Advertisement

Plant and Soil

, Volume 363, Issue 1–2, pp 7–18 | Cite as

How useful is the mutualism-parasitism continuum of arbuscular mycorrhizal functioning?

  • F. Andrew Smith
  • Sally E. Smith
Commentary

Abstract

Background

A recent review in this journal puts forward the premise that our recent studies have resulted in our questioning the validity of the so-called mutualism-parasitism continuum of functioning of arbuscular mycorrhizas. This premise is incorrect and appears largely to result from a misunderstanding of terminology.

Scope and conclusions

We clarify a comment in one of our publications that influenced the previous review, which contains several statements that do not accurately represent our views. Our research has overturned not the continuum concept itself, but some past ideas about the balance of resources traded between AM fungi and plants. Of course, we recognize that outcomes of AM symbiosis in relation to the non-mycorrhizal (NM) state are strongly influenced by many environmental factors. Nevertheless, underlying resource trade is always a key determinant of costs and benefits of the symbiosis for both partners. In this context, we address uncertainties and contradictory ideas about mechanisms, causes, effects and outcomes in AM symbioses that occur in the literature, and issues of relevance of research at different scales. We also discuss semantics that can cause confusion. Finally, we assess how useful the mutualism-parasitism continuum is for design of hypothesis-driven experiments to disentangle the complex interactions that determine growth of AM plants, i.e. the so-called emergent properties.

Keywords

Arbuscular mycorrhizas Benefits Costs Mycorrhizal growth response Resource trade Mutualism Parasitism 

Abbreviations

AM

Arbuscular mycorrhizal

MGR

Mycorrhizal growth response

NM

Non-mycorrhizal

Notes

Acknowledgements

We thank the editors of Plant and Soil for inviting us to produce this contribution, clarify the aims of our research, and explore further some important conceptual issues raised by Johnson and Graham (2012). We are grateful to members of the Adelaide group whose studies have contributed to ideas in “Smiths” papers, to our colleague Iver Jakobsen, to our other co-authors, and not least to other colleagues who are interested in the physiology of AM symbiosis and the extent to which it can be validly extrapolated to higher scales of research.

