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An overview of the role and significance of 15N methodologies in quantifying biological N2 fixation (BNF) and BNF dynamics in agro-ecosystems

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Abstract

Quantitative estimates of BNF are needed to improve our understanding of the ecology of N in the environment and aid efforts to improve agricultural N management. Static models based on the principle of 15N isotope dilution have been proposed to estimate the proportion of N in a N2-fixing species that is derived from the atmosphere via biological N2 fixation. Furthermore, equations have been developed to quantify the movement of biologically fixed N between neighboring species or from legumes to cereals in crop rotations. The present paper is structured to provide a comprehensive overview of these methods in a logical and systematic manner. While the relevant literature is vast, some aspects have fortunately been covered by recent in-depth reviews which will be identified and briefly summarized. The overview will emphasize the more practical indirect methodologies based either on artificial 15N enrichment or 15N depletion, or alternatively on 15N natural abundance. In considering methods used to estimate symbiotic dependence, the major structural division is whether or not a non-N2-fixing reference plant is employed, and approaches taken to remove this source of error are described. Four examples are provided to illustrate the contemporary success of 15N-based methods, one in basic research involving endophytic BNF, and three in applied research involving legume breeding for enhanced BNF, the response of legumes to climate change and biotic and abiotic factors affecting legume symbiotic performance.

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References

  • Angus JF, Grace PR (2017) Nitrogen balance in Australia and nitrogen use efficiency on Australian farms. Soil Res 55:435–450

    Article  Google Scholar 

  • Barnes DK, Heichel GH, Vance CP, Ellis WR (1984) A multiple-trait breeding program for improving the symbiosis for N2 fixation between Medicago sativa L. and Rhizobium meliloti. Plant Soil 82:303–314

    Article  CAS  Google Scholar 

  • Bergersen FJ, Turner GL (1983) An evaluation of 15N methods for estimating nitrogen fixation in a subterranean clover-perennial ryegrass sward. Crop Pasture Sci 34:391–401

    Article  Google Scholar 

  • Bliss FA (1993) Breeding common bean for improved biological nitrogen fixation. Plant Soil 152:71–79

    Article  Google Scholar 

  • Boddey RM, Peoples MB, Palmer B, Dart PJ (2000) Use of the 15N natural abundance technique to quantify biological nitrogen fixation by woody perennials. Nutr Cycl Agroecosyst 57:235–270

    Article  Google Scholar 

  • Boller BC, Nösberger J (1994) Differences in nitrogen fixation among field-grown red clover strains at different levels of 15N fertilization. Euphytica 78:167–174

    Article  CAS  Google Scholar 

  • Bourion V, Laguerre G, Depret G, Voisin A-S, Salon C, Duc G (2007) Genetic variability in nodulation and root growth affects nitrogen fixation and accumulation in pea. Ann Bot 100:1–10

    Article  Google Scholar 

  • Boyd ES, Peters JW (2013) New insights into the evolutionary history of biological nitrogen fixation. Front Microbiol 4:201

    PubMed  PubMed Central  Google Scholar 

  • Broadbent FE, Nakashima T, Chang GY (1982) Estimation of nitrogen fixation by isotope dilution in field and greenhouse experiments. Agron J 74:625–628

    Article  Google Scholar 

  • Carlsson G, Palmborg C, Huss-Danell K (2006) Discrimination against 15N in three N2-fixing Trifolium species as influenced by Rhizobium strain and plant age. Acta Agric Scand Sect B 56:31–38

    CAS  Google Scholar 

  • Chalk PM (1985) Estimation of N2 fixation by isotope dilution: an appraisal of techniques involving 15N enrichment and their application. Soil Biol Biochem 17:389–410

    Article  CAS  Google Scholar 

  • Chalk PM (1991) The contribution of associative and symbiotic nitrogen fixation to the nitrogen nutrition of non-legumes. Plant Soil 132:29–39

