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Regulation of resource exchange in the arbuscular mycorrhizal symbiosis

Nature Plants volume 1, Article number: 15159 (2015) Cite this article

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Abstract

Arbuscular mycorrhizal (AM) fungi are one of the most important groups of plant symbionts. These fungi provide mineral nutrients to plants in exchange for carbon. Although substantial amounts of resources are exchanged, the factors that regulate trade in the AM symbiosis are poorly understood. Recent evidence for the reciprocally regulated exchange of resources by AM fungi and plants has led to the suggestion that these symbioses operate according to biological market dynamics, in which interactions are viewed from an economic perspective, and the most beneficial partners are favoured. Here we present five arguments that challenge the importance of reciprocally regulated exchange, and thereby market dynamics, for resource exchange in the AM symbiosis, and suggest that such reciprocity is only found in a subset of symbionts, under specific conditions. We instead propose that resource exchange in the AM symbiosis is determined by competition for surplus resources, functional diversity and sink strength.

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Figure 1: Mycorrhizal responsiveness of different plant species co-occurring in experimental plant communities inoculated with different AM fungi.
Figure 2: Exchange of carbon for soil nutrients in arbuscular mycorrhizal symbiosis.

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References

  1. Fitter, A. H. Darkness visible: reflections on underground ecology. J. Ecol. 93, 231–243 (2005).

    Article  Google Scholar 

  2. Wang, B. & Qiu, Y. L. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363 (2006).

    Article  CAS  PubMed  Google Scholar 

  3. Drigo, B., Pijl, A. & Duyts, H. Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2 . Proc. Natl Acad. Sci. 107, 10938–10942 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Van der Heijden, M. G. A., Martin, F. M., Selosse, M.-A. & Sanders, I. R. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 205, 1406–1423 (2015).

    Article  CAS  PubMed  Google Scholar 

  5. Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis. (Academic, 2008).

    Google Scholar 

  6. Selosse, M.-A. & Le Tacon, F. The land flora: A phototroph-fungus partnership? Trends Ecol. Evol. 13, 15–19 (1998).

    Article  CAS  PubMed  Google Scholar 

  7. Kiers, E. T. & Denison, R. F. Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu. Rev. Ecol. Evol. Syst. 39, 215–236 (2008).

    Article  Google Scholar 

  8. Hoeksema, J. D. et al. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol. Lett. 13, 394–407 (2010).

    Article  PubMed  Google Scholar 

  9. Klironomos, J. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84, 2292–2301 (2003).

    Article  Google Scholar 

  10. Johnson, N. C., Graham, J. H. & Smith, F. A. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 135, 575–586 (1997).

    Article  Google Scholar 

  11. Bever, J. D., Morton, J. B., Antonovics, J. & Schultz, P. A. Host-dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. J. Ecol. 84, 71–82 (1996).

    Article  Google Scholar 

  12. Kiers, E. T. et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880–882 (2011).

    Article  CAS  PubMed  Google Scholar 

  13. Noë, R. & Hammerstein, P. Biological markets. Trends Ecol. Evol. 10, 336–9 (1995).

    Article  PubMed  Google Scholar 

  14. Schwartz, M. W. & Hoeksema, J. D. Specialization and resource trade: Biological markets as a model of mutualisms. Ecology 79, 1029–1038 (1998).

    Article  Google Scholar 

  15. Werner, G. D. A. et al. Evolution of microbial markets. Proc. Natl Acad. Sci. 111, 1237–1244 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Axelrod, R. & Hamilton, W. D. The evolution of cooperation. Science 211, 1390–1396 (1981).

    Article  CAS  PubMed  Google Scholar 

  17. Selosse, M.-A. & Rousset, F. The plant-fungal marketplace. Science 333, 828–829 (2011).

    Article  CAS  PubMed  Google Scholar 

  18. Archetti, M. & Scheuring, I. Coexistence of cooperation and defection in public goods games. Evolution 65, 1140–8 (2011).

    Article  PubMed  Google Scholar 

  19. Bücking, H. & Shachar-Hill, Y. Y. Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimulated by increased carbohydrate availability. New Phytol. 165, 899–912 (2005).