References

  1. Allen MF, Swenson W, Querejeta JI, Egerton-Warberton LM, Treseder KK (2003) Ecology of mycorrhizae: a conceptual framework for complex interactions among plants and fungi. Annu Rev Phytopathol 41:27–303CrossRefGoogle Scholar
  2. Baylis GTS (1975) The magnolioid mycorrhiza and mycotrophy in root systems derived from it. In: Sanders FE, Mosse B, Tinker PB (eds) Endomycorrhizas. Academic, London, UK, pp 373–389Google Scholar
  3. Bergelson JM, Crawley MJ (1988) Mycorrhizal infection and plant species diversity. Nature 334:202CrossRefGoogle Scholar
  4. Bryla DR, Koide RT (1990) Role of mycorrhizal infection in the growth and reproduction of wild vs. cultivated plants. II. Eight wild accessions and two cultivars of Lycopersicon esculentum Mill. Oecologia 84:82–92CrossRefGoogle Scholar
  5. Burleigh SH, Cavagnaro TR, Jakobsen I (2002) Functional diversity of arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition. J Exp Bot 53:1593–1601PubMedCrossRefGoogle Scholar
  6. Cavagnaro TR, Smith FA, Hay G, Carne-Cavagnaro VL, Smith SE (2004) Inoculum type does not affect overall resistance of an arbuscular mycorrhiza-defective tomato mutant to colonisation but inoculation does change competitive interactions with wild-type tomato. New Phytol 161:485–494CrossRefGoogle Scholar
  7. Daft MJ, Okusanya BO (1973) Effect of Endogone mycorrhiza on plant growth. VI. Influence of infection on the anatomy and reproductive development in four hosts. New Phytol 72:1333–1339CrossRefGoogle Scholar
  8. Diaz S, Cabido M (2001) Vive la differerence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655CrossRefGoogle Scholar
  9. Egger KN, Hibbett DS (2004) The evolutionary implications of exploitation in mycorrhizas. Can J Bot 82:1110–1121CrossRefGoogle Scholar
  10. Facelli E, Smith SE, Facelli JM, Christophersen HM, Smith FA (2010) Underground friends or enemies: model plants help to unravel direct and indirect effects of arbuscular mycorrhizal fungi on plant competition. New Phytol 185:1050–1061PubMedCrossRefGoogle Scholar
  11. Fitter AH (1977) Influence of mycorrhizal infection on competition for phosphorus and potassium by two grasses. New Phytol 79:119–125CrossRefGoogle Scholar
  12. Fitter AH (1985) Functioning of vesicular-arbuscular mycorrhizas under field conditions. New Phytol 99:257–265CrossRefGoogle Scholar
  13. Fitter AH (2006) What is the link between carbon and phosphorus fluxes in arbuscular mycorrhizas? A null hypothesis for symbiotic function. New Phytol 172:3–6PubMedCrossRefGoogle Scholar
  14. Fitter AH, Heinemeyer A, Staddon PL (2000) The impact of elevated CO2 and global climate change on arbuscular mycorrhizas: a mycocentric approach. New Phytol 147:179–187CrossRefGoogle Scholar
  15. Francis R, Read DJ (1995) Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to impacts on plant community structure. Can J Bot 73:S1301–S1309CrossRefGoogle Scholar
  16. Govindarajulu M, Pfeffer P, Jin H, Abubaker J, Douds D, Allen JW, Bucking H, Lammers P, Shachar Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823PubMedCrossRefGoogle Scholar
  17. Grace EJ, Cotsaftis O, Tester M, Smith FA, Smith SE (2009) 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 181:938–949PubMedCrossRefGoogle Scholar
  18. Graham JH (2000) Assessing costs of arbuscular mycorrhizal symbiosis in agroecosystems. In: Podila GK, Douds DD (eds) Current advances in mycorrhizae research. APS Press, St Paul, pp 127–140Google Scholar
  19. Graham JH, Abbott LK (2000) Wheat responses to aggressive and non-aggressive arbuscular mycorrhizal fungi. Plant Soil 220:207–218CrossRefGoogle Scholar
  20. Grime JP, Mackey JML, Hillier SH, Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature 328:420–422CrossRefGoogle Scholar
  21. Grman E, Robinson TMP, Klausmeier CA (2012) Ecological specialization and trade affect the outcome of negotiations in mutualism. Am Nat 179:567–581PubMedCrossRefGoogle Scholar
  22. Helgason T, Fitter AH (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). J Exp Bot 60:2465–2480PubMedCrossRefGoogle Scholar
  23. Hetrick BAD, Wilson GWT, Schwab AP (1994) Mycorrhizal activity in warm- and cool-season grasses: variation in nutrient uptake strategies. Can J Bot 72:1002–1008CrossRefGoogle Scholar
  24. Jakobsen I (1994) Research approaches to study the functioning of vesicular-arbuscular mycorrhizas in the field. Plant Soil 159:141–147Google Scholar
  25. Jakobsen I (1999) Transport of phosphorus and carbon in arbuscular mycorrhizas. In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer, Berlin, pp 309–332Google Scholar
  26. Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 2. Hyphal transport of 32P over defined distances. New Phytol 120:509–516CrossRefGoogle Scholar
  27. Jifon JL, Graham JH, Drouillard DL, Syvertsen JP (2002) Growth depression of mycorrhizal Citrus seedlings grown at high phosphorus supply is mitigated by elevated CO2. New Phytol 153:133–142CrossRefGoogle Scholar
  28. Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647PubMedCrossRefGoogle Scholar
  29. Johnson NC, Graham JH (2012) The continuum concept remains a useful framework for studying mycorrhizal functioning. Plant Soil. doi: 10.1007/s11104-11012-11406-11101
