Contribution of different sources and origins of nitrogen in above- and below-ground structures to the partial nitrogen balance in soybean.

Kehoe, Esteban; Rubio, Gerardo; Salvagiotti, Fernando

doi:10.1007/s11104-022-05418-0

Regular Article
Published: 15 April 2022

Contribution of different sources and origins of nitrogen in above- and below-ground structures to the partial nitrogen balance in soybean.

Plant and Soil (2022)Cite this article

158 Accesses
Metrics details

A Correction to this article was published on 04 July 2022

This article has been updated

Abstract

Aims

Most studies that quantified the biological N fixation (BNF) and partial N balances of soybean have ignored the belowground structures. Our objectives were to evaluate the contribution of belowground structures to the partial N balance of soybean and to identify the origin (soil or BNF) and source (apparent remobilization or current gain during the seed-filling period) of seed N.

Methods

Biomass, BNF, and N uptake coming from different N sources and origins, including belowground structures, were quantified in a two-year field study involving two soybean genotypes (MG IV and V) and two water availability conditions (rainfed and irrigated).

Results

The inclusion of BNF-derived N present in belowground components (which averaged +12 kg N ha⁻¹ at R₇) changed the results of the partial N balances from negative to positive. BNF was the main origin of seed N, accounting for 73 and 79% of seed N under water stressed and non-stressed conditions, respectively. Regarding the seed N source, apparent remobilization was the main contributor to seed N under water stress, whereas current N gain was the main contributor to seed N in unstressed plants.

Conclusions

We conclude that i) the root system retains a relevant proportion of the atmospheric N fixed during the crop cycle and should be included in the partial N balance estimations; and ii) BNF is the main origin of seed N, even under contrasting growing conditions.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Change history

04 July 2022
A Correction to this paper has been published: https://doi.org/10.1007/s11104-022-05541-y

Abbreviations

N:: Nitrogen uptake
BNF:: Biological nitrogen fixation
BNF-N:: Nitrogen from biological nitrogen fixation
soil-N:: Nitrogen intake from soil nitrogen
%Ndfa:: Percentage of biological nitrogen fixation
BB:: Belowground biomass
AB:: Aboveground biomass
AB_Veg :: Vegetative aboveground biomass
Tot:: Total biomass
PB:: Partial balance

