Burdon JJ, Bever JD. 2006. Coevolution of symbiotic mutualists and parasites in a community context. Trends in Ecology & Evolution 22 : 120 126.
150. Tilman D. 1982. Resource competition and community structure. Princeton, NJ, USA : Princeton University Press.
151. Tilman D. 1988. Plant strategies and the dynamics and structure of plant communities. Princeton, NJ, USA : Princeton University Press.
152. 2 in field studies. New Phytologist 164 : 347 355.
153. 2. Ecosystems 6 : 786 796.
154. Tu C, Booker FL, Watson DM, Chen X, Rufty TW, Shi W, Hu S. 2006. Mycorrhizal mediation of plant N acquisition and residue edecomposition: Impact of mineral N inputs. Global Change Biology 12 : 793 803.
155. Valentine AJ, Osborne BA, Mitchell DT. 2001. Interactions between phosphorus supply and total nutrient availability on mycorrhizal colonization, growth and photosynthesis of cucumber. Scientia Horticulturae 88 : 177 189.
156. Waksman SA, Tenney FG. 1927. The composition of natural organic materials and their decomposition in the soil II: Influence of age of plant upon the rapidity and nature of its decomposition - rye plant. Soil Science 24 : 317 333.
157. Wallander H. 1995. A new hypothesis to explain allocation of dry matter between mycorrhizal fungi and pine seedlings in relation to nutrient supply. Plant and Soil 168-169 : 243 248.
158. Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, LeRoy CJ, Lonsdorf EV, Allan GJ, DiFazio SP, Potts BM et al. 2006. A framework for community and ecosystem genetics: From genes to ecosystems. Nature Reviews Genetics 7 : 511 523.
159. Wilson GWT, Rice CW, Rillig MC, Springer A, Hertnett DC. 2009. Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhial fungi: Results fom long-term field experiments. Ecology Letters 12 : 452 461.
160. Wolf J, Johnson NC, Rowland DL, Reich PB. 2003. Elevated carbon dioxide and plant species richness impact arbuscular mycorrhizal fungal spore communities. New Phytologist 157 : 579 588.