Skip to main content

Advertisement

Log in

Arbuscular mycorrhiza maintains nodule function during external NH +4 supply in Phaseolus vulgaris (L.)

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

The synergistic benefits of the dual inoculation of legumes with nodule bacteria and arbuscular mycorrhizae (AM) are well established, but the effect of an external NH +4 supply on this tripartite relationship is less clear. This effect of NH +4 supply was investigated with regards to the growth and function of the legume host and both symbionts. Nodulated Phaseolus vulgaris seedlings with and without AM, were grown in a sand medium with either 0 N, 1 mM or 3 mM NH +4 . Plants were harvested at 30 days after emergence and measurements were taken for biomass, N2 fixation, photosynthesis, asparagine concentration, construction costs and N nutrition. The addition of NH +4 led to a decline in the percentage AM colonization and nodule dry weights, although AM colonization was affected to a lesser extent. NH +4 supply also resulted in a decrease in the reliance on biological nitrogen fixation (BNF); however, the AM roots maintained higher levels of NH +4 uptake than their non-AM counterparts. Furthermore, the non-AM plants had a higher production of asparagine than the AM plants. The inhibitory effects of NH +4 on nodule function can be reduced by the presence of AM at moderate levels of NH +4 (1 mM), via improving nodule growth or relieving the asparagine-induced inhibition of BNF.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Almeida JPF, Hartwig UA, Frehner M, Nösberger J, Lüscher A (2000) Evidence that P deficiency induces N feedback regulation of symbiotic N2 fixation in white clover (Trifolium repens L.). J Exp Bot 51:1289–1297

    Article  PubMed  CAS  Google Scholar 

  • Awonaike KO, Lea PJ, Day JM, Roughley RJ, Miflin BJ (1980) Effect of combined nitrogen on nodulation and growth of Phaseolus vulgaris. Exp Agric 16:303–311

    Article  CAS  Google Scholar 

  • Azcon R, Gomez M, Tobar R (1992) Effects of nitrogen source on growth, nutrition, photosynthetic rate and nitrogen metabolism of mycorrhizal and phosphorous-fertilized plants of Lactuca sativa L. New Phytol 121:227–234

    Google Scholar 

  • Boddey RM, Oliveira OC, Alves BJR, Urquiaga S (1995) Field application of the 15N isotope dilution technique for the reliable quantification of plant-associated biological nitrogen fixation. Fert Res 42:77–87

    Article  CAS  Google Scholar 

  • Brown MS, Bethlenfalvay GJ (1987) The Glycine–GlomusRhizobium symbiosis: IV. Photosynthesis in nodulated, mycorrhizal, or N- and P-fertilized soybean plants. Plant Phys 85:120–123

    Article  CAS  Google Scholar 

  • Brundrett M, Melville L, Peterson L (eds) (1994) Practical methods in mycorrhiza 14 research. Mycologue Publications, Guelph

    Google Scholar 

  • Carling DE, Reihle WG, Brown MF, Johnston DR (1978) Effects of vesicular-arbuscular mycorrhizal fungus on nitrate reductase and nitrogenase activities in nodulating and non-nodulating soybeans. Phytopathology 68:1590–1596

    Article  CAS  Google Scholar 

  • Chambers CA, Smith SE, Smith FA (1980) Effects of ammonium and nitrate ions on mycorrhizal infection, nodulation and growth of Trifolium subterraneum. New Phytologist 85:47–62

    Google Scholar 

  • Constable JVH, Bassirirad H, Lussenhop J, Ayalsew Z (2001) Influence of elevated CO2 and mycorrhizae on nitrogen acquisition: contrasting responses in Pinus taeda and Liquidambar styraciflua. Tree Physiol 21:83–91

    Article  PubMed  CAS  Google Scholar 

  • Dennis DT, Turpin DH, Lefebvre DD, Layzell DB (1997) Plant metabolism, 2nd edn. Adison Wesley Longman, England

    Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Physiol Plant Mol Biol 40:503–537

    Google Scholar 

  • Fredeen AL, Terry N (1988) Influence of vesicular–arbuscular mycorrhizal infection and soil phosphorous level on growth and carbon metabolism of soybean. Can J Bot 66:2311–2316