    Article  PubMed  CAS  Google Scholar 

  20. Lekberg, Y., Hammer, E. C. & Olsson, P. A. Plants as resource islands and storage units - adopting the mycocentric view of arbuscular mycorrhizal networks. FEMS Microbiol. Ecol. 74, 336–345 (2010).

    Article  CAS  PubMed  Google Scholar 

  21. Hammer, E. C., Pallon, J., Wallander, H. & Olsson, P. A. Tit for tat? A mycorrhizal fungus accumulates phosphorus under low plant carbon availability. FEMS Microbiol. Ecol. 76, 236–244 (2011).

    Article  CAS  PubMed  Google Scholar 

  22. Fellbaum, C. R. et al. Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc. Natl Acad. Sci. 109, 2666–2671 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Fellbaum, C. R. et al. Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytol. 203, 646–656 (2014).

    Article  CAS  PubMed  Google Scholar 

  24. Bever, J. D., Richardson, S. C., Lawrence, B. M., Holmes, J. & Watson, M. Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecol. Lett. 12, 13–21 (2009).

    Article  PubMed  Google Scholar 

  25. Fitter, A. H. What is the link between carbon and phosphorus fluxes in arbuscular mycorrhizas? A null hypothesis for symbiotic function. New Phytol. 172, 3–6 (2006).

    Article  CAS  PubMed  Google Scholar 

  26. Drew, M. C. Comparison of effects of a localized supply of phosphate, nitrate, ammonium and potassium on growth of seminal root system, and shoot, in barley. New Phytol. 75, 479–490 (1975).

    Article  CAS  Google Scholar 

  27. Leake, J. R. Myco-heterotroph/epiparasitic plant interactions with ectomycorrhizal and arbuscular mycorrhizal fungi. Curr. Opin. Plant Biol. 7, 422–428 (2004).

    Article  CAS  PubMed  Google Scholar 

  28. Courty, P.-E. et al. Carbon and nitrogen metabolism in mycorrhizal networks and mycoheterotrophic plants of tropical forests: a stable isotope analysis. Plant Physiol. 156, 952–961 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Imhof, S. Root morphology, anatomy and mycotrophy of the achlorophyllous Voyria aphylla (Jacq.) Pers.(Gentianaceae). Mycorrhiza 9, 33–39 (1999).

    Article  Google Scholar 

  30. Peng, S., Eissenstat, D. M., Graham, J. H., Williams, K. & Hodge, N. C. Growth depression in mycorrhizal citrus at high-phosphorus supply (analysis of carbon costs). Plant Physiol. 101, 1063–1071 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Wilson, G. W. T. & Hartnett, D. C. Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am. J. Bot. 85, 1732–1738 (1998).

    Article  CAS  PubMed  Google Scholar 

  32. Veiga, R. S. L., Jansa, J., Frossard, E. & van der Heijden, M. G. A. Can arbuscular mycorrhizal fungi reduce the growth of agricultural weeds? PLoS ONE 6, e27825 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Smith, S. E., Smith, F. A. & Jakobsen, I. Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol. 162, 511–524 (2004).

    Article  Google Scholar 

  34. Grace, E. J., Cotsaftis, O., Tester, M., Smith, F. A. & Smith, S. E. Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter genes. New Phytol. 181, 938–49 (2009).

    Article  CAS  PubMed  Google Scholar 

  35. Lekberg, Y. & Koide, R. T. Integrating physiological, community, and evolutionary perspectives on the arbuscular mycorrhizal symbiosis. Botany 92, 241–251 (2014).

    Article  CAS  Google Scholar 

  36. Sanders, I. R. in Mycorrhizal Ecology (eds Van der Heijden, M. G. A. & Sanders, I. R. ), 415–440 (Springer, 2002).

    Book  Google Scholar 

  37. Law, R. & Koptur, S. On the evolution of non-specific mutualism. Biol. J. Linn. Soc. 27, 251–267 (1986).

    Article  Google Scholar 

  38. Bshary, R. & Bronstein, J. L. Game structures in mutualistic interactions: what can the evidence tell us about the kind of models we need? Adv. Study Behav. 34, 59–101 (2004).

    Article  Google Scholar 

  39. Kiers, E. T., Rousseau, R. A., West, S. A. & Denison, R. F. Host sanctions and the legume–rhizobium mutualism. Nature 425, 78–81 (2003).

