Plant and Soil

, Volume 328, Issue 1–2, pp 1–16 | Cite as

Integrated effects of abiotic stresses on inoculant performance, legume growth and symbiotic dependence estimated by 15N dilution

  • Phillip M. Chalk
  • Bruno J. R. Alves
  • Robert M. Boddey
  • Segundo Urquiaga
Marschner Review


Temperature, water, salinity, sodicity, acidity and nutrient disorders are major abiotic stresses that can affect legume growth or the establishment and function of the legume-Rhizobium symbiosis. We have examined the literature where the application of the 15N isotope dilution methodology permits the effect of individual abiotic stresses to be independently and quantitatively separated into plant growth-mediated and BNF (biological N2 fixation)-mediated components. The response of the symbiosis to a particular stress depends on a host of factors, including legume genotype, cultivar, Rhizobium inoculant, climatic conditions, and the duration, timing and severity of the stress. Published data are analysed in terms of the above variables and their interactions. As a general rule, severe stress inhibits both legume dry matter (DM) and the proportional dependence of the legume on BNF as a source of N. The symbiosis is resilient to low to moderate stress, but there may still be a penalty on legume DM. Gaps in knowledge are identified, and general guidelines on the identification and amelioration of abiotic stresses are provided.


15N isotope dilution Biological nitrogen fixation Legumes Abiotic stresses 



The authors thank the Brazilian National Research Council (CNPq) for support through individual research fellowships, and also Dr. Larry Purcell for making available his Excel file data from the original paper of Purcell et al. (2004).