References

Anglade J, Billen G, Garnier J (2015) Relationships for estimating N₂ fixation in legumes: incidence for N balance of legume-based cropping systems in Europe. Ecosphere 6:art37. https://doi.org/10.1890/ES14-00353.1
Article Google Scholar
Bacanamwo M, Purcell LC (1999) Soybean root morphological and anatomical traits associated with acclimation to flooding. Crop Sci 39:143–149. https://doi.org/10.2135/cropsci1999.0011183X003900010023x
Article Google Scholar
Bacigaluppo S, Bodrero ML, Balzarini M, Gerster GR, Andriani JM, Enrico JM, Dardanelli JL (2011) Main edaphic and climatic variables explaining soybean yield in Argiudolls under no-tilled systems. Eu J Agron 35(4):247–254. https://doi.org/10.1016/j.eja.2011.07.001
Article Google Scholar
Bationo A, Kihara J, Vanlauwe B, Waswa B, Kimetu J (2007) Soil organic carbon dynamics, functions and management in west African agro-ecosystems. Agric Syst 94:13–25. https://doi.org/10.1016/j.agsy.2005.08.011
Article Google Scholar
Bender RR, Haegele JW, Below FE (2015) Nutrient uptake, partitioning, and remobilization in modern soybean varieties. Agron J 107:563–573. https://doi.org/10.2134/agronj14.0435
CAS Article Google Scholar
Bergersen FJ, Turner GL, Peoples MB, Gault RR, Morthorpe LJ, Brockwell J (1992) Nitrogen fixation during vegetative and reproductive growth of irrigated soybeans in the field: application of 15N methods. Aust J Agric Res 43:145–153. https://doi.org/10.1071/AR9920145
CAS Article Google Scholar
Cafaro La Menza N, Monzon JP, Specht JE, Grassini P (2017) Is soybean yield limited by nitrogen supply? Field Crop Res 213:204–212. https://doi.org/10.1016/j.fcr.2017.08.009
Article Google Scholar
Carranca C, Torres MO, Madeira M (2015) Underestimated role of legume roots for soil N fertility. Agron Sustain Dev 35:1095–1102. https://doi.org/10.1007/s13593-015-0297-y
CAS Article Google Scholar
Cassman KG, Whitney AS, Stockinger KR (1980) Root growth and dry matter distribution of soybean as affected by phosphorus stress, nodulation, and nitrogen source1. Crop Sci 20:239–244. https://doi.org/10.2135/cropsci1980.0011183X002000020022x
CAS Article Google Scholar
Cheng W, Johnson DW, Fu S (2003) Rhizosphere effects on decomposition. Soil Sci Soc Am J 67:1418–1427. https://doi.org/10.2136/sssaj2003.1418
CAS Article Google Scholar
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
CAS Article Google Scholar
Collino DJ, Salvagiotti F, Perticari A, Piccinetti C, Ovando G, Urquiaga S, Racca RW (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
CAS Article Google Scholar
Dardanelli JL, Bachmeier OA, Sereno R, Gil R (1997) Rooting depth and soil water extraction patterns of different crops in a silty loam haplustoll. Field Crop Res 54:29–38. https://doi.org/10.1016/S0378-4290(97)00017-8
Article Google Scholar
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2011) InfoStat. versión 24-03-2011 edn. Universidad Nacional de Córdoba, Córdoba, Argentina
Dingkuhn M, Le Gal PY (1996) Effect of drainage date on yield and dry matter partitioning in irrigated rice. Field Crop Res 46(1–3):117–126. https://doi.org/10.1016/0378-4290(95)00094-1
Article Google Scholar
Dominguez J, Rubio G (2019) Agriculture. In: Rubio G, Lavado R, Pereyra F (eds) The soils of Argentina. World soils book series. Springer, Cham, pp 209–238. https://doi.org/10.1007/978-3-319-76853-3_16
Chapter Google Scholar
Erisman JW, Sutton MA, Galloway J, Klimont Z, Winiwarter W (2008) How a century of ammonia synthesis changed the world. Nat Geosci 1:636–639. https://doi.org/10.1038/ngeo325
CAS Article Google Scholar
Fan J, McConkey B, Wang H, Janzen H (2016) Root distribution by depth for temperate agricultural crops. Field Crop Res 189:68–74. https://doi.org/10.1016/j.fcr.2016.02.013
Article Google Scholar
Fehr WR, Caviness CE (1977) Stages of soybean development. Coop. Ext. Serv., agriculture and home economics Exp. Stn., Iowa state Univ., Ames
Food and Agriculture Organization of the United Nations (2021) FAOSTAT Database. Rome, Italy: FAO. Retrieved September 23, 2021 from http://www.fao.org/faostat/en/#data/RFN