    Article  CAS  PubMed  Google Scholar 

  40. Pellmyr, O. & Huth, C. J. Evolutionary stability of mutualism between yuccas and yucca moth. Nature 372, 257–260 (1994).

    Article  CAS  Google Scholar 

  41. Jandér, K. C. & Herre, E. A. Host sanctions and pollinator cheating in the fig tree–fig wasp mutualism. Proc. R. Soc. Biol. Sci. 277, 1481–1488 (2010).

    Article  Google Scholar 

  42. Poisot, T., Bever, J. D., Nemri, A., Thrall, P. H. & Hochberg, M. E. A conceptual framework for the evolution of ecological specialisation. Ecol. Lett. 14, 841–51 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Brundrett, M. C. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320, 37–77 (2009).

    Article  CAS  Google Scholar 

  44. Öpik, M. et al. Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23, 411–30 (2013).

    Article  PubMed  Google Scholar 

  45. Kõljalg, U. et al. Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 22, 5271–5277 (2013).

    Article  PubMed  CAS  Google Scholar 

  46. Helgason, T. et al. Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. J. Ecol. 90, 371–384 (2002).

    Article  Google Scholar 

  47. Vandenkoornhuyse, P., Ridgway, K. P., Watson, I. J., Fitter, A. H. & Young, J. P. W. Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol. Ecol. 12, 3085–3095 (2003).

    Article  CAS  PubMed  Google Scholar 

  48. Ohsowski, B. M., Zaitsoff, P. D., Öpik, M. & Hart, M. M. Where the wild things are: looking for uncultured Glomeromycota. New Phytol. 204, 171–179 (2014).

    Article  PubMed  Google Scholar 

  49. Helgason, T. & Fitter, A. H. Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). J. Exp. Bot. 60, 2465–2480 (2009).

    Article  CAS  PubMed  Google Scholar 

  50. Öpik, M., Metsis, M. & Daniell, T. J. Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytol. 184, 424–437 (2009).

    Article  PubMed  CAS  Google Scholar 

  51. Torrecillas, E., Alguacil, M. M. & Roldán, a. Host preferences of arbuscular mycorrhizal fungi colonizing annual herbaceous plant species in semiarid Mediterranean prairies. Appl. Envir. Microbiol. 78, 6180–6 (2012).

    Article  CAS  Google Scholar 

  52. Montesinos-Navarro, A., Segarra-Moragues, J. G., Valiente-Banuet, A. & Verdú, M. The network structure of plant–arbuscular mycorrhizal fungi. New Phytol. 194, 536–547 (2012).

    Article  CAS  PubMed  Google Scholar 

  53. Van der Heijden, M. G. A. et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72 (1998).

    Article  CAS  Google Scholar 

  54. Bever, J. D. et al. Rooting theories of plant community ecology in microbial interactions. Trends Ecol. Evol. 25, 468–478 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Newman, E. I. Mycorrhizal links between plants: their functioning and ecological signifcance. Adv. Ecol. Res. 18 243–270 (1988).

    Article  Google Scholar 

  56. Hart, M. M. et al. Hiding in a crowd—does diversity facilitate persistence of a low-quality fungal partner in the mycorrhizal symbiosis? Symbiosis 59, 47–56 (2012).

    Article  Google Scholar 

  57. Smith, F. A. & Smith, S. E. Mutualism and parasitism: diversity in function and structure in the “arbuscular” (VA) mycorrhizal symbiosis. Adv. Bot. Res. 22, 1–43 (1996).

  58. Harrison, M. J., Dewbre, G. R. & Liu, J. Y. A phosphate transporter from Medicago truncatula involved in the acquisiton of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14, 2413–2429 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Kobae, Y., Tamura, Y., Takai, S., Banba, M. & Hata, S. Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol. 51, 1411–1415 (2010).

    Article  CAS  PubMed  Google Scholar 

  60. Hodge, A., Helgason, T. & Fitter, A. H. Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol. 3, 267–273 (2010).

    Article  Google Scholar 

  61. Helber, N. et al. A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23, 3812–3823 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Floss, D. S., Levy, J. G., Lévesque-Tremblay, V., Pumplin, N. & Harrison, M. J. DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc. Natl Acad. Sci. 110, E5025–E5034 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Walder, F. et al. Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol. 159, 789–797 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Grime, J. P., Mackey, J. M. L., Hillier, S. H. & Read, D. J. Floristic diversity in a model system using experimental microcosms. Nature 328, 420–422 (1987).

