Shift in origin of plant nitrogen alters carbon and nitrogen assimilation during reproductive stages of soybean grown in a Mollisol
Y. S. Li A , X. B. Liu A , G. H. Wang A , Z. H. Yu A , U. Mathesius B , J. D. Liu A , S. J. Herbert C and J. Jin A D
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin 150081, China.
B Division of Plant Science, Research School of Biology, Australian National University, Canberra, ACT 2601, Australia.
C Stockbridge School of Agriculture, University of Massachusetts, Amherst, MA 01003, USA.
D Corresponding author. Email: jinjian29@hotmail.com
Crop and Pasture Science 67(8) 872-880 https://doi.org/10.1071/CP15184
Submitted: 7 June 2015 Accepted: 29 March 2016 Published: 29 July 2016
Abstract
Excessive fertiliser has been commonly applied in the soybean (Glycine max (L.) Merr.) cropping system in fertile Mollisols in Northeast China. However, it is necessary to understand how reducing nitrogen (N) fertiliser application may affect plant N acquisition and remobilisation, which is associated with photosynthetic carbon (C) assimilation and seed yield. The aim of this study was to investigate the origin of plant N (i.e. derived from N2 fixation, fertiliser or soil) under two different levels of N application, and the subsequent influence on C assimilation. A pot experiment was conducted with soybean grown in a Mollisol supplied with 5 mg N kg–1 soil (N5) or 100 mg N kg–1 soil (N100). Nitrogen was applied as 19.83% of 15N atom-excess in urea before sowing, and 13CO2 labelling was performed at the R5 (initial seed-filling) stage. Plants were harvested at R5 and full maturity stages to determine the 15N and 13C abundance in plant tissues. Seed yield and N content were not affected by different N rates. Symbiotically fixed N accounted for 64% of seed N in treatment N5, whereas fertiliser-derived N dominated seed N in N100, resulting in 58% of seed N. The proportion of soil-derived N in shoot and seed showed no difference between the two N treatments. A similar trend was observed for whole-plant N. The enhanced N2 fixation in N5 significantly increased assimilation of N and C during the seed-filling period compared with N100. Nodule density (nodule number per unit root length) and amount of photosynthetically fixed 13C in roots in N5 were greater than in N100. These results indicate that a greater contribution of N2 fixation to N assimilation during the seed-filling period is likely to meet N demand for maintaining soybean yield when fertiliser N supply is reduced. Greater allocation of photosynthetic C to roots and enhanced nodulation would greatly contribute to the alteration of N acquisition pattern under such condition.
Additional keywords: dual-labelling, fertiliser use efficiency, nodule density, soybean yield.
References
Barker DW, Sawyer JE (2005) Nitrogen application to soybean at early reproductive development. Agronomy Journal 97, 615–619.| Nitrogen application to soybean at early reproductive development.Crossref | GoogleScholarGoogle Scholar |
Caliskan S, Ozkaya I, Caliskan ME, Arslan M (2008) The effects of nitrogen and iron fertilization on growth, yield and fertilizer use efficiency of soybean in a Mediterranean-type soil. Field Crops Research 108, 126–132.
| The effects of nitrogen and iron fertilization on growth, yield and fertilizer use efficiency of soybean in a Mediterranean-type soil.Crossref | GoogleScholarGoogle Scholar |
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. European Journal of Agronomy 10, 49–56.
| Biological nitrogen fixation by fababean, pea and chickpea, under field conditions, estimated by the 15N isotope dilution technique.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsVWrtb0%3D&md5=5d5c8a1ff29a2382df169b85655fc1e4CAS |
Chalk PM, Ladha JK (1999) Estimation of legume symbiotic dependence: an evaluation of techniques based on 15N dilution. Soil Biology & Biochemistry 31, 1901–1917.
| Estimation of legume symbiotic dependence: an evaluation of techniques based on 15N dilution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntVOitb8%3D&md5=abc706154884c40399dd37394c9d0620CAS |
Chen Y, Yu ZH, Wang JF, Zhang XY (2014) Allocation of photosynthetic carbon to nodules of soybean in three geographically different Mollisols. European Journal of Soil Biology 62, 60–65.
