Abstract
The effect of environmental factors on the proportion of the nitrogen (N) derived from the atmosphere (Ndfa) in soybean [Glycine max (L.) Merril] have been traditionally approached individually given their intrinsic complexity. Alternatively, a more in-depth investigation of such complex interactions can be pursued by delimiting environments where Ndfa is uniform. Thus, the aim of this study was to define environments on 24 sites by extensively characterizing weather, plant, and Ndfa-related traits to find discriminant variables defining three Ndfa classes (low, medium, and high). The Ndfa was determined at the beginning of the seed filling (R5 growth stage) using the 15N natural abundance method. Twenty environmental variables were utilized to categorize Ndfa in low (< 57%), medium (57–66%), and high (≥ 66%) classes via implementation of discriminant multivariate analysis. The Ndfa averaged 60%, lower to previous values reported for Brazil (ranging from 69 to 94%). Mean air temperature, associated to SOM and soil N, was the most important variable related to low Ndfa, while improving soil fertility (soil pH, base saturation, exchangeable Ca and Mg, and available P) was critical for high Ndfa and, consequently, seed yield. The high contribution of those factors highlight the importance of implementing strategies to improve soil fertility, to promote better plant growth, and thus enhancing Ndfa contribution to crop N uptake.
Similar content being viewed by others
References
Alves BJR, Zotarelli L, Fernandes FM et al (2006) Fixação biológica de nitrogênio e fertilizantes nitrogenados no balanço de nitrogênio em soja, milho e algodão. Pesq Agrop Bras 41:449–456. https://doi.org/10.1590/S0100-204X2006000300011
Alves LA, Ambrosini VG, Denardin LG de O et al (2021) Biological N2 fixation by soybeans grown with or without liming on acid soils in a no-till integrated crop-livestock system. Soil Tillage Res 209. https://doi.org/10.1016/j.still.2020.104923
Ambrosini VG, Fontoura SMV, de Moraes RP et al (2019a) Assessing nitrogen limitation in inoculated soybean in Southern Brazil. Agrosyst Geosci Environ 190016:1–6. https://doi.org/10.2134/age2019.03.0016
Ambrosini VG, Fontoura SMV, de Moraes RP et al (2019b) Soybean yield response to Bradyrhizobium strains inoculation in fields with inoculation history in Southern Brazil. J Plant Nutr 42:1–11. https://doi.org/10.1080/01904167.2019.1648680
Aparecido LE de O, de Souza Rolim G, Richetti J et al (2016) Köppen, Thornthwaite and Camargo climate classifications for climatic zoning in the State of Paraná, Brazil. Ciênc Agrotecnol 40:405–417. https://doi.org/10.1590/1413-70542016404003916
Balboa GR, Ciampitti IA (2020) Estimating biological nitrogen fixation in field-grown soybeans: impact of B value. Plant Soil 446:195–210. https://doi.org/10.1007/s11104-019-04317-1
Chessel D, Dufour AB, Thioulouse J (2004) The ade4 package - I: one-table methods. R News 4:5–10
Ciampitti IA, Salvagiotti F (2018) New insights into soybean biological nitrogen fixation. Agron J 110:1185–1196. https://doi.org/10.2134/agronj2017.06.0348
Collino DJ, Salvagiotti F, Perticari A et al (2015) Biological nitrogen fixation in soybean in Argentina: relationships with crop, soil, and meteorological factors. Plant Soil 392:239–252. https://doi.org/10.1007/s11104-015-2459-8
Cooper JE, Scherer HW (2012) Nitrogen fixation. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants, 3rd edn. Acaddemic Press, London, pp 389–408