  1. Alves BJR, Boddey RM, Urquiaga S (2003) The success of BNF in soybean in Brazil. Plant Soil 252:1–9CrossRefGoogle Scholar
  2. Bordeleau LM, Prévost D (1994) Nodulation and nitrogen fixation in extreme environments. Plant Soil 161:115–125CrossRefGoogle Scholar
  3. Bremer E, Rennie RJ, Rennie DA (1988) Dinitrogen fixation of lentil, field pea and fababean under dryland conditions. Can J Soil Sci 68:553–562Google Scholar
  4. Bremer E, van Kessel C, Karamanos R (1989) Inoculant, phosphorus and nitrogen responses of lentil. Can J Plant Sci 69:691–701Google Scholar
  5. Brockwell J, Roughley RJ, Herridge DF (1987) Population dynamics of Rhizobium japonicum strains used to inoculate three successive crops of soybean. Aust J Agric Res 38:61–74CrossRefGoogle Scholar
  6. Butler JHA (1993) Nitrogen fixation by a sub-clover-grass mixture grown on two acid soils treated with lime. Aust J Agric Res 44:863–873CrossRefGoogle Scholar
  7. Cadisch G, Sylvester-Bradley R, Boller BC, Nösberger J (1993) Effects of phosphorus and potassium on N2 fixation (15N-dilution) of field-grown Centrosema acutifolium and C. macrocarpum. Field Crops Res 31:329–340CrossRefGoogle Scholar
  8. Calvache AM, Reichardt K (1996) Water deficit at different growth stages for common bean (Phaseolus vulgaris L.) cv. Imbabello and nitrogen use efficiency. Scientia Agricola 53:343–353 in PortugueseCrossRefGoogle Scholar
  9. Calvache AM, Reichardt K, Bacchi OOS, Dourado-Neto D (1997) Deficit irrigation at different growth stages of the common bean (Phaseolus vulgaris L., cv. Imbabello). Scientia Agricola 54:1–16Google Scholar
  10. Campillo R, Urquiaga S, Undurraga P, Pino I, Boddey RM (2005) Strategies to optimise biological nitrogen fixation in legume/grass pastures in the southern region of Chile. Plant Soil 273:57–67CrossRefGoogle Scholar
  11. Carranca C, de Varennes A, Rolston D (1999) Biological nitrogen fixation by fababean, pea and chickpea, under field conditions, estimated by the 15N isotope dilution technique. Europ J Agron 10:49–56CrossRefGoogle Scholar
  12. Chalk PM (1985) Estimation of nitrogen fixation by isotope dilution: An appraisal of techniques involving 15N enrichment and their application. Soil Biol Biochem 17:389–410. doi: 10.1016/0038-0717(85)90001-X CrossRefGoogle Scholar
  13. Chalk PM (2000) Integrated effects of mineral nutrition on legume performance. Soil Biol Biochem 32:577–579. doi: 10.1016/S0038-0717(99)00173-X CrossRefGoogle Scholar
  14. Chalk PM, Smith CJ, Hopmans P, Hamilton SD (1996) A yield-independent, 15N-isotope dilution method to estimate legume symbiotic dependence without a non-N2-fixing reference plant. Biol Fertil Soils 23:196–199. doi: 10.1007/BF00336063 CrossRefGoogle Scholar
  15. Chalk PM, Souza RdeF, Urquiaga S, Alves BJR, Boddey RM (2006) The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biol Biochem 38:2944–2951. doi: 10.1016/j.soilbio.2006.05.005 CrossRefGoogle Scholar
  16. Eaglesham ARJ, Ayanaba A (1984) Tropical stress ecology of rhizobia, root nodulation and legume nitrogen fixation. In: Subba Rao NS (ed) Current developments in biological nitrogen fixation, pp 1–35. Oxford and IBH, New DelhiGoogle Scholar
  17. Edmeades DC, Rys G, Smart CE, Wheeler DM (1986) Effect of lime on soil nitrogen uptake by a ryegrass-white clover pasture. New Zeal J Agric Res 29:49–53Google Scholar
  18. Elsheikh EAE, Wood M (1995) Nodulation and N2 fixation by soybean inoculated with salt-tolerant Rhizobia or salt-sensitive Bradyrhizobia in saline soil. Soil Biol Biochem 27:657–661CrossRefGoogle Scholar
  19. Fehr WH, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybean, Glycine max (L) Merrill. Crop Sci 11:929–931CrossRefGoogle Scholar
  20. Garcia A, Hernandez G, Nuviola A, Duenas G, Méndez N, Toscano V, Herrero G, Curbelo S, Reyes JL (2007) Improving grain yield and nitrogen fixation of common bean grown in an acid Acrisol from Cuba. In: Management practices for improving sustainable crop production in tropical acid soils, pp 201–216. Proceedings Series STI/PUB/1285, IAEA, Vienna, AustriaGoogle Scholar
  21. Giller KE (2001) Nitrogen fixation in tropical cropping systems, 2nd edn. CABI, WallingfordCrossRefGoogle Scholar
  22. Hardarson G, Atkins C (2003) Optimising biological N2 fixation by legumes in farming systems. Plant Soil 252:41–54CrossRefGoogle Scholar
  23. Hungria M, Vargas MAT (2000) Environmental factors affecting N2 fixation in grain legumes in the tropics, with emphasis on Brazil. Field Crops Res 65:151–164CrossRefGoogle Scholar
  24. Jayasundara HPS, Thomson BD, Tang C (1998) Responses of cool season grain legumes to soil abiotic stresses. Adv Agron 63:77–151CrossRefGoogle Scholar
  25. Kirda C, Danso SKA, Zapata F (1989) Temporal water stress effects on nodulation, nitrogen accumulation and growth of soybean. Plant Soil 120:49–55CrossRefGoogle Scholar