    Google Scholar 

  • Goergen E, Chambers JC, Blank R (2009) Effects of water and nitrogen availability on nitrogen contribution by the legume, Lupinus albus Pursh. Appl Soil Ecol 42:200–208

    Article  Google Scholar 

  • Goss MJ, de Varennes A (2002) Soil disturbance reduces the efficacy of mycorrhizal associations for early soybean growth and N2 fixation. Soil Biol Biochem 34:1167–1173

    Article  CAS  Google Scholar 

  • Govindarajulu M, Pfeffer PE, Hairu J, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823

    Article  PubMed  CAS  Google Scholar 

  • Harley JL (1989) The significance of mycorrhiza. Mycol Res 92:129–139

    Article  Google Scholar 

  • Harris D, Pacovsky RS, Paul EA (1985) Carbon economy of soy-bean–RhizobiumGlomus associations. New Phytol 101:427–440

    Article  CAS  Google Scholar 

  • Hartwig UA (1998) The Regulation of symbiotic N2 fixation: a conceptual model of N feedback from the ecosystem to the gene expression level. Perspect Plant Ecol Evol Syst 1:92–120

    Article  Google Scholar 

  • Hewitt EJ (1986) Sand and water culture methods used in the study of plant nutrition. Technical Communication 1966: Nr.22. Commonwealth Bureau of Horticulture and Plantation Crops, East Malling

  • Jia Y, Gray VM, Straker CJ (2004) The influence of Rhizobium and arbuscular mycorrhiazl fungi on Nitrogen and Phosphorous accumulation by Vicia faba. Ann Bot 94:251–258

    Article  PubMed  CAS  Google Scholar 

  • Johnson CR, Jarrell WM, Mengi JA (1984) Influence of ammonium nitrate ratio and solution ph on mycorrhizal infection, growth and nutrient composition of Chrysanthemum morifolium var. circus. Plant Soil 77:151–157

    Google Scholar 

  • 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 Biol Biochem 41:1233–1244

    Article  CAS  Google Scholar 

  • Kaschuk G, Leffelaar PA, Giller KE, Alberton O, Hungria M, Kuyper TW (2010) Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses. Soil Biol Biochem 42:125–127

    Article  CAS  Google Scholar 

  • Kawai Y, Yamamoto Y (1986) Increase in the formation and nitrogen fixation of soybean nodules by vesicular–arbuscular mycorrhiza. Plant Cell Physiol 27:399–405

    CAS  Google Scholar 

  • Luciñski R, Polcyn W, Ratajczak (2002) Nitrate reduction and nitrogen fixation in symbiotic association Rhizobium-legumes. Acta Biochim Pol 49(2):537–546

    PubMed  Google Scholar 

  • Luis I, Lim G (1988) Differential response in growth and mycorrhizal colonization of soybean to inoculation with two isolates of Glomus clarum in soils of different P availability. Plant Soil 112:37–43

    Article  Google Scholar 

  • Malik NSA, Calvert HE, Bauer WD (1987) Nitrate induced regulation of nodule formation in soybean. Plant Physiol 84:266–271

    Article  PubMed  CAS  Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 59:89–102

    Google Scholar 

  • Mortimer PE, Archer E, Valentine AJ (2005) Mycorrhizal C costs and nutritional benefits in developing grapevines. Mycorrhiza 15:159–165

    Google Scholar 

  • Mortimer PE, Pérez-Fernández MA, Valentine AJ (2008) The role of arbuscular mycorrhizal colonization in the carbon and nutrient economy of the tripartite symbiosis with nodulated Phaseolus vulgaris. Soil Biol Biochem 40:1019–1027

    Article  CAS  Google Scholar 

  • Mortimer PE, Pérez-Fernández MA, Valentine AJ (2009) Arbuscular mycorrhizae affect the N and C economy of nodulated Phaseolus vulgaris (L.) during NH +4 nutrition. Soil Biol Biochem 41:2115–2121