| Allocation of photosynthetic carbon to nodules of soybean in three geographically different Mollisols.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXosFartLk%3D&md5=fa7c7465ae7636d6b8efb358f8cc4ccdCAS |
Cornfield AH (1960) Ammonia released on treating soils with N-sodium hydroxide as a possible means of predicting the nitrogen-supplying power of soils. Nature 187, 260–261.
| Ammonia released on treating soils with N-sodium hydroxide as a possible means of predicting the nitrogen-supplying power of soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3cXhtlaltLs%3D&md5=9a0da4b80aa278586d3aa3c16cd93efaCAS |
Ding XL, Yuan YR, Liang Y, Li LJ, Han XZ (2014) Impact of long-term application of manure, crop residue, and mineral fertilizer on organic carbon pools and crop yields in a Mollisol. Journal of Soils and Sediments 14, 854–859.
| Impact of long-term application of manure, crop residue, and mineral fertilizer on organic carbon pools and crop yields in a Mollisol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1yksLY%3D&md5=c2b4c843803f50d48a6b7c6479a430f6CAS |
Egli DB, Bruening WP (2007) Accumulation of nitrogen and dry matter by soybean seeds with genetic differences in protein concentration. Crop Science 47, 359–366.
| Accumulation of nitrogen and dry matter by soybean seeds with genetic differences in protein concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsF2msrs%3D&md5=1f34abafc0e719cd47e6c63ad5d7294bCAS |
Egli DB, Leggett JE, Duncan WG (1978) Influence of N-stress on leaf senescence and N redistribution in soybeans. Agronomy Journal 70, 43–47.
| Influence of N-stress on leaf senescence and N redistribution in soybeans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXhs1yqtb4%3D&md5=3559d650eba60d7c0c560e2ac1445edbCAS |
Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Science 11, 929–931.
| Stage of development descriptions for soybeans, Glycine max (L.) Merrill.Crossref | GoogleScholarGoogle Scholar |
Gan YB, Stulen I, van Keulen H, Kuiper PJC (2003) Effect of N fertilizer top-dressing at various reproductive stages on growth, N2 fixation and yield of three soybean (Glycine max (L.) Merr.) genotypes. Field Crops Research 80, 147–155.
| Effect of N fertilizer top-dressing at various reproductive stages on growth, N2 fixation and yield of three soybean (Glycine max (L.) Merr.) genotypes.Crossref | GoogleScholarGoogle Scholar |
Griffiths RI, Manefield M, Ostle N, McNamara N, O’Donnell AG, Bailey MJ, Whiteley AS (2004) 13CO2 pulse labelling of plants in tandem with stable isotope probing: methodological considerations for examining microbial function in the rhizosphere. Journal of Microbiological Methods 58, 119–129.
| 13CO2 pulse labelling of plants in tandem with stable isotope probing: methodological considerations for examining microbial function in the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXks1Wrs7s%3D&md5=2aeb3941aa405e43fbd1fa0bfd7a445cCAS | 15177910PubMed |
Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KWT, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327, 1008–1010.
| Significant acidification in major Chinese croplands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVSjtbg%3D&md5=938a5630624090b83ac544120369429aCAS | 20150447PubMed |
Hacin JI, Bohlool BB, Singleton PW (1997) Partitioning of 14C-labelled photosynthate to developing nodules and roots of soybean (Glycine max). New Phytologist 137, 257–265.
| Partitioning of 14C-labelled photosynthate to developing nodules and roots of soybean (Glycine max).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvFagsL0%3D&md5=9e79f4dd974b404f945b5f4eb330d60bCAS |
Harper JE (1987) Nitrogen metabolism. In ‘Soybeans: improvement, production and uses’. (Ed. JR Wilcox) pp. 497–533. (American Society of Agronomy, Crop Science Society of America, Soil Science Society of America: Madison, WI, USA)
Jin J, Wang GH, Liu JD, Yu ZH, Liu XB, Herbert SJ (2013) The fate of soyabean photosynthetic carbon varies in Mollisols differing in organic carbon. European Journal of Soil Science 64, 500–507.
