, Volume 26, Issue 1, pp 77–83 | Cite as

Evidence for functional redundancy in arbuscular mycorrhizal fungi and implications for agroecosystem management

  • Paul Gosling
  • Julie Jones
  • Gary D. Bending
Short Note


Arbuscular mycorrhizal (AM) fungi provide benefits to host plants and show functional diversity, with evidence of functional trait conservation at the family level. Diverse communities of AM fungi ought therefore to provide increased benefits to the host, with implications for the management of sustainable agroecosystems. However, this is often not evident in the literature, with diversity saturation at low species number. Growth and nutrient uptake were measured in onions in the glasshouse on AM-free phosphorus (P)-poor soil, inoculated with between one and seven species of AM fungi in all possible combinations. Inoculation with AM fungi increased shoot dry weight as well as P and copper concentrations in shoots but reduced the concentration of potassium and sulphur. There was little evidence of increased benefit from high AM fungal diversity, and increasing diversity beyond three species did not result in significantly higher shoot weight or P or Cu concentrations. Species of Glomeraceae had the greatest impact on growth and nutrient uptake, while species of Acaulospora and Racocetra did not have a significant impact. Failure to show a benefit from high AM fungal diversity in this and other studies may be the result of experimental conditions, with the benefits of AM fungal diversity only becoming apparent when the host plant is faced with multiple stress factors. Replicating the complex interactions between AM fungi, the host plant and their environment in the laboratory in order to fully understand these interactions is a major challenge to AM research.


Arbuscular mycorrhiza Fungal diversity Phosphorus Onion 



Thanks to the UK Department of Food, Environment and Rural Affairs for funding and Chris Walker for assistance in preparation of AM inoculum.

Supplementary material

572_2015_651_MOESM1_ESM.docx (17 kb)
ESM 1 (DOCX 17 kb)


