SpringerLink
Log in

Do arbuscular mycorrhizas or heterotrophic soil microbes contribute toward plant acquisition of a pulse of mineral phosphate?

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

We investigated the role of arbuscular mycorrhizal fungi (AMF) and heterotrophic soil microbes in the uptake of phosphorus (P) by Trifolium subterraneum from a pulse.

Methods

Plants were grown in sterilised pasture field soil with a realistic level of available P. There were five treatments, two of which involved AMF: 1) unsterilised field soil containing a community of AMF and heterotrophic organisms; 2) Scutellospora calospora inoculum (AMF); 3) microbes added as filtrate from the field soil; 4) microbes added as filtrate from the S. calospora inoculum; 5) no additions, i.e. sterilised field soil. After 11 weeks, plants were harvested: 1 day before (day 0), 1 day after (day 2) and 7 days after (day 8) the pulse of P (10 mg kg−1).

Results

There was no difference among treatments in shoot and root dry weight, which increased from day 0 to day 8. At day 0, shoots and roots of plants in the colonised treatments had higher P and lower Mn concentrations. After the pulse, the rate of increase in P concentration in the shoots was slower for the colonised plants, and the root Mn concentration declined by up to 50 % by day 2.

Conclusions

Plants colonised by AMF had a lower rate of increase in shoot P concentration after a pulse, perhaps because intraradical hyphae accumulated P and thus reduced its transport to the shoots.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abbott LK, Robson AD (1977) Growth stimulation of subterranean clover with vesicular arbuscular mycorrhizas. Aust J Agric Res 28:639–649

    Article  CAS  Google Scholar 

  • Bainard LD, Koch AM, Gordon AM, Klironomos JN (2012) Growth response of crops to soil microbial communities from conventional monocrop** and tree-based intercrop** systems. Plant Soil 363:1–12

    Google Scholar 

  • Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778

    Article  PubMed  CAS  Google Scholar 

  • Blackwell MSA, Brookes PC, de la Fuente-Martinez N, Gordon H, Murray PJ, Snars KE, Williams JK, Bol R, Haygarth PM (2010) Phosphorus solubilization and potential transfer to surface waters from the soil microbial biomass following drying–rewetting and freezing–thawing. Adv Agron 106:1–35

    Article  CAS  Google Scholar 

  • Blair GJ, Chinoim N, Lefroy RDB, Anderson G, Crocker G (1991) A soil sulfur test for pastures and crops. Aust J Soil Res 29:619–626

    Article  CAS  Google Scholar 

  • Bolan NS, Robson AD, Barrow NJ (1987) Effects of vesicular-arbuscular mycorrhiza on the availability of iron phosphates to plants. Plant Soil 99:401–410

    Article  CAS  Google Scholar 

  • Butterly CR, Bünemann EK, McNeill AM, Baldock JA, Marschner P (2009) Carbon pulses but not phosphorus pulses are related to decreases in microbial biomass during repeated drying and rewetting of soils. Soil Biol Biochem 41:1406–1416

    Article  CAS  Google Scholar 

  • Colwell JD (1965) An automatic procedure for the determination of phosphorus in sodium hydrogen carbonate extracts of soils. Chem Ind 10:893–895

    Google Scholar 

  • 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 185:1050–1061

    Article  PubMed  Google Scholar 

  • Fageria NK, Baligar C, Clark RB (2002) Micronutrients in crop production. Adv Agron 77:185–268

    Article  CAS  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Godo GH, Reisenauer HM (1980) Plant effects on soil manganese availability. Soil Sci Soc Am J 44:993–995

    Article  CAS  Google Scholar 

  • Graham J, Abbott L (2000) Wheat responses to aggressive and non-aggressive arbuscular mycorrhizal fungi. Plant Soil 220:207–218

    Article  CAS  Google Scholar 

  • Graham JH, Linderman RG, Menge JA (1982) Development of external hyphae by different isolates of mycorrhizal Glomus spp. in relation to root colonisation and growth of Troyer citrange. New Phytol 91:183–189

    Article  Google Scholar 

  • Gyaneshwar P, Naresh Kumar G, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93

    Article  CAS  Google Scholar 

  • Haling RE, Simpson RJ, McKay AC, Hartley D, Lambers H, Ophel-Keller K, Wiebkin S, Herdina, Riley IT, Richardson AE (2011) Direct measurement of roots in soil for single and mixed species using a quantitative DNA-based method. Plant Soil 348:123–137