Fustec J, Lesuffleur F, Mahieu S, Cliquet JB (2010) Nitrogen rhizodeposition of legumes. A review. Agron Sustain Dev 30:57–66. https://doi.org/10.1051/agro/2009003
CAS Article Google Scholar
Gaspar AP, Laboski CAM, Naeve SL, Conley SP (2017) Dry matter and nitrogen uptake, partitioning, and removal across a wide range of soybean seed yield levels. Crop Sci 57:2170–2182. https://doi.org/10.2135/cropsci2016.05.0322
CAS Article Google Scholar
Gelfand I, Philip Robertson G (2014) A reassessment of the contribution of soybean biological nitrogen fixation to reactive N in the environment. Biogeochemistry 123:175–184. https://doi.org/10.1007/s10533-014-0061-4
CAS Article Google Scholar
Giller KE, Cadisch G (1995) Future benefits from biological nitrogen fixation: an ecological approach to agriculture. In: Ladha JK, Peoples MB (eds) Management of biological nitrogen fixation for the development of more productive and sustainable agricultural systems. Developments in plant and soil sciences, vol 65. Springer, Dordrecht, Dordrecht. https://doi.org/10.1007/978-94-011-0053-3_13
Chapter Google Scholar
Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research. Wiley
Google Scholar
Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451:293–296. https://doi.org/10.1038/nature06592
CAS Article PubMed Google Scholar
Grubinger V, Zobel R, Vendeland J, Cortes P (1982) Nodule distribution on roots of field-grown soybeans in subsurface soil horizons 1. Crop Sci 22(1):153–155. https://doi.org/10.2135/cropsci1982.0011183X002200010036x
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 1. Plant Physiol 93:708–716. https://doi.org/10.1104/pp.93.2.708
CAS Article PubMed PubMed Central Google Scholar
Hoogenboom G, Huck MG, Peterson CM (1987) Root growth rate of soybean as affected by drought stress1. Agron J 79:607–614. https://doi.org/10.2134/agronj1987.00021962007900040003x
Article Google Scholar
Jackson RB, Lajtha K, Crow SE, Hugelius G, Kramer MG, Piñeiro G (2017) The ecology of soil carbon: pools, vulnerabilities, and biotic and abiotic controls. Annu Rev Ecol Evol S 48:419–445. https://doi.org/10.1146/annurev-ecolsys-112414-054234
Article Google Scholar
Kätterer T, Bolinder MA, Andrén O, Kirchmann H, Menichetti L (2011) Roots contribute more to refractory soil organic matter than above-ground crop residues, as revealed by a long-term field experiment. Agric Ecosyst Environ 141:184–192. https://doi.org/10.1016/j.agee.2011.02.029
Article Google Scholar
Kirda C, Danso SKA, Zapata F (1989) Temporal water stress effects on nodulation, nitrogen accumulation and growth of soybean. Plant Soil 120:49–55. https://doi.org/10.1007/BF02370289
Article Google Scholar
Kumar PA, Parry MAJ, Mitchell RAC, Ahmad A, Abrol YP (2002) Photosynthesis and nitrogen-use efficiency. In: Foyer CH, Noctor G (eds) Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism. Advances in photosynthesis and respiration, vol 12. Springer, Dordrecht. https://doi.org/10.1007/0-306-48138-3_2
Chapter Google Scholar
Kumudini S, Hume DJ, Chu G (2002) Genetic improvement in short-season soybeans: ii. Nitrogen accumulation, remobilization, and partitioning. Crop Sci 42:141–145. https://doi.org/10.2135/cropsci2002.1410
Article PubMed Google Scholar
Laberge G, Franke AC, Ambus P, Høgh-Jensen H (2009) Nitrogen rhizodeposition from soybean (Glycine max) and its impact on nutrient budgets in two contrasting environments of the Guinean savannah zone of Nigeria. Nutr Cycl Agroecosyst 84:49–58. https://doi.org/10.1007/s10705-008-9225-8
Article Google Scholar
Ladha JK, Jat ML, Stirling CM, Chakraborty D, Pradhan P, Krupnik TJ, Sapkota TB, Pathak H, Rana DS, Tesfaye K, Gerard B (2020) Chapter two - achieving the sustainable development goals in agriculture: the crucial role of nitrogen in cereal-based systems. In: Sparks DL (ed) Adv Agron, 163rd edn. Academic Press. https://doi.org/10.1016/bs.agron.2020.05.006
Chapter Google Scholar
Manavalan LP, Guttikonda SK, Nguyen VT, Shannon JG, Nguyen HT (2010) Evaluation of diverse soybean germplasm for root growth and architecture. Plant Soil 330:503–514. https://doi.org/10.1007/s11104-009-0222-8