    Article  CAS  Google Scholar 

  • Chalk PM (1996) Nitrogen transfer from legumes to cereals in intercropping. In: Ito O, Johansen C, Adu-Gyamfi JJ, Katayama K, Kumar Rao JVDK, Rego TJ (eds) Dynamics of roots and nitrogen in cropping Systems of the Semi-Arid Tropics. Japan International Research Center for Agricultural Sciences, Tsukuba, pp 351–374

    Google Scholar 

  • Chalk PM (1998) Dynamics of biologically-fixed N in legume-cereal rotations: a review. Crop Past Sci 49:303–316

    Article  CAS  Google Scholar 

  • Chalk PM (2016) The strategic role of 15N in quantifying the contribution of endophytic N2 fixation to the N nutrition of non-legumes. Symbiosis 69:63–80

    Article  CAS  Google Scholar 

  • Chalk PM, Alves BJR, Boddey RM, Urquiaga S (2010) Integrated effects of abiotic stresses on inoculant performance, legume growth and symbiotic dependence estimated by 15N dilution. Plant Soil 328:1–16

    Article  CAS  Google Scholar 

  • Chalk PM, He J-Z, Peoples MB, Chen D (2017) 15N2 as a tracer of biological N2 fixation: a 75-year retrospective. Soil Biol Biochem 106:36–50

    Article  CAS  Google Scholar 

  • Chalk PM, Inácio CT, Balieiro FC, Rouws JRC (2016a) Do techniques based on 15N enrichment and 15N natural abundance give consistent estimates of the symbiotic dependence of N2-fixing plants? Plant Soil 399:415–426

    Article  CAS  Google Scholar 

  • Chalk PM, Inácio CT, Craswell ET, Chen D (2015) Letter to the editor. On the usage of absolute (x) and relative (δ) values of 15N abundance. Soil Biol Biochem 85:51–53

    Article  CAS  Google Scholar 

  • Chalk PM, Ladha JK (1999) Estimation of legume symbiotic dependence: an evaluation of techniques based on 15N dilution. Soil Biol Biochem 31:1901–1917

    Article  CAS  Google Scholar 

  • Chalk PM, Lam SK, Chen D (2016b) 15N methodologies for quantifying the response of N2-fixing associations to elevated [CO2]: a review. Sci Total Environ 571:624–632

    Article  CAS  PubMed  Google Scholar 

  • Chalk PM, Peoples MB, McNeill AM, Boddey RM, Unkovich MJ, Gardener MJ, Silva CF, Chen D (2014) Methodologies for estimating nitrogen transfer between legumes and companion species in agro-ecosystems: a review of 15N-enriched techniques. Soil Biol Biochem 73:10–21

    Article  CAS  Google Scholar 

  • Chalk PM, Smith CJ (2017) 15N methodologies for estimating the transfer of N from legumes to non-legumes in crop sequences. Nutr Cycl Agroecosyst 107:279–301

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Chalk PM, Souza RF, Urquiaga S, Alves BJR, Boddey RM (2006) The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biol Biochem 38:2944–2951

    Article  CAS  Google Scholar 

  • Connor DJ (2008) Organic agriculture cannot feed the world. Field Crop Res 106:187–190

    Article  Google Scholar 

  • Coplen TB (2011) Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun Mass Spectrom 25:2538–2560

    Article  CAS  PubMed  Google Scholar 

  • Danso SKA, Hera C, Douka C (1987) Nitrogen fixation in soybean as influenced by cultivar and Rhizobium strain. Plant Soil 99:163–174

    Article  CAS  Google Scholar 

  • Doughton JA, Vallis I, Saffigna PG (1992) An indirect method for estimating 15N isotope fractionation during nitrogen fixation by a legume under field conditions. Plant Soil 144:23–29