    Article  CAS  Google Scholar 

  • Müller S, Pereira PAA, Martin P (1993) Effect of different levels of mineral nitrogen on nodulation and N2 fixation of two cultivars of common bean (Phaseolus vulgaris L.). Plant Soil 152:139–143

    Article  Google Scholar 

  • Peng S, Eissenstat DM, Graham JH, Williams K, Hodge NC (1993) Growth depression in mycorrhizal citrus at high-phosphorous supply. Plant Physiol 101:1063–1071

    Google Scholar 

  • Provorov NA, Tikhonovich IA (2003) Genetic resources for improving nitrogen fixation in legume-rhizobia symbioses. Genet Res Crop Evol 359:907–918

    Google Scholar 

  • Ruffel S, Freixes S, Balzergue S, Tillard P, Jeudy C, Martin-Magniette ML, vd Merwe MJ, Kakar K, Gouzy J, Fernie AR, Udvardi M, Salon C, Gojon A, Lepetit M (2008) Systematic signaling of the plant nitrogen status triggers specific transcriptome responses depending on the nitrogen source in Medicago truncatula 1[W]. Plant Physiol 146(4):2020–2035

    Article  PubMed  CAS  Google Scholar 

  • Senaratne R, Amornpinol C, Hardarson G (1987) Effect of combined nitrogen on nitrogen fixation of soybean (Glycine max L. Merril.) as affected by cultivar and rhizobial strain. Plant Soil 102:42–50

    Google Scholar 

  • Shearer GB, Kohl DH (1986) N2-fixation in field settings: estimations based on natural 15N abundance. Aust J Plant Physiol 13:699–756

    CAS  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, London, UK

    Google Scholar 

  • Smith RG, Vanlerberghe GC, Stitt M, Turpin DH (1989) Short-term metabolite changes during transient ammonium assimilation by N-limited green algae Selenastrum minutum. Plant Physiol 91:749–755

    Article  PubMed  CAS  Google Scholar 

  • 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 92:75–87

    Article  Google Scholar 

  • Sulieman S, Fischinger SA, Gresshoff PM, Schulze J (2010) Asparagine as a major factor in N-feedback regulation of N2 fixation in Medicago truncatula. Physiol Plant 140:21–31

    Article  PubMed  CAS  Google Scholar 

  • Valentine AJ, Kleinert A (2006) Respiratory metabolism of root-zone CO2 in mycorrhizal plants with NH +4 and NO 3 nutrition. Symbiosis 41(3):119–126

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Valentine AJ, Osbourne BA, Mitchell DT (2002) Form of inorganic nitrogen influences mycorrhizal colonization and photosynthesis of cucumber. Scientia Horticulturae 92:229–239

    Google Scholar 

  • Vance CP (2002) Root-bacteria interactions. Symbiotic Nitrogen fixation. In: Waisel Y, Eschel A, Kafkafi U (eds) Plant roots; The hidden half, 3rd edn. Marcel Dekker, New York, 839 pp. 868

  • Vesjsadova H, Siblikova D, Gryndler M, Simon T, Miksik I (1993) Influence of inoculation with Bradyrhizobium japonicum and Glomus claroideum on seed yield of soybean under greenhouse and field conditions. J Plant Nutr 16:619–629

    Article  Google Scholar 

  • Vessey JK, Layzell DB (1987) Regulation of assimilate partitioning in soybean. Initial effects following change in nitrate supply. Plant Physiol 83:341–348

    Article  PubMed  CAS  Google Scholar 

  • Williams K, Percival F, Merino J, Mooney HA (1987) Estimation of tissue construction cost from heat of combustion and organic nitrogen content. Plant Cell Environ 10:725–734

    Google Scholar 

  • Zar JH (1999) Biostatistical Analysis. 4th edition, Prentice-Hall, Upper Saddle River, New Jersey, USA

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alex J. Valentine.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mortimer, P.E., Pérez-Fernández, M.A. & Valentine, A.J. Arbuscular mycorrhiza maintains nodule function during external NH +4 supply in Phaseolus vulgaris (L.). Mycorrhiza 22, 237–245 (2012). https://doi.org/10.1007/s00572-011-0396-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-011-0396-9

Keywords

Navigation