Córdova SC, Castellano MJ, Dietzel R et al (2019) Soybean nitrogen fixation dynamics in Iowa, USA. F Crop Res 236:165–176. https://doi.org/10.1016/j.fcr.2019.03.018
Di Ciocco C, Penón E, Coviella C et al (2011) Nitrogen fixation by soybean in the Pampas: relationship between yield and soil nitrogen balance. Agrochimica 55:1–10
Divito GA, Sadras VO (2014) How do phosphorus, potassium and sulphur affect plant growth and biological nitrogen fixation in crop and pasture legumes? A meta-analysis. F Crop Res 156:161–171. https://doi.org/10.1016/j.fcr.2013.11.004
Du M, Gao Z, Li X, Liao H (2020) Excess nitrate induces nodule greening and reduces transcript and protein expression levels of soybean leghaemoglobins. Ann Bot 126:61–72. https://doi.org/10.1093/aob/mcaa002
Ellert BH, Bettany JR (1992) Temperature dependence of net nitrogen and sulfur mineralization. Soil Sci Soc Am J 56:1133–1141. https://doi.org/10.2136/sssaj1992.03615995005600040021x
Fehr WR, Caviness CE (1977) Stages of soybean development. Spec. Report. 87 12 p
Ferguson BJ, Gresshoff PM (2016) Physiological implications of legume nodules associated with soil acidity. In: Sulieman S, Tran L-SP (eds) Legume nitrogen fixation in a changing environment - achievements and challenges. Springer, Cham, pp 113–125
Ferguson BJ, Lin M-H, Gresshoff PM (2013) Regulation of legume nodulation by acidic growth conditions. Plant Signal Behav 8:e23426. https://doi.org/10.4161/psb.23426
Fontoura SMV, Bayer C (2009) Adubação nitrogenada para alto rendimento de milho em plantio direto na região centro-sul do Paraná. Rev Bras Cienc 33:1721–1732. https://doi.org/10.1590/S0100-06832009000600021
Fontoura SMV, Vieira RCB, Bayer C et al (2015) Fertilidade do solo e seu manejo em plantio direto no Centro-Sul do Paraná. Fundação Agrária de Pesquisa Agropecuária, Guarapuava
Fujikake H, Yamazaki A, Ohtake N et al (2003) Quick and reversible inhibition of soybean root nodule growth by nitrate involves a decrease in sucrose supply to nodules. J Exp Bot 54:1379–1388. https://doi.org/10.1093/jxb/erg147
George T, Singleton PW, Ben Bohlool B (1988) Yield, soil nitrogen uptake, and nitrogen fixation by soybean from four maturity groups grown at three elevations. Agron J 80:563–567. https://doi.org/10.2134/agronj1988.00021962008000040004x
Guimarães AP, de Morais RF, Urquiaga S et al (2008) Bradyrhizobium strain and the 15N natural abundance quantification of biological N2 fixation in soybean. Sci Agric 65:516–524. https://doi.org/10.1590/S0103-90162008000500011
Herridge DF, Turpin JE, Robertson MJ (2001) Improving nitrogen fixation of crop legumes through breeding and agronomic management: analysis with simulation modelling. Aust J Exp Agric 41:391–401. https://doi.org/10.1071/EA00041
Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18. https://doi.org/10.1007/s11104-008-9668-3
Hungria M, Franco AA (1993) Effects of high temperature on nodulation and nitrogen fixation by Phaseolus vulgaris L. Plant Soil 149:95–102. https://doi.org/10.1007/BF00010766
Hungria M, Mendes IC (2015) Nitrogen fixation with soybean: the perfect symbiosis? In: de Bruijn FJ (ed) Biological nitrogen fixation. Wiley Inc, Hoboken, pp 1005–1023
Hungria M, Stacey G (1997) Molecular signals exchanged between host plants and rhizobia: basic aspects and potential application in agriculture. Soil Biol Biochem 29:819–830. https://doi.org/10.1016/S0038-0717(96)00239-8
Hungria M, Vargas MAT (2000) Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. F Crop Res 65:151–164. https://doi.org/10.1016/S0378-4290(99)00084-2