    Article  CAS  Google Scholar 

  • Hetrick BAD, Wilson GT, Kitt DG, Schwab AP (1988) Effects of soil microorganisms on mycorrhizal contribution to growth of big bluestem grass in non-sterile soil. Soil Biol Biochem 20:501–507

    Article  Google Scholar 

  • Jakobsen I, Abbott LK, Robson AD (1992a) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 2. hyphal transport of 32P over defined distances. New Phytol 120:509–516

    Article  CAS  Google Scholar 

  • Jakobsen I, Abbott LK, Robson AD (1992b) External hyphae of vesicular–arbuscular mycorrhizal fungi associated with Trifolium subterraneum L.1. spread of hyphae and phosphorus inflow into roots. New Phytol 120:371–380

    Article  CAS  Google Scholar 

  • Jansa J, Mozafar A, Frossard E (2005) Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. Plant Soil 276:163–176

    Article  CAS  Google Scholar 

  • Koide RT, Mosse B (2004) A history of research on arbuscular mycorrhiza. Mycorrhiza 14:145–163

    Article  PubMed  Google Scholar 

  • Kothari SK, Marschner H, Römheld V (1991) Effect of a vesicular–arbuscular mycorrhizal fungus and rhizosphere micro-organisms on manganese reduction in the rhizosphere and manganese concentrations in maize (Zea mays L.). New Phytol 117:649–655

    Google Scholar 

  • Lamont B (1982) Mechanisms for enhancing nutrient uptake in plants, with particular reference to mediterranean South Africa and Western Australia. Bot Rev 48:597–689

    Article  CAS  Google Scholar 

  • Lewis DC, Clarke AL, Hall WB (1987) Accumulation of plant nutrients and changes in soil properties of sandy soils under fertilized pasture in southeastern South-Australia.I. Phosphorus. Aust J Soil Res 25:193–202

    Article  Google Scholar 

  • Liu A, Hamel C, Hamilton RI, Ma BL, Smith DL (2000) Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9:331–336

    Article  CAS  Google Scholar 

  • Pittman JK (2005) Managing the manganese: molecular mechanisms of manganese transport and homeostasis. New Phytol 167:733–742

    Article  PubMed  CAS  Google Scholar 

  • Posta K, Marschner H, Römheld V (1994) Manganese reduction in the rhizosphere of mycorrhizal and nonmycorrhizal maize. Mycorrhiza 5:119–124

    Article  CAS  Google Scholar 

  • Qiu S, McComb AJ, Bell RW, Davis JA (2004) Phosphorus dynamics from vegetated catchment to lakebed during seasonal refilling. Wetlands 24:828–836

    Article  Google Scholar 

  • Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Funct Plant Biol 28:897–906

    Article  Google Scholar 

  • Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    Article  CAS  Google Scholar 

  • Ryan MH, Angus JF (2003) Arbuscular mycorrhizae in wheat and field pea crops on a low P soil: increased Zn-uptake but no increase in P-uptake or yield. Plant Soil 250:225–239

    Article  CAS  Google Scholar 

  • Ryan MH, McCully ME, Huang CX (2003) Location and quantification of phosphorus and other elements in fully hydrated, soil-grown arbuscular mycorrhizas: a cryo-analytical scanning electron microscopy study. New Phytol 160:429–441

    Article  CAS  Google Scholar 

  • Ryan MH, McCully ME, Huang CX (2007) Relative amounts of soluble and insoluble forms of phosphorus and other elements in intraradical hyphae and arbuscules of arbuscular mycorrhizas. Funct Plant Biol 34:457–464

    Article  CAS  Google Scholar 

  • Ryan MH, Tibbett M, Edmonds-Tibbett T, Suriyagoda LDB, Lambers H, Cawthray GR, Pang J (2012) Carbon trading for phosphorus gain: the balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition. Plant Cell Environ 35:2170–2180

    Article  PubMed  CAS  Google Scholar 

  • Scanlon T (2011) Decline in subterranean clover (Trifolium subterraneum L.)-based pasture systems : causes and solutions. MSc Dissertation, University of Western Australia