    Article  CAS  Google Scholar 

  • Duc G, Mariotti A, Amarger N (1988) Measurement of genetic variability for symbiotic dinitrogen fixation in field-grown fababean (Vicia faba L.) using a low level 15N-tracer technique. Plant Soil 106:269–276

    Article  CAS  Google Scholar 

  • Duque FF, Neves MCP, Franco AA, Victoria RL, Boddey RM (1985) The response of field grown Phaseolus vulgaris to Rhizobium inoculation and the quantification of N2 fixation using 15N. Plant Soil 88:333–343

    Article  Google Scholar 

  • Eriksen J, Høgh-Jensen H (1998) Variations in the natural abundance of 15N in ryegrass/white clover shoot material as influenced by cattle grazing. Plant Soil 205:67–76

    Article  CAS  Google Scholar 

  • Fillery IRP (2001) The fate of biologically fixed nitrogen in legume-based dryland farming systems: a review. Anim Prod Sci 41:361–381

    Article  CAS  Google Scholar 

  • Galloway JN, Leach AM, Erisman JW, Bleeker A (2017) Nitrogen: the historical progression from ignorance to knowledge, with a view to future solutions. Soil Res 55:417–424

    Article  Google Scholar 

  • Giller KE, Cadisch G (1995) Future benefits from biological nitrogen fixation: an ecological approach to agriculture. Plant Soil 174:255–277

    Article  CAS  Google Scholar 

  • Giller KE, Nambiar PTC, Srinivasa Rao B, Dart PJ, Day JM (1987) A comparison of nitrogen fixation in genotypes of groundnut (Arachis hyopgaea L.) using 15N-isotope dilution. Biol Fertil Soils 5:23–25

    Article  Google Scholar 

  • Graham PH, Hungria M, Tlusty B (2004) Breeding for better nitrogen fixation in grain legumes: where do the Rhizobia fit in? Crop Manage 3 (1) 0–0. https://doi.org/10.1094/CM-2004-0301-02-RV

  • Guimarães AP, de Morais RF, Urquiaga S, Boddey RM, Alves BJR (2008) Bradyrhizobium strain and the 15N natural abundance quantification of biological N2 fixation in soybean. Sci Agric 65:516–524

    Article  Google Scholar 

  • Hardarson G, Zapata F, Danso SKA (1984) Effect of plant genotype and nitrogen fertilizer on symbiotic nitrogen fixation by soybean cultivars. Plant Soil 82:397–405

    Article  CAS  Google Scholar 

  • Hauck RD, Bremner JM (1976) Use of tracers for soil and fertilizer nitrogen research. Adv Agron 28:219–266

    Article  Google Scholar 

  • Herridge DF, Bergersen FJ, Peoples MB (1990) Measurement of nitrogen fixation by soybean in the field using the ureide and natural 15N abundance methods. Plant Physiol 93:708–716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herridge DF, Danso SKA (1995) Enhancing crop legume N2 fixation through selection and breeding. Plant Soil 174:51–82

    Article  CAS  Google Scholar 

  • Herridge DF, Peoples MB (1990) Ureide assay for measuring nitrogen fixation by nodulated soybean calibrated by 15N methods. Plant Physiol 93:495–503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herridge D, Rose I (2000) Breeding for enhanced nitrogen fixation in crop legumes. Field Crop Res 65:229–248

    Article  Google Scholar 

  • Høgh-Jensen H, Schjoerring JK (1994) Measurement of biological dinitrogen fixation in grassland: comparison of the enriched 15N dilution and the natural 15N abundance methods at different nitrogen application rates and defoliation frequencies. Plant Soil 166:153–163

    Article  Google Scholar 

  • Holdensen L, Hauggaard-Nielsen H, Jensen ES (2007) Short-range spatial variability of soil delta-15N natural abundance – effects on symbiotic N2-fixation estimates in pea. Plant Soil 298:265–272