    Article  Google Scholar 

  65. Munkvold, L., Kjøller, R., Vestberg, M., Rosendahl, S. & Jakobsen, I. High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol. 164, 357–364 (2004).

    Article  PubMed  Google Scholar 

  66. Koch, A. M. et al. High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi. Proc. Natl Acad. Sci. 101, 2369–2374 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Ravnskov, S. & Jakobsen, I. Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. New Phytol. 129, 611–618 (1995).

    Article  Google Scholar 

  68. Lendenmann, M. et al. Symbiont identity matters: carbon and phosphorus fluxes between Medicago truncatula and different arbuscular mycorrhizal fungi. Mycorrhiza 21, 689–702 (2011).

    Article  CAS  PubMed  Google Scholar 

  69. Smith, S. E., Jakobsen, I., Gronlund, M. & Smith, F. A. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: Interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 156, 1050–1057 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Newsham, K., Fitter, A. H. & Watkinson, A. R. Multi-funcionality and biodiversity in arbuscular micorrhizas. Trends Ecol. Evol. 10, 407–411 (1995).

    Article  CAS  PubMed  Google Scholar 

  71. Jandér, C. K., Herre, E. A., Simms, E. L. & Irwin, R. Precision of host sanctions in the fig tree-fig wasp mutualism: consequences for uncooperative symbionts. Ecol. Lett. 15, 1362–9 (2012).

    Article  Google Scholar 

  72. Heil, M. et al. Divergent investment strategies of Acacia myrmecophytes and the coexistence of mutualists and exploiters. Proc. Natl Acad. Sci. 106, 18091–18096 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Grman, E. Plant species differ in their ability to reduce allocation to non-beneficial arbuscular mycorrhizal fungi. Ecology 93, 711–718 (2012).

    Article  PubMed  Google Scholar 

  74. Zheng, C., Ji, B., Zhang, J., Zhang, F. S. & Bever, J. D. Shading decreases plant carbon preferential allocation towards the most beneficial mycorrhizal mutualist. New Phytol. 205, 361–368 (2015).

    Article  CAS  PubMed  Google Scholar 

  75. Bever, J. D. Soil community feedback and the coexistence of competitiors: conceptual framewords and empirical tests. New Phytol. 157, 465–473 (2003).

    Article  PubMed  Google Scholar 

  76. Bever, J. D. Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc. R. Soc. Lond. B 269, 2595–2601 (2002).

    Article  Google Scholar 

  77. Fortin, J. A. et al. Arbuscular mycorrhiza on root-organ cultures. Can. J. Bot. 80, 1–20 (2002).

    Article  CAS  Google Scholar 

  78. Bever, J. D. Preferential allocation, physio-evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts. New Phytol. 205, 1503–1514 (2015).

    Article  CAS  PubMed  Google Scholar 

  79. Simard, S. W. & Durall, D. M. Mycorrhizal networks: a review of their extent, function, and importance. Can. J. Bot. 82, 1140–1165 (2004).

    Article  CAS  Google Scholar 

  80. Kytoviita, M. M., Vestberg, M. & Tuom, J. A test of mutual aid in common mycorhizal networks: established vegetation negates benefit in seedlings. Ecology 84, 898–906 (2003).

    Article  Google Scholar 

  81. Merrild, M. P., Ambus, P., Rosendahl, S. & Jakobsen, I. Common arbuscular mycorrhizal networks amplify competition for phosphorus between seedlings and established plants. New Phytol. 200, 229–40 (2013).

    Article  CAS  PubMed  Google Scholar 

  82. Weremijewicz, J. & Janos, D. P. Common mycorrhizal networks amplify size inequality in Andropogon gerardii monocultures. New Phytol. 198, 203–13 (2013).

    Article  CAS  PubMed  Google Scholar 

  83. Walder, F. et al. Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. New Phytol. 205, 1632–1645 (2015).

    Article  CAS  PubMed  Google Scholar 

  84. Egger, K. N. & Hibbett, D. S. D. S. The evolutionary implications of exploitation in mycorrhizas. Can. J. Bot. 82, 1110–1121 (2004).