  • Searle PL (1984) The berthelot or indophenol reaction and its use in the analytical chemistry of nitrogen. A review. Analyst 109:549–568

    Article  CAS  Google Scholar 

  • Shane MW, Lambers H (2005) Manganese accumulation in leaves of Hakea prostrata (Proteaceae) and the significance of cluster roots for micronutrient uptake as dependent on phosphorus supply. Physiol Plant 124:441–450

    Article  CAS  Google Scholar 

  • Shane MW, McCully ME, Lambers H (2004) Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae). J Exp Bot 55:1033

    Article  PubMed  CAS  Google Scholar 

  • Simpson RJ, Oberson A, Culvenor RA, Ryan MH, Veneklaas EJ, Lambers H, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Richardson AE (2011) Strategies and agronomic interventions to improve the phosphorus-use efficiency of farming systems. Plant Soil 349:89–120

    Article  CAS  Google Scholar 

  • Singh S, Kapoor KK (1998) Effects of inoculation of phosphate-solubilizing microorganisms and an arbuscular mycorrhizal fungus on mungbean grown under natural soil conditions. Mycorrhiza 7:249–253

    Article  CAS  Google Scholar 

  • Smith SE (1982) Inflow of phosphate into mycorrhizal and non-mycorrhizal plants of Trifolium subterraneum at different levels of soil phosphate. New Phytol 90:293–303

    Article  CAS  Google Scholar 

  • Smith SE, Jakobsen I, Groenlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus (P) nutrition: interactions between pathways of P uptake in arbuscular mycorrhizal (AM) roots have important implications for understanding and manipulating plant P acquisition. Plant Physiol 156:1050–1057

    Article  PubMed  CAS  Google Scholar 

  • Snowball K, Robson AD (1988) Symptoms of nutrient deficiencies: subterranean clover and wheat. Department of Soil Science and Plant Nutrition, Institute of Agriculture, University of Western Australia, Nedlands, pp 73

  • Tibbett M, Ryan MH, Barker SJ, Chen Y, Denton MD, Edmonds-Tibbett T, Walker C (2008) The diversity of arbuscular mycorrhizas of selected Australian Fabaceae. Plant Biosyst 142:420–427

    Article  Google Scholar 

  • Turner BL, McKelvie ID, Haygarth PM (2002) Characterisation of water-extractable soil organic phosphorus by phosphatase hydrolysis. Soil Biol Biochem 34:27–35

    Article  CAS  Google Scholar 

  • Van der Heijden MGA, 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

    Article  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    PubMed  CAS  Google Scholar 

  • Wagg C, Jansa J, Stadler M, Schmid B, Van der Heijden MGA (2011) Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology 92:1303–1313

    Article  PubMed  Google Scholar 

  • Weaver DM, Reed AEG (1998) Patterns of nutrient status and fertiliser practice on soils of the south coast of Western Australia. Agric Ecosyst Environ 67:37–53

    Article  Google Scholar 

Download references

Acknowledgments

This project was funded by the Future Farm Industries CRC. We wish to thank Tamara Edmonds-Tibbett for technical support of the preliminary experiment.

Author information

Authors and Affiliations

  1. School of Plant Biology and Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Nazanin K. Nazeri, Hans Lambers & Megan H. Ryan

  2. Future Farm Industries Cooperative Research Centre, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Nazanin K. Nazeri, Mark Tibbett & Megan H. Ryan

  3. School of Earth and Environment, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Mark Tibbett

  4. National Soil Resources Institute, Department of Environmental Science and Technology, School of Applied Sciences, Cranfield University, Cranfield, MK43 0SZ, England, UK

    Mark Tibbett

  5. School of Plant Biology, M080, The University of Western Australia, Crawley, WA, 6009, Australia

    Nazanin K. Nazeri

Authors
  1. Nazanin K. Nazeri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hans Lambers
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark Tibbett
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Megan H. Ryan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nazanin K. Nazeri.

Additional information

Responsible Editor: Timothy Cavagnaro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nazeri, N.K., Lambers, H., Tibbett, M. et al. Do arbuscular mycorrhizas or heterotrophic soil microbes contribute toward plant acquisition of a pulse of mineral phosphate?. Plant Soil 373, 699–710 (2013). https://doi.org/10.1007/s11104-013-1838-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-013-1838-2

Keywords

Search

Navigation