    Article  CAS  Google Scholar 

  • Inácio CT, Chalk PM, Magalhães AMT (2015) Principles and limitations of stable isotopes in differentiating organic and conventional foodstuffs: 1. Plant products. Crit Rev Food Sci Nutr 55:1206–1218

    Article  PubMed  Google Scholar 

  • Inácio CT, Magalhães AMT, Souza PO, Chalk PM, Urquiaga S (2017) The isotopic composition (13C, 15N) during composting of agricultural wastes in relation to compost quality and feedstock. Isot Environ Health Stud:1–11. https://doi.org/10.1080/10256016.2017.1377196

  • Junk G, Svec HJ (1958) The absolute abundance of the nitrogen isotopes in the atmosphere and compressed gas from various sources. Geochim Cosmochim Acta 14:234–243

    Article  CAS  Google Scholar 

  • Khadka J, Tatsumi J (2006a) Difference in δ15N signatures among plant parts of perennial species subjected to drought stress with special reference to the contribution of symbiotic N2-fixation to plant N. Plant Prod Sci 9:115–122

    Article  CAS  Google Scholar 

  • Khadka J, Tatsumi J (2006b) Alteration in intra-plant distribution of δ 15N in response to shading in legumes. Plant Prod Sci 9:219–227

    Article  CAS  Google Scholar 

  • Kohl DH, Shearer G, Harper JE (1980) Estimates of N2-fixation based on differences in the natural abundance of I5N in nodulating and non-nodulating isolines of soybeans. Plant Physiol 66:61–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kyei-Boahen S, Slankard A, Walley F (2002) Isotopic fractionation during N2 fixation by chickpea. Soil Biol Biochem 34:417–420

    Article  CAS  Google Scholar 

  • Ledgard SF, Brier GJ, Upsdell MP (1990) Effect of clover cultivar on production and nitrogen fixation in clover-ryegrass swards under dairy cow grazing. New zeal. J Agric Res 33:243–249

    Google Scholar 

  • Ledgard SF, Sprosen MS, Steele KW (1996) Nitrogen fixation by nine white clover cultivars in grazed pasture, as affected by nitrogen fertilization. Plant Soil 178:193–203

    Article  CAS  Google Scholar 

  • López-Bellido FJ, López-Bellido RJ, Redondo R, López-Bellido L (2010) B value and isotopic fractionation in N2 fixation by chickpea (Cicer arietinum L.) and faba bean (Vicia faba L.) Plant Soil 337:425–434

    Article  Google Scholar 

  • Malarvizhi P, Ladha JK (1999) Influence of available nitrogen and rice genotype on associative dinitrogen fixation. Soil Sci Soc Am J 63:93–99

    Article  CAS  Google Scholar 

  • McAuliffe C, Chamblee DS, Uribe-Arango H, Woodhouse WW Jr (1958) Influence of inorganic nitrogen on nitrogen fixation by legumes as revealed by N15. Agron J 50:334–337

    Article  CAS  Google Scholar 

  • McNeill AM, Hood RC, Wood M (1994) Direct measurement of nitrogen fixation by Trifolium repens L. and Alnus glutinosa L. using 15N2. J Exp Bot 45:749–755

    Article  CAS  Google Scholar 

  • Mohr RM, Janzen HH, Bremer E, Entz MH (1998) Fate of symbiotically-fixed 15N2 as influenced by method of alfalfa termination. Soil Biol Biochem 30:1359–1367

    Article  CAS  Google Scholar 

  • Nebiyu A, Huygens D, Upadhayay HR, Diels J, Boeckx P (2014) Importance of correct B value determination to quantify biological N2 fixation and N balances of faba beans (Vicia faba L.) via 15N natural abundance. Biol Fertil Soils 50:517–525

    Article  CAS  Google Scholar 

  • Okito A, Alves BJR, Urquiaga S, Boddey RM (2004) Isotopic fractionation during N2 fixation by four tropical legumes. Soil Biol Biochem 36:1179–1190