CAS Article Google Scholar
Masclaux-Daubresse C, Reisdorf-Cren M, Orsel M (2008) Leaf nitrogen remobilisation for plant development and grain filling. Plant Biol 10:23–36. https://doi.org/10.1111/j.1438-8677.2008.00097.x
CAS Article PubMed Google Scholar
Mayaki WC, Stone LR, Teare ID (1976) Irrigated and nonirrigated soybean, corn, and grain sorghum root systems1. Agron J 68:532–534. https://doi.org/10.2134/agronj1976.00021962006800030028x
Article Google Scholar
Mazzilli SR, Kemanian AR, Ernst OR, Jackson RB, Piñeiro G (2015) Greater humification of belowground than aboveground biomass carbon into particulate soil organic matter in no-till corn and soybean crops. Soil Biol Biochem 85:22–30. https://doi.org/10.1016/j.soilbio.2015.02.014
CAS Article Google Scholar
McNeill AM, Zhu C, Fillery IRP (1997) Use of in situ ¹⁵N-labelling to estimate the total below-ground nitrogen of pasture legumes in intact soil;plant systems. Aus J Agr Res 48:295–304. https://doi.org/10.1071/A96097
Article Google Scholar
Mosconi F, Priano L, Hein N, Moscatelli G, Salazar J, Gutiérrez T, Cáceres L (1985) INTA, Instituto Nacional de Tecnología Agropecuaria. Carta de suelos de la República Argentina. Hoja 3360–7 y 8 –Totoras y Serodino
Muchow RC, Robertson MJ, Pengelly BC (1993) Accumulation and partitioning of biomass and nitrogen by soybean, mungbean and cowpea under contrasting environmental conditions. Field Crop Res 33:13–36. https://doi.org/10.1016/0378-4290(93)90092-2
Article Google Scholar
Nissen T, Rodriguez V, Wander M (2008) Sampling soybean roots: a comparison of excavation and coring methods. Commun Soil Sci Plan 39:1875–1883. https://doi.org/10.1080/00103620802073933
CAS Article Google Scholar
Novelli LE, Caviglia OP, Melchiori RJM (2011) Impact of soybean cropping frequency on soil carbon storage in Mollisols and Vertisols. Geoderma 167-168:254–260. https://doi.org/10.1016/j.geoderma.2011.09.015
CAS Article Google Scholar
Okito A, Alves BRJ, Urquiaga S, Boddey RM (2004) Isotopic fractionation during N2 fixation by four tropical legumes. Soil Biol Biochem 36:1179–1190. https://doi.org/10.1016/j.soilbio.2004.03.004
CAS Article Google Scholar
Ordoñez RA, Castellano MJ, Hatfield JL, Helmers MJ, Licht MA, Liebman M, Dietzel R, Martinez-Feria R, Iqbal J, Puntel LA, Córdova SC, Togliatti K, Wright EE, Archontoulis SV (2018) Maize and soybean root front velocity and maximum depth in Iowa, USA. Field Crop Res 215:122–131. https://doi.org/10.1016/j.fcr.2017.09.003
Article Google Scholar
Ortez OA, Salvagiotti F, Enrico JM, Prasad PVV, Armstrong P, Ciampitti IA (2018) Exploring nitrogen limitation for historical and modern soybean genotypes. Agron J 110:2080–2090. https://doi.org/10.2134/agronj2018.04.0271
CAS Article Google Scholar
Ortez OA, Tamagno S, Salvagiotti F, Prasad PVV, Ciampitti IA (2019) Soybean nitrogen sources and demand during the seed-filling period. Agron J 111:1779–1787. https://doi.org/10.2134/agronj2018.10.0656
CAS Article Google Scholar
Ping X, Zhou G, Zhuang Q, Wang Y, Zuo W, Shi G, Lin X, Wang Y (2010) Effects of sample size and position from monolith and core methods on the estimation of total root biomass in a temperate grassland ecosystem in Inner Mongolia. Geoderma 155:262–268. https://doi.org/10.1016/j.geoderma.2009.12.009
Article Google Scholar
Purcell LC, King CA (1996) Drought and nitrogen source effects on nitrogen nutrition, seed growth, and yield in soybean. J Plant Nutr 19:969–993. https://doi.org/10.1080/01904169609365173
CAS Article Google Scholar
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. https://doi.org/10.2135/cropsci2004.4840
CAS Article Google Scholar
Rochester IJ, Peoples MB, Constable GA, Gault RR (1998) Faba beans and other legumes add nitrogen to irrigated cotton cropping systems. Aus J Exp Agr 38:253–260. https://doi.org/10.1071/EA97132
Article Google Scholar
Roder W, Mason SC, Clegg MD, Kniep KR (1989) Crop root distribution as influenced by grain sorghum-soybean rotation and fertilization. Soil Sc Soc Am J 53:1464–1470. https://doi.org/10.2136/sssaj1989.03615995005300050027x