  1. Afkhami ME, Rudgers JA, Stachowicz JJ (2014) Multiple mutualist effects: conflict and synergy in multispecies mutualisms. Ecology 95:833–844PubMedCrossRefGoogle Scholar
  2. Aurélien R, Alexandre C, Caroline A, Sanders IR (2013) Relatedness among arbuscular mycorrhizal fungi drives plant growth and intraspecific fungal coexistence. ISME J 7:2137–2146CrossRefGoogle Scholar
  3. Bennett AE, Bever JD (2007) Mycorrhizal species differentially alter plant growth and response to herbivory. Ecology 88:210–218PubMedCrossRefGoogle Scholar
  4. Brussaard L, Ruiter PC, de Brown GG (2007) Soil biodiversity for agricultural sustainability. Agric Ecosyst Environ 121:233–244CrossRefGoogle Scholar
  5. Dai M, Hamel C, Bainard LD, Arnaud MS, Grant CA, Lupwayi NZ, Malhi SS, Lemke R (2014) Negative and positive contributions of arbuscular mycorrhizal fungal taxa to wheat production and nutrient uptake efficiency in organic and conventional systems in the Canadian prairie. Soil Biol Biochem 74:156–166CrossRefGoogle Scholar
  6. Dickie IA, Alexander I, Lennon S, Öpik M, Selosse MA, van der Heijden MGA, Martin FM (2015) Evolving insights to understanding mycorrhizas. New Phytol 205:1369–1374PubMedCrossRefGoogle Scholar
  7. Galvan GA, Paradi I, Burger K, Baar J, Kuyper TW, Scholten OE, Kik C (2009) Molecular diversity of arbuscular mycorrhizal fungi in onion roots from organic and conventional farming systems in the Netherlands. Mycorrhiza 19:317–328PubMedPubMedCentralCrossRefGoogle Scholar
  8. VSN International (2013) GenStat for Windows (13th edn). VSN International, Hemel HempsteadGoogle Scholar
  9. Gosling P, Ozaki A, Jones J, Turner M, Rayns F, Bending GD (2010) Organic management of tilled agricultural soils results in a rapid increase in colonisation potential and spore populations of arbuscular mycorrhizal fungi. Agric Ecosyst Environ 139:273–279CrossRefGoogle Scholar
  10. Gosling P, Mead A, Proctor M, Hammond J, Bending GD (2013) Contrasting arbuscular mycorrhizal communities colonising different host plants show a similar response to a soil phosphorus concentration gradient. New Phytol 198:546–556PubMedPubMedCentralCrossRefGoogle Scholar
  11. Gosling P, Proctor M, Jones J, Bending GD (2014) Distribution and diversity of Paraglomus spp in tilled agricultural soils. Mycorrhiza 24:1–11PubMedCrossRefGoogle Scholar
  12. Grace C, Stribley DP (1991) A safer procedure for routine staining of vesicular-arbuscular mycorrhizal fungi. Mycol Res 95:1160–1162CrossRefGoogle Scholar
  13. Hart MM, Forsythe JA (2012) Using arbuscular mycorrhizal fungi to improve the nutrient quality of crops; nutritional benefits in addition to phosphorus. Sci Hort Amsterdam 148:206–214CrossRefGoogle Scholar
  14. Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 7150:188–191CrossRefGoogle Scholar
  15. Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide web? Nature 394:431PubMedCrossRefGoogle Scholar
  16. Hijri I, Sykorova Z, Oehl F, Ineichen K, Mader P, Wiemken A, Redecker D (2006) Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Mol Ecol 15:2277–2289PubMedCrossRefGoogle Scholar
  17. Hole DG, Perkins AJ, Wilson JD, Alexander IH, Grice F, Evans AD (2005) Does organic farming benefit biodiversity? Biol Conserv 122:113–130CrossRefGoogle Scholar
  18. Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789PubMedCrossRefGoogle Scholar
  19. Johnson D (2015) Priorities for research on priority effects. New Phytol 205:1375–1377PubMedCrossRefGoogle Scholar
  20. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301CrossRefGoogle Scholar
  21. Koide RT, Li M (1989) Appropriate controls for vesicular-arbuscular mycorrhiza research. New Phytol 111:35–44CrossRefGoogle Scholar
  22. Lekberg Y, Koide RT (2014) Integrating physiological community and evolutionary perspectives on the arbuscular mycorrhizal symbiosis. Botany 92:241–251CrossRefGoogle Scholar
  23. Lekberg Y, Koide RT, Rohr JR, Aldrich-Wolfe L, Morton JB (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol 95:95–105CrossRefGoogle Scholar
  24. Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748PubMedCrossRefGoogle Scholar
  25. McDonald JH (2009) Handbook of biological statistics, 2nd edn. Sparky House Publishing, BaltimoreGoogle Scholar
  26. McGonigle TP, Millers MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–502CrossRefGoogle Scholar
  27. Munkvold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364CrossRefGoogle Scholar
  28. Oehl F, Sieverding E, Mader P, Dubois D, Ineichen K, Boller T, Wiemken A (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583PubMedCrossRefGoogle Scholar
  29. Oehl F, de Silva GA, Goto BT, Sieverding E (2011) Glomeromycota: three new genera and gloomed species reorganized. Mycotaxon 116:75–120CrossRefGoogle Scholar
  30. Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium carbonate. Circular no. 939. US Department of Agriculture, Washington, D.C.Google Scholar
  31. Opik M, Metsis M, Daniell TJ, Zobel M, Moora M (2009) Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytol 184:424–437PubMedCrossRefGoogle Scholar
  32. Pellegrino E, Bedini S, Avio L, Bonari E, Giovannetti M (2011) Field inoculation effectiveness of native and exotic arbuscular mycorrhizal fungi in a Mediterranean agricultural soil. Soil Biol Biochem 43:367–376CrossRefGoogle Scholar
  33. Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig M, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc R Soc Lond B Biol 276:4237–4245CrossRefGoogle Scholar
  34. Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531PubMedCrossRefGoogle Scholar
  35. Rodriguez A, Sanders IR (2015) The role of community and population ecology in applying mycorrhizal fungi for improved food security. ISME J 9:1053–1061PubMedPubMedCentralCrossRefGoogle Scholar
  36. Schlapfer F, Schmid B (1999) Ecosystem effects of biodiversity: a classification of hypotheses and exploration of empirical results. Ecol Appl 9:893–912CrossRefGoogle Scholar
  37. Schultea RPO, Melland AR, Fenton O, Herlihy M, Richards K, Jordan P (2010) Modelling soil phosphorus decline: expectations of water framework directive policies. Environ Sci Pol 13:472–484CrossRefGoogle Scholar
  38. Schüßler A, Walker C (2010) The Glomeromycota: a species list with new families and genera. Accessed 18 February 2015Google Scholar
  39. Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421CrossRefGoogle Scholar
  40. Sikes BA, Cottenie K, Klironomos JN (2009) Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J Ecol 97:1274–1280CrossRefGoogle Scholar
  41. Tarbell TJ, Koske RE (2007) Evaluation of commercial arbuscular mycorrhizal inocula in a sand/peat medium. Mycorrhiza 18:51–56PubMedCrossRefGoogle Scholar
  42. Tian H, Drijber RA, Li XL, Miller DN, Wienhold BJ (2013) Arbuscular mycorrhizal fungi differ in their ability to regulate the expression of phosphate transporters in maize (Zea mays L). Mycorrhiza 23:507–514PubMedCrossRefGoogle Scholar
  43. Van der Gast C, Gosling P, Tiwari B, Bending GD (2011) Spatial scaling of arbuscular mycorrhizal fungal diversity is affected by farming practice. Environ Microbiol 13:241–249PubMedCrossRefGoogle Scholar
  44. van Ruijven J, Berendse F (2005) Diversity-productivity relationships: initial effects, long-term patterns and underlying mechanisms. Proc Natl Acad Sci U S A 102:695–700PubMedPubMedCentralCrossRefGoogle Scholar
  45. Verbruggen E, Kiers ET (2010) Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl 3:547–560PubMedPubMedCentralCrossRefGoogle Scholar
  46. Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562PubMedCrossRefGoogle Scholar
  47. Vosatka M, Latr A, Gianinazzi S, Albrechtova J (2012) Development of arbuscular mycorrhizal biotechnology and industry: current achievements and bottlenecks. Symbiosis 58:29–37CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.School of Life SciencesUniversity of WarwickCoventryUK
  2. 2.AHDBKenilworthUK

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