| The fate of soyabean photosynthetic carbon varies in Mollisols differing in organic carbon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFClsrjM&md5=9b36a06c36fbcd5ac5fb9f4141f7ebc0CAS |
Jin J, Tang CX, Robertson A, Franks AE, Armstrong R, Sale P (2014) Increased microbial activity contributes to phosphorus immobilization in the rhizosphere of wheat under elevated CO2. Soil Biology & Biochemistry 75, 292–299.
| Increased microbial activity contributes to phosphorus immobilization in the rhizosphere of wheat under elevated CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpslKrsL8%3D&md5=6230bb8706d0eda358de441b221c852aCAS |
Klute A (1986) Water retention: laboratory methods. In ‘Methods of soil analysis. Part I. Physical and mineralogical methods’. 2nd edn. pp. 635–662. (American Society of Agronomy: Madison, WI, USA)
Kumudini S, Hume DJ, Chu G (2002) Genetic improvement in short-season soybeans: II. Nitrogen accumulation, remobilization, and partitioning. Crop Science 42, 141–145.
| Genetic improvement in short-season soybeans: II. Nitrogen accumulation, remobilization, and partitioning.Crossref | GoogleScholarGoogle Scholar | 11756264PubMed |
Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. Journal of Experimental Botany 60, 2859–2876.
| Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFWjtLc%3D&md5=62050a51e7c4ed59ff08f6252db50a4cCAS |
Lindström K, Murwira M, Willems A, Altier N (2010) The biodiversity of beneficial microbe-host mutualism: the case of rhizobia. Research in Microbiology 161, 453–463.
| The biodiversity of beneficial microbe-host mutualism: the case of rhizobia.Crossref | GoogleScholarGoogle Scholar | 20685242PubMed |
Liu X, Zhang F (2011) Nitrogen fertilizer induced greenhouse gas emissions in China. Current Opinion in Environmental Sustainability 3, 407–413.
| Nitrogen fertilizer induced greenhouse gas emissions in China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXosVOqsrw%3D&md5=a0e816196b9aa796e70f95b1b51d48f4CAS |
Liu XB, Liu JD, Xing BS, Herbert SJ, Meng K, Han XZ, Zhang XY (2005) Effects of long-term continuous cropping, tillage, and fertilization on soil organic carbon and nitrogen of black soils in China. Communications in Soil Science and Plant Analysis 36, 1229–1239.
| Effects of long-term continuous cropping, tillage, and fertilization on soil organic carbon and nitrogen of black soils in China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlt1Oqu74%3D&md5=b179de48ef7571abcdc78e2a934a9a2dCAS |
Makino A, Osmond B (1991) Effects of nitrogen nutrition on nitrogen partitioning between chloroplasts and mitochondria in pea and wheat. Plant Physiology 96, 355–362.
| Effects of nitrogen nutrition on nitrogen partitioning between chloroplasts and mitochondria in pea and wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkslSmsrY%3D&md5=216ceecbbc03bde9551605a18253726aCAS | 16668193PubMed |
Mariotti A, Lancelot C, Billen G (1984) Natural isotopic composition of nitrogen as a tracer of origin for suspended organic-matter in the Scheldt estuary. Geochimica et Cosmochimica Acta 48, 549–555.
| Natural isotopic composition of nitrogen as a tracer of origin for suspended organic-matter in the Scheldt estuary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXhsF2rtLo%3D&md5=2d010c80fc2912feecb44e7ce0bebcd2CAS |
Martínez-Alcántara B, Quinones A, Legaz F, Primo-Millo E (2012) Nitrogen-use efficiency of young citrus trees as influenced by the timing of fertilizer application. Journal of Plant Nutrition and Soil Science 175, 282–292.
| Nitrogen-use efficiency of young citrus trees as influenced by the timing of fertilizer application.Crossref | GoogleScholarGoogle Scholar |
Mastrodomenico AT, Purcell LC (2012) Soybean nitrogen fixation and nitrogen remobilization during reproductive development. Crop Science 52, 1281–1289.
| Soybean nitrogen fixation and nitrogen remobilization during reproductive development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xns12jt7s%3D&md5=c4683e04f962f5fb41f31bde519cf39fCAS |
Mattos D, Graetz DA, Alva AK (2003) Biomass distribution and nitrogen-15 partitioning in citrus trees on a sandy entisol. Soil Science Society of America Journal 67, 555–563.