Hungria M, Franchini JC, Campo RJ, Graham PH (2005) The importance of nitrogen fixation to soybean cropping in South America. In: Werner D, Newton WE (eds) Nitrogen fixation in agriculture, forestry, ecology, and the environment. Springer, Dordrecht, pp 25–42
Hungria M, Franchini JC, Campo RJ et al (2006) Nitrogen nutrition of soybean in Brazil: contributions of biological N2 fixation and N fertilizer to grain yield. Can J Plant Sci 86:927–939. https://doi.org/10.4141/P05-098
Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071. https://doi.org/10.1093/bioinformatics/btr521
Keyser HH, Li F (1992) Potential for increasing biological nitrogen fixation in soybean. Plant Soil 141:119–135. https://doi.org/10.1007/BF00011313
Lévy J, Bres C, Geurts R et al (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science (80-) 303:1361–1364. https://doi.org/10.1126/science.1093038
Lim CW, Lee YW, Lee SC, Hwang CH (2014) Nitrate inhibits soybean nodulation by regulating expression of CLE genes. Plant Sci 229:1–9. https://doi.org/10.1016/j.plantsci.2014.08.014
Lin MH, Gresshoff PM, Ferguson BJ (2012) Systemic regulation of soybean nodulation by acidic growth conditions. Plant Physiol 160:2028–2039. https://doi.org/10.1104/pp.112.204149
Mapope N, Dakora FD (2016) N2 fixation, carbon accumulation, and plant water relations in soybean (Glycine max L. Merrill) varieties sampled from farmers’ fields in South Africa, measured using 15N and 13C natural abundance. Agric Ecosyst Environ 221:174–186. https://doi.org/10.1016/j.agee.2016.01.023
Miransari M, Balakrishnan P, Smith D et al (2006) Overcoming the stressful effect of low pH on soybean root hair curling using lipochitooligosacharides. Commun Soil Sci Plant Anal 37:1103–1110. https://doi.org/10.1080/00103620600586391
Moro Rosso LH, Reis AFB, Tamagno S, Correndo AA, Prasad PVV, Ciampitti IA (2023) Temporal variation of soil N supply defines N fixation in soybeans. Eur J Agron 144:126745. https://doi.org/10.1016/j.eja.2023.126745
Ordóñez RA, Castellano MJ, Hatfield JL et al (2018) Maize and soybean root front velocity and maximum depth in Iowa, USA. F Crop Res 215:122–131. https://doi.org/10.1016/j.fcr.2017.09.003
Pauferro N, Guimarães AP, Jantalia CP et al (2010) 15N natural 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. https://doi.org/10.1016/j.soilbio.2010.05.032
Peng WT, Zhang LD, Zhou Z et al (2018) Magnesium promotes root nodulation through facilitation of carbohydrate allocation in soybean. Physiol Plant 163:372–385. https://doi.org/10.1111/ppl.12730
Peoples MB, Craswell ET (1992) Biological nitrogen fixation: investments, expectations and actual contributions to agriculture. Plant Soil 141:13–39. https://doi.org/10.1007/BF00011308
Purcell LC, Serraj R, Sinclair TR, De A (2004) Soybean N2 fixation estimates, ureide concentration, and yield responses to drought. Crop Sci 44:484–492
Riffkin PA, Quigley PE, Kearney GA et al (1999) Factors associated with biological nitrogen fixation in dairy pastures in south-western Victoria. Aust J Agric Res 50:261–272. https://doi.org/10.1071/A98035
Sadras VO, Lake L, Li Y et al (2016) Phenotypic plasticity and its genetic regulation for yield, nitrogen fixation and δ13C in chickpea crops under varying water regimes. J Exp Bot 67:4339–4351. https://doi.org/10.1093/jxb/erw221
Salvagiotti F, Specht JE, Cassman KG et al (2009) Growth and nitrogen fixation in high-yielding soybean: impact of nitrogen fertilization. Agron J 101:958–970. https://doi.org/10.2134/agronj2008.0173x