  30. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586CrossRefGoogle Scholar
  31. Jones MD, Smith SE (2004) Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? Can J Bot 82:1089–1109CrossRefGoogle Scholar
  32. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilise cooperation in the mycorrhizal symbiosis. Science 333:880–882PubMedCrossRefGoogle Scholar
  33. Klironomos JN (2000) Host specificity and functional diversity among arbuscular mycorrhizal fungi. In Microbial Biosystems: In: Bell CR, Brylinsky M, Johnson-Green P (eds) New Frontiers: Proceedings of the 8th International Symposium on Microbial Ecology. Atlantic Canada Society for Microbial Ecology, Halifax, Canada, pp 845–851Google Scholar
  34. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301CrossRefGoogle Scholar
  35. Lewis DH (1973) Concepts in fungal nutrition and the origin of biotrophy. Biol Rev 48:261–278CrossRefGoogle Scholar
  36. Lewis DH (1974) Microorganisms and plants: the evolution of parasitism and mutualism. Symp Soc Exp Biol 24:367–392Google Scholar
  37. Li HY, Zhu YG, Marschner P, Smith FA, Smith SE (2005) Wheat responses to arbuscular mycorrhizal fungi in a highly calcareous soil differ from those of clover, and change with plant development and P supply. Plant Soil 277:221–232CrossRefGoogle Scholar
  38. Li H-Y, Smith SE, Holloway RE, Zhu Y-G, Smith FA (2006) Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. New Phytol 172:536–543PubMedCrossRefGoogle Scholar
  39. Manjunath A, Habte M (1991) Root morphological characteristics of host species having distinct mycorrhizal dependency. Can J Bot 69:671–676CrossRefGoogle Scholar
  40. Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364CrossRefGoogle Scholar
  41. Nagy R, Drissner D, Amrhein N, Jakobsen I, Bucher M (2008) Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytol 181:950–959CrossRefGoogle Scholar
  42. Oliver AJ, Smith SE, Nicholas DJD, Wallace W, Smith FA (1983) Activity of nitrate reductase in Trifolium subterraneum: effects of mycorrhizal infection and phosphate nutrition. New Phytol 94:63–79CrossRefGoogle Scholar
  43. Pearson JN, Jakobsen I (1993) The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants measured by dual labelling with 32P and 33P. New Phytol 124:489–494CrossRefGoogle Scholar
  44. Plenchette C, Fortin JA, Furlan V (1983) Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility. I. Mycorrhizal dependency under field conditions. Plant Soil 70:199–209CrossRefGoogle Scholar
  45. Read DJ (2002) Towards ecological relevance-progress and pitfalls in the path towards and understanding of mycorrhizal functions in nature. In: Sanders IR, van der Heijden MGA (eds) Mycorrhizal ecology. Springer, Berlin Heidelberg, pp 3–29Google Scholar
  46. Smith FA, Smith SE (1996) Mutualism and parasitism: diversity in function and structure in the “arbuscular” (VA) mycorrhizal symbiosis. Adv Bot Res 22:1–43CrossRefGoogle Scholar
  47. Smith FA, Smith SE (2011a) What is the significance of the arbuscular mycorrhizal colonisation of many economically important crop plants? Plant Soil 348:63–79CrossRefGoogle Scholar
  48. Smith SE, Smith FA (2011b) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosytems scales. Annu Rev Plant Biol 62:227–250PubMedCrossRefGoogle Scholar
  49. Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20PubMedCrossRefGoogle Scholar
  50. Smith SE, Smith FA, Jakobsen I (2004) 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 162:511–524CrossRefGoogle Scholar
  51. Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182:347–358PubMedCrossRefGoogle Scholar
  52. Smith SE, Jakobsen I, Groenlund M, Smith FA (2011) 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 156:1050–1057PubMedCrossRefGoogle Scholar
  53. Snellgrove RC, Splittstoesser WE, Stribley DP, Tinker PB (1982) The distribution of carbon and the demand of the fungal symbiont in leek plants with vesicular-arbuscular mycorrhizas. New Phytol 92:75–87CrossRefGoogle Scholar
  54. Sudová R (2009) Different growth response of five co-existing stoloniferous plant species to inoculation with native arbuscular mycorrhizal fungi. Plant Ecol 204:135–143CrossRefGoogle Scholar
  55. Thomson BD, Robson AD, Abbott LK (1986) Effects of phosphorus on the formation of mycorrhizas by Gigaspora calospora and Glomus fasciculatum in relation to root carbohydrates. New Phytol 103:751–765CrossRefGoogle Scholar
  56. Tilman D, Knops J, Wedin D, Reich P, Richie M, Siemann E (1997) The influence of functional diversity and composition on ecosystem processes. Science 277:1300–1302CrossRefGoogle Scholar
  57. Trappe JM (1994) What is a mycorrhiza? In: Azcon-Aguilar C, Barea JM (eds) Fourth European Symposium on Mycorrhizae Granada, Spain. Commission of the European Union, Luxemburg, pp 3–6Google Scholar
  58. Urcelay C, Diaz S (2003) The mycorrhizal dependence of subordinates determines the effect of arbuscular mycorrhizal fungi on plant diversity. Ecol Lett 6:388–391CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Soils Group, School of Agriculture, Food and Wine, Waite CampusUniversity of AdelaideAdelaideAustralia

Personalised recommendations