    Article  CAS  Google Scholar 

  • Olesniewicz KE, Thomas RB (1999) Effects of mycorrhizal colonization on biomass production and nitrogen fixation of black locust (Robinia pseudoacacia) seedlings grown under elevated atmospheric carbon dioxide. New Phytol 142:133–140

    Article  Google Scholar 

  • Pacheco RS, Boddey RM, Alves BJR, Straliotto R, Araújo AP (2017) Growth patterns of common bean cultivars affect the 'B' value required to quantify biological N2 fixation using the 15N natural abundance technique. Plant Soil 419:293–304

  • Pauferro N, Guimarães AP, Jantalia CP, Urquiaga S, Alves BJR, Boddey RM (2010) 15N natiral abundance of biologically fixed N2 in soybean is controlled more by the Bradyrhizobium strain than by the variety of the host plant. Soil Biol Biochem 42:1694–1700

    Article  CAS  Google Scholar 

  • Pareek RP, Ladha JK, Watanabe I (1990) Estimating N2 fixation by Sesbania rostrata and S. cannabina (syn. S. aculeata) in lowland rice soil by the 15N dilution method. Biol Fertil Soils 10:77–88

    Google Scholar 

  • Peoples MB, Chalk PM, Unkovich MJ, Boddey RM (2015) Can differences in 15N natural abundance be used to quantify the transfer of nitrogen from legumes to non-legume plant species. Soil Biol Biochem 87:97–109

    Article  CAS  Google Scholar 

  • Peoples MB, Craswell ET (1992) Biological nitrogen fixation: investments, expectations and actual contributions to agriculture. Plant Soil 141:13–39

    Article  CAS  Google Scholar 

  • Pereira PAA, Burris RH, Bliss FA (1989) N-determined dinitrogen fixation potential of genetically diverse bean lines (Phaseolus vulgaris L.) Plant Soil 120:171–179

    Article  CAS  Google Scholar 

  • Polania J, Poschenrieder C, Rao I, Beebe S (2016) Estimation of phenotypic variability in symbiotic nitrogen fixation ability of common bean under drought stress using 15N natural abundance in grain. Eur J Agron 79:66–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 89:563–570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riffkin PA, Quigley PE, Kearney GA, Cameron FJ, Gault RR, Peoples MB, Theis JE (1999) Factors associated with biological nitrogen fixation in dairy pastures in south-western Victoria. Crop Pasture Sci 50:261–272

    Article  Google Scholar 

  • Ruschel AP, Vose PB, Matsui E, Victoria RL, Tsai Saito SM (1982) Field evaluation of N2-fixation and N-utilization by Phaseolus bean varieties determined by 15N isotope dilution. Plant Soil 65:397–407

    Article  Google Scholar 

  • Schortemeyer M, Atkin OK, McFarlane N, Evans JR (1999) The impact of elevated atmospheric CO2 and nitrate supply on growth, biomass allocation, nitrogen partitioning and N2 fixation of Acacia melanoxylon. Aust J Plant Physiol 26(8):737

    Article  CAS  Google Scholar 

  • Schweiger P, Hofer M, Hartl W, Wanek W, Vollmann J (2012) N2 fixation by organically grown soybean in Central Europe: method of quantification and agronomic effects. Eur J Agron 41:11–17

    Article  CAS  Google Scholar 

  • Schweiger P, Hofer M, Vollmann J, Wanek W (2014) The relationship between N isotopic fractionation within soybean and N2 fixation during soybean development. Physiol Plant 152:546–557

    Article  CAS  PubMed  Google Scholar 

  • Shearer G, Kohl DH (1986) N2 fixation in field settings: estimates based on natural 15N abundance. Funct Plant Biol 13:699–756

    CAS  Google Scholar 

  • Shearer G, Kohl DH (1993) Natural abundance of 15N: fractional contribution of two sources to a common sink and use of isotope discrimination. In: Knowles R, Blackburn TH (eds) Nitrogen Isotope Techniques. Academic Press, Inc., San Deigo, pp 89–125