Santachiara G, Borrás L, Salvagiotti F et al (2017) Relative importance of biological nitrogen fixation and mineral uptake in high yielding soybean cultivars. Plant Soil 418:191–203. https://doi.org/10.1007/s11104-017-3279-9
Santachiara G, Salvagiotti F, Rotundo JL (2019) Nutritional and environmental effects on biological nitrogen fixation in soybean: a meta-analysis. F Crop Res 240:106–115. https://doi.org/10.1016/j.fcr.2019.05.006
Schipanski ME, Drinkwater LE, Russelle MP (2010) Understanding the variability in soybean nitrogen fixation across agroecosystems. Plant Soil 329:379–397. https://doi.org/10.1007/s11104-009-0165-0
Serraj R, Sinclair TR, Purcell LC (1999) Symbiotic N2 fixation response to drought. J Exp Bot 50:143–155. https://doi.org/10.1093/jxb/50.331.143
Shearer G, Kohl DH (1986) N2-fixation in field settings: estimations based on natural 15N abundance. Aust J Plant Physiol 13:699–756. https://doi.org/10.1071/PP9860699
Sinclair TR, Nogueira MA (2018) Selection of host-plant genotype: the next step to increase grain legume N2 fixation activity. J Exp Bot 69:3523–3530. https://doi.org/10.1093/jxb/ery115
Staff SS (2014) Keys to soil taxonomy, 12th edn. USDA-Natural Resources Conservation Service, Washington
Stanford G, Frere MH, Schwaninger DH (1973) Temperature coefficient of soil nitrogen mineralization. Soil Sci 115:321–323
Streeter J, Wong PP (1988) Inhibition of legume nodule formation and N2 fixation by nitrate. CRC Crit Rev Plant Sci 7:1–23. https://doi.org/10.1080/07352688809382257
Tamagno S, Balboa GR, Assefa Y et al (2017) Nutrient partitioning and stoichiometry in soybean: a synthesis-analysis. F Crop Res 200:18–27. https://doi.org/10.1016/j.fcr.2016.09.019
Tamagno S, Sadras VO, Haegele JW et al (2018) Interplay between nitrogen fertilizer and biological nitrogen fixation in soybean: implications on seed yield and biomass allocation. Sci Rep 8:1–11. https://doi.org/10.1038/s41598-018-35672-1
Tedesco MJ, Gianello C, Bissani C et al (1995) Análise de solo, plantas e outros materiais, 2nd edn. Departamento de Solos da Universidade Federal do Rio Grande do Sul, Porto Alegre
Torabian S, Farhangi-Abriz S, Denton MD (2019) Do tillage systems influence nitrogen fixation in legumes? A review. Soil Tillage Res 185:113–121. https://doi.org/10.1016/j.still.2018.09.006
Tsai S, Bonetti R, Agbala S, Rossetto R (1993) Minimizing the effect of mineral nitrogen on biological nitrogen fixation in common bean by increasing nutrient levels. Plant Soil:131–138. https://doi.org/10.1007/BF00016342
van Kessel C, Hartley C (2000) Agricultural management of grain legumes: has it led to an increase in nitrogen fixation? F Crop Res 65:165–181. https://doi.org/10.1016/S0378-4290(99)00085-4
Wais RJ, Keating DH, Long SR (2002) Structure-function analysis of Nod factor-induced root hair calcium spiking in rhizobium-legume symbiosis. Plant Physiol 129:211–224. https://doi.org/10.1104/pp.010690
Acknowledgements
The authors thank the staff of the Fundação Agrária de Pesquisa Agropecuária, whose help and support at field activities were essential.
Funding
This study was supported by Coordination for the Improvement of Personnel in Higher Education (CAPES), National Council for Scientific and Technological Development (CNPq) (207113/2017–3), and Kansas State Research and Extension (19–789).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ambrosini, V.G., Ciampitti, I.A., Fontoura, S.M.V. et al. Environmental variables controlling biological nitrogen fixation in soybean. Symbiosis (2024). https://doi.org/10.1007/s13199-024-00988-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13199-024-00988-2