  26. Kucey RMN, Chaiwanakupt P, Arayangkool T, Snitwongse P, Siripaibool C, Wadisirisuk P, Boonkerd N (1988) Nitrogen fixation (15N dilution) with soybeans under Thai field conditions. II. Effect of herbicides and water application schedule. Plant Soil 108:87–92CrossRefGoogle Scholar
  27. Lynch DH, Smith DL (1993) Early seedling and seasonal N2-fixing symbiotic activity of two soybean [Glycine max (L.) Merr.] cultivars inoculated with Bradyrhizobium strains of diverse origin. Plant Soil 157:289–303CrossRefGoogle Scholar
  28. Montanez A, Danso SKA, Hardarson G (1995) The effect of temperature on nodulation and nitrogen fixation by five Bradyrhizobium japonicum strains. Appl Soil Ecol 2:165–174CrossRefGoogle Scholar
  29. Nesheim L, Boller BC (1991) Nitrogen fixation by white clover when competing with grasses at moderately low temperatures. Plant Soil 133:47–56CrossRefGoogle Scholar
  30. O’Hara GW, Boonkerd N, Dilworth MJ (1988) Mineral constraints to nitrogen fixation. Plant Soil 108:93–110. doi: 10.1007/BF02370104 CrossRefGoogle Scholar
  31. Pena-Cabriales JJ, Castellanos JZ (1993) Effects of water stress on N2 fixation and grain yield of Phaseolus vulgaris L. Plant Soil 152:151–155CrossRefGoogle Scholar
  32. Peoples MB, Gault RR, Scammell GJ, Dear BS, Virgona J, Sandral GA, Paul J, Wolfe EC, Angus JF (1998) Effect of pasture management on the contributions of fixed N to the N economy of ley-farming systems. Aust J Agric Res 49:459–474CrossRefGoogle Scholar
  33. Peoples MB, Lilley DM, Burnett VF, Ridley AM, Garden DL (1995) Effects of surface application of lime and super-phosphate to acid soils on growth and N2 fixation by subterranean clover in mixed pasture swards. Soil Biol Biochem 27:663–671CrossRefGoogle Scholar
  34. Purcell LC, Serraj R, Sinclair TR, De A (2004) Soybean N2 fixation estimates, ureide concentration, and yield responses to drought. Crop Sci 44:484–492Google Scholar
  35. Rao DLN, Giller KE, Yeo AR, Flowers TJ (2002) The effects of salinity and sodicity upon nodulation and nitrogen fixation in chickpea (Cicer arietinum). Ann Bot 89:563–570CrossRefPubMedGoogle Scholar
  36. Sangakkara UR, Hartwig UA, Nösberger J (1996a) Growth and symbiotic nitrogen fixation of Vicia faba and Phaseolus vulgaris as affected by fertilizer potassium and temperature. J Sci Food Agric 70:315–320CrossRefGoogle Scholar
  37. Sangakkara UR, Hartwig UA, Nösberger J (1996b) Soil moisture and potassium affect the performance of symbiotic nitrogen fixation in fababean and common bean. Plant Soil 184:123–130CrossRefGoogle Scholar
  38. Serraj R, Sinclair TR, Purcell LC (1999) Symbiotic N2 fixation response to drought. J Exp Bot 50:143–155CrossRefGoogle Scholar
  39. Shock CC, Williams WA, Jones MB, Center DM, Phillips DA (1984) Nitrogen fixation by sub-clover associations fertilized with sulfur. Plant Soil 81:323–332CrossRefGoogle Scholar
  40. Smith AP, Chen D, Chalk PM (2009) N2 fixation by fababean (Vicia faba L.) in a gypsum-amended sodic soil. Biol Fertil Soils 45:329–333. doi: 10.1007/s00374-008-0347-6 CrossRefGoogle Scholar
  41. Smith CJ, Chalk PM, Noble CL, Prendergast JB, Robertson F (1993) Nitrogen fixation in a white clover-grass pasture irrigated with saline groundwater. Irrig Sci 13:189–194. doi: 10.1007/BF00190035 CrossRefGoogle Scholar
  42. Steele KW, Watson RN, Bonish PM, Littler RA, Yeates GW (1985) Effect of invertebrates on nitrogen fixation in temperate pastures. In: Proceedings 15th International Grasslands Congress, Kyoto, Japan. pp 450–451. The Science Council of Japan and the Japanese Society of Grassland ScienceGoogle Scholar
  43. Swaraj K (1987) Environmental stress and symbiotic N2-fixation in legumes. Pl Physiol Biochem 14:117–130Google Scholar
  44. Unkovich M, Herridge D, Peoples M, Cadisch G, Boddey B, Giller K, Alves B, Chalk P (2008) Measuring plant-associated nitrogen fixation in agricultural systems. ACIAR Monograph No. 136, Australian Centre for International Agricultural Research, Canberra. 258 pp.
  45. Unkovich MJ, Sanford P, Pate JS (1996) Nodulation and nitrogen fixation by subterranean clover in acid soils as influenced by lime application, toxic aluminium, soil mineral N, and competition from annual ryegrass. Soil Biol Biochem 28:639–648CrossRefGoogle Scholar
  46. Wheeler DM, Edmeades DC, Morton JD (1997) Effect of lime on yield, N fixation, and plant N uptake from the soil by pasture on 3 contrasting trials in New Zealand. New Zeal J Agric Res 40:397–408Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Phillip M. Chalk
    • 1
  • Bruno J. R. Alves
    • 1
  • Robert M. Boddey
    • 1
  • Segundo Urquiaga
    • 1
  1. 1.EMBRAPA-CNPABSeropédicaBrazil

Personalised recommendations