    Chapter  Google Scholar 

  • Shearer G, Kohl DH, Harper JE (1980) Distribution of 15N among plant parts of nodulating and nonnodulating isolines of soybeans. Plant Physiol 66:57–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shrestha RK, Ladha JK (1996) Genotypic variation in promotion of rice dinitrogen fixation as determined by nitrogen-15 dilution. Soil Sci Soc Am J 60:1815–1821

    Article  CAS  Google Scholar 

  • Smith AP, Chen D, Chalk PM (2009) N2 fixation by faba bean (Vicia faba L.) in a gypsum-amended sodic soil. Biol Fertil Soils 45:329–333

    Article  Google Scholar 

  • Snoeck D, Zapata F, Domenach A-M (2000) Isotopic evidence of the transfer of nitrogen fixed by legumes to coffee trees. Biotechnol Agron Soc Environ 4:95–100

    CAS  Google Scholar 

  • St. Clair DA, Bliss FA (1991) Intrapopulation recombination for 15N-determined dinitrogen fixation ability in common bean. Plant Breed 106:215–225

    Article  Google Scholar 

  • St. Clair DA, Wolyn DJ, DuBois J, Burris RH, Bliss FA (1988) Field comparison of dinitrogen fixation determined with nitrogen-15-depleted and nitrogen-15-enriched ammonium sulfate in selected inbred backcross lines of common bean. Crop Sci 28:773–778

    Article  Google Scholar 

  • Unkovich M (2013) Isotope discrimination provides new insight into biological nitrogen fixation. New Phytol 198:643–646

    Article  CAS  PubMed  Google Scholar 

  • 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. Australian Centre for International Agricultural Research, Canberra, 258 pp

    Google Scholar 

  • Unkovich MJ, Pate JS, Sanford P, Armstrong EL (1994) Potential precision of the δ15N natural abundance method in field estimates of nitrogen fixation by crop and pasture legumes in S.W. Australia. Crop Past Sci 45:119–132

    Article  Google Scholar 

  • Vallis I, Haydock KP, Ross PJ, Henzell EF (1967) Isotopic studies on the uptake of nitrogen by pasture plants. III. The uptake of small additions of 15N-labelled fertilizer by Rhodes grass and Townsville Lucerne. Crop Past Sci 18:865–877

    Article  CAS  Google Scholar 

  • Van Kessel C, Nakao P (1986) The use of nitrogen-15-depleted ammonium sulfate for estimating nitrogen fixation by leguminous trees. Agron J 78:549–551

    Article  Google Scholar 

  • Vitousek PM, Cassman K, Cleveland C, Crews T, Fields CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter E, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57(58):1–45

    Article  Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499

    Article  CAS  Google Scholar 

  • Voisin A-S, Bourion V, Duc G, Salon C (2007) Using an ecophysiological analysis to dissect genetic variability and to propose an ideotype for nitrogen nutrition of pea. Ann Bot 100:1525–1536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wanek W, Arndt SK (2002) Difference in δ15N signatures between nodulated roots and shoots of soybean is indicative of the contribution of symbiotic N2 fixation to plant N. J Exp Bot 53:1109–1118

    Article  CAS  PubMed  Google Scholar 

  • Wolyn DJ, St. Clair DA, DuBois J, Rosas JC, Burris RH, Bliss FA (1991) Distribution of nitrogen in common bean (Phaseolus vulgaris L.) genotypes selected for differences in nitrogen fixation ability. Plant Soil 138:303–311

    Article  CAS  Google Scholar 

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Chalk, P.M., Craswell, E.T. An overview of the role and significance of 15N methodologies in quantifying biological N2 fixation (BNF) and BNF dynamics in agro-ecosystems. Symbiosis 75, 1–16 (2018). https://doi.org/10.1007/s13199-017-0526-z

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