Article Google Scholar
Rubio G, Pereyra FX, Taboada MA (2019) Soils of the Pampean region. In: Rubio G, Lavado R, Pereyra F (eds) The soils of Argentina. World soils book series. Springer, Cham. https://doi.org/10.1007/978-3-319-76853-3_6
Chapter Google Scholar
Rymuza K, Eb R, Wysokiński A (2020) Nitrogen uptake from different sources by non-GMO. Soybean Varieties 10. https://doi.org/10.3390/agronomy10091219
Salon C, Avice J-C, Larmure A, Ourry A, Prudent M, Voisin A-S (2011) Plant N fluxes and modulation by nitrogen, heat and water stresses: a review based on comparison of legumes and non legume plants. Abiotic Stress in Plants–Mechanisms and Adaptations Intech Open Access Publisher, Rijeka, pp 79–118
Google Scholar
Salvagiotti F, Cassman KG, Specht JE, Walters DT, Weiss A, Dobermann A (2008) Nitrogen uptake, fixation and response to fertilizer N in soybeans: a review. Field Crop Res 108:1–13. https://doi.org/10.1016/j.fcr.2008.03.001
Article Google Scholar
Salvagiotti F, Specht JE, Cassman KG, Walters DT, Weiss A, Dobermann A (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
CAS Article Google Scholar
Salvagiotti F, Magnano L, Ortez O, Enrico J, Barraco M, Barbagelata P, Condori A, Di Mauro G, Manlla A, Rotundo J (2021) Estimating nitrogen, phosphorus, potassium, and sulfur uptake and requirement in soybean. Eu J Agron 127:126289. https://doi.org/10.1016/j.eja.2021.126289
CAS Article Google Scholar
Santachiara G, Borrás L, Salvagiotti F, Gerde JA, Rotundo JL (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
CAS Article Google Scholar
Serraj R, Sinclair TR, Purcell LC (1999) Symbiotic N2 fixation response to drought. Journal of Experimental Botany 50: 143–155. https://doi.org/10.1093/jxb/50.331.143
Shearer G, Kohl DH (1986) N fixation in field settings: estimations based on natural ¹⁵N abundance. Funct Plant Biol 13:699–756. https://doi.org/10.1071/PP9860699
CAS Article Google Scholar
Shearer G, Kohl DH, Harper JE (1980) Distribution of ¹⁵N among plant parts of Nodulating and Nonnodulating Isolines of soybeans 1. Plant Physiol 66:57–60. https://doi.org/10.1104/pp.66.1.57
CAS Article PubMed PubMed Central Google Scholar
Sinclair T, de Wit C (1975) Photosynthate and nitrogen requirements for seed production by various crops. Science 189:565–567. https://doi.org/10.1126/science.189.4202.565
CAS Article PubMed Google Scholar
Suematsu K, Abiko T, Nguyen VL, Mochizuki T (2017) Phenotypic variation in root development of 162 soybean accessions under hypoxia condition at the seedling stage. Plant Prod Sci 20(3):323–335. https://doi.org/10.1080/1343943X.2017.1334511
Article Google Scholar
Unkovich M, Herridge D, Peoples M, Cadisch G, Boddey B, Giller KE, Alves BJR, Chalk P (2008) Measuring plant-associated nitrogen fixation in agricultural systems. Australian Center for International Agricultural Research (ACIAR) Canberra, Australia. Monograph 136, 258pp. https://www.aciar.gov.au/publication/books-and-manuals/measuring-plant-associated-nitrogen-fixation-agricultural-systems
Varela MF, Scianca CM, Taboada MA, Rubio G (2014) Cover crop effects on soybean residue decomposition and P release in no-tillage systems of Argentina. Soil Tillage Res 143:59–66. https://doi.org/10.1016/j.still.2014.05.005
Article Google Scholar
Wang X, Yang Y, Pei K, Zhou J, Peixoto L, Gunina A, Zeng Z, Zang H, Rasmussen J, Kuzyakov Y (2021) Nitrogen rhizodeposition by legumes and its fate in agroecosystems: a field study and literature review. Land Degrad Dev 32:410–419. https://doi.org/10.1002/ldr.3729
Article Google Scholar
Werner RA, Schmidt HL (2002) The in vivo nitrogen isotope discrimination among organic plant compounds. Phytochemistry 61:465–484. https://doi.org/10.1016/S0031-9422(02)00204-2
CAS Article PubMed Google Scholar
Zeiher C, Egli DB, Leggett JE, Reicosky DA (1982) Cultivar differences in N redistribution in soybeans1. Agron J 74:375–379. https://doi.org/10.2134/agronj1982.00021962007400020027x
CAS Article Google Scholar