    Article  Google Scholar 

  85. Corrêa, A., Gurevitch, J., Martins-Loucao, M. A. & Cruz, C. C allocation to the fungus is not a cost to the plant in ectomycorrhizae. Oikos 121, 449–463 (2012).

    Article  Google Scholar 

  86. Bryla, D. R. & Eissenstat, D. M. in Advances in Photosynthesis and Respiration (eds Lambers, H. & Ribas-Carbo, H. ) 207–224 (Springer, 2005).

    Google Scholar 

  87. Poorter, H. & De Jong, R. O. B. A comparison of specific leaf area, chemical composition and leaf construction costs of field plants from 15 habitats differing in productivity. New Phytol. 143, 163–176 (1999).

    Article  CAS  Google Scholar 

  88. Kiers, E. T. & van der Heijden, M. G. A. Mutualistic stability in the arbuscular mycorrhizal symbiosis: exploring hypotheses of evolutionary cooperation. Ecology 87, 1627–1636 (2006).

    Article  PubMed  Google Scholar 

  89. Corrêa, A., Cruz, C. & Ferrol, N. Nitrogen and carbon/nitrogen dynamics in arbuscular mycorrhiza: the great unknown. Mycorrhiza http://dx.doi.org/10.1007/s00572-015-0627-6 (2015)

  90. Smith, F. A. & Smith, S. E. How harmonious are arbuscular mycorrhizal symbioses? Inconsistent concepts reflect different mindsets as well as results. New Phytol. 205, 1381–1384 (2015).

    Article  PubMed  Google Scholar 

  91. Archetti, M. & Scheuring, I. Trading public goods stabilizes interspecific mutualism. J. Theor. Biol. 318, 58–67 (2013).

    Article  PubMed  Google Scholar 

  92. Fayle, T. M. et al. Public goods, public services and by-product mutualism in an ant-fern symbiosis. Oikos 121, 1279–1286 (2012).

    Article  Google Scholar 

  93. Johnson, N. C. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol. 185, 631–647 (2010).

    Article  CAS  PubMed  Google Scholar 

  94. Johnson, N. C., Wilson, G. W. T., Bowker, M. A., Wilson, J. A. & Miller, R. M. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc. Natl Acad. Sci. 107, 2093–2098 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Bronstein, J. L. The exploitation of mutualisms. Ecol. Lett. 4, 277–287 (2001).

    Article  Google Scholar 

  96. Van der Heijden, M. G. A. & Horton, T. R. Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J. Ecol. 97, 1139–1150 (2009).

    Article  Google Scholar 

  97. Field, K. J. et al. From mycoheterotrophy to mutualism: mycorrhizal specificity and functioning in Ophioglossum vulgatum sporophytes. New Phytol. 205, 1492–1502 (2015).

    Article  CAS  PubMed  Google Scholar 

  98. Palmer, T. M. et al. Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proc. Natl Acad. Sci. 107, 17234–9 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank S. Pellkofer and K. Hartman for assistance in copyediting the manuscript, and Manu Magic Meyer for contributing artwork for Fig. 2. We also thank A. Fitter for constructive comments. This work was supported by Agroscope, the Swiss National Science Foundation (grant 143097) and the EU project OSCAR.

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Authors and Affiliations

  1. Plant–Soil Interactions, Institute for Sustainability Sciences, Agroscope, Zürich, 8046, Switzerland

    Florian Walder & Marcel G.A. van der Heijden

  2. Institute of Evolutionary Biology and Environmental Studies, University of Zürich, Zürich, 8057, Switzerland

    Marcel G.A. van der Heijden

  3. Plant–Microbe Interactions, Institute of Environmental Biology, Faculty of Science, Utrecht University, Utrecht, 3584 CH, The Netherlands

    Marcel G.A. van der Heijden

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  1. Florian Walder
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F.W. and M.G.A.v.d.H. co-wrote and edited the paper and generated the figures.

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Correspondence to Florian Walder or Marcel G.A. van der Heijden.

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Walder, F., van der Heijden, M. Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nature Plants 1, 15159 (2015). https://doi.org/10.1038/nplants.2015.159

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