Download references

Acknowledgements

We are greatly thankful for the help of Dr. Fernando García on funding acquisition. We also thank Diego Uliassi for assistance in field collections and agronomy interns for essential research collaboration in laboratory assistance.

Funding

This work was supported by Agencia Nacional de Promocion Cientifica y Tecnológica (ANPCyT - PICT 03431), University of Buenos Aires (UBACYT 20020170100686BA), International Plant Nutrition Institute (IPNI) and Instituto Nacional de Tecnología Agropecuaria (INTA - National Projects PNCYO 1127033 and PE-I011).

Author information

Authors and Affiliations

Crops, Soil, and Water Management Group, National Institute of Agricultural Research (INTA), EEA Oliveros, Ruta 11 km 353, Oliveros, 2206, Santa Fe, Argentina
Esteban Kehoe & Fernando Salvagiotti
CONICET, Santa Fe, Argentina
Esteban Kehoe & Fernando Salvagiotti
INBA (UBA - CONICET) and Soil Fertility and Fertilizers, School of Agriculture, University of Buenos Aires, Av San Martin 4453, 1417, Buenos Aires, Argentina
Gerardo Rubio

Authors

Esteban Kehoe
View author publications
You can also search for this author in PubMed Google Scholar
Gerardo Rubio
View author publications
You can also search for this author in PubMed Google Scholar
Fernando Salvagiotti
View author publications
You can also search for this author in PubMed Google Scholar

Contributions

Esteban Kehoe: conceptualization, design of the research, performance of the research, data analysis, collection and interpretation, and writing the manuscript. Gerardo Rubio: conceptualization, funding acquisition, data interpretation and writing the manuscript. Fernando Salvagiotti: conceptualization, funding acquisition, design of the research, data interpretation and writing the manuscript. The authors read and approved the final manuscript.

Corresponding author

Correspondence to Fernando Salvagiotti.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

All authors consent to participate.

Consent for publication

All authors consent for publication.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible Editor: Euan K. James.

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.

Supplementary file1 (DOCX 34 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kehoe, E., Rubio, G. & Salvagiotti, F. Contribution of different sources and origins of nitrogen in above- and below-ground structures to the partial nitrogen balance in soybean.. Plant Soil (2022). https://doi.org/10.1007/s11104-022-05418-0

Download citation

Received: 22 October 2021
Accepted: 29 March 2022
Published: 15 April 2022
DOI: https://doi.org/10.1007/s11104-022-05418-0

Keywords

Soybean
Biological nitrogen fixation
¹⁵N abundance method
Apparent N gain
Apparent N remobilization
Belowground N