| Biomass distribution and nitrogen-15 partitioning in citrus trees on a sandy entisol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkslChsb4%3D&md5=6573e09fefbd4d096b7e067b10f24bd6CAS |
Meng F, Dungait JJ, Zhang X, He M, Guo Y, Wu W (2013) Investigation of photosynthate-C allocation 27 days after 13C-pulse labeling of Zea mays L. at different growth stages. Plant and Soil 373, 755–764.
| Investigation of photosynthate-C allocation 27 days after 13C-pulse labeling of Zea mays L. at different growth stages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFKntbvJ&md5=8501f4e0bc8a93077b755447b2c2cb5fCAS |
Nobuyasu H, Liu S, Adu-Gyamfi JJ, Mohapatra PK, Fujita K (2003) Variation in the export of 13C and 15N from soybean leaf: the effects of nitrogen application and sink removal. Plant and Soil 253, 331–339.
| Variation in the export of 13C and 15N from soybean leaf: the effects of nitrogen application and sink removal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsFKqsr8%3D&md5=4ccf38a7e0a09c91e8174dd9dbf275adCAS |
Qin J, Yang RQ, Jiang CX, Li WB, Li YH, Guan RX, Chang RZ, Qiu LJ (2010) Discovery and transmission of functional QTL in the pedigree of an elite soybean cultivar Suinong14. Plant Breeding 129, 235–242.
| Discovery and transmission of functional QTL in the pedigree of an elite soybean cultivar Suinong14.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXot1eru7g%3D&md5=45dd9fc23707b8618297b9174645c7d1CAS |
Ray JD, Heatherly LG, Fritschi FB (2006) Influence of large amounts of nitrogen on nonirrigated and irrigated soybean. Crop Science 46, 52–60.
| Influence of large amounts of nitrogen on nonirrigated and irrigated soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsFKjsL0%3D&md5=e68250adeec28f6352764dabeb3e5701CAS |
Rennie RJ, Dubetz S (1986) Nitrogen-15-determined nitrogen-fixation in field-grown chickpea, lentil, fababean, and field pea. Agronomy Journal 78, 654–660.
| Nitrogen-15-determined nitrogen-fixation in field-grown chickpea, lentil, fababean, and field pea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XltFCiu7s%3D&md5=5bcc4b355697b52cb761f59ca9911efbCAS |
Sage RF, Pearcy RW, Seemann JR (1987) The nitrogen use efficiency of C3 and C4 plants. 3. Leaf nitrogen effects on the activity of carboxylating enzymes in Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiology 85, 355–359.
| The nitrogen use efficiency of C3 and C4 plants. 3. Leaf nitrogen effects on the activity of carboxylating enzymes in Chenopodium album (L.) and Amaranthus retroflexus (L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXjsFOq&md5=e0fb41383ad1aacfcb8d48a8be2cfbe1CAS | 16665701PubMed |
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 Crops Research 108, 1–13.
| Nitrogen uptake, fixation and response to fertilizer N in soybeans: A review.Crossref | GoogleScholarGoogle 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. Agronomy Journal 101, 958–970.
| Growth and nitrogen fixation in high-yielding soybean: impact of nitrogen fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXps1Omtb8%3D&md5=6736421e249a9f3569db0bdaee4108d8CAS |
Schmitt MA, Lamb JA, Randall GW, Orf JH, Rehm GW (2001) In-season fertilizer nitrogen applications for soybean in Minnesota. Agronomy Journal 93, 983–988.
| In-season fertilizer nitrogen applications for soybean in Minnesota.Crossref | GoogleScholarGoogle Scholar |
Sinclair TR (2004) Improved carbon and nitrogen assimilation for increased yield. In ‘Soybeans: improvement, production and uses’. (Eds HR Boerma, JE Specht) pp. 537–568. (American Society of Agronomy: Madison, WI, USA)
Sinclair TR, de Wit CT (1975) Photosynthate and nitrogen requirements for seed production by various crops. Science 189, 565–567.
| Photosynthate and nitrogen requirements for seed production by various crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXltlSmurk%3D&md5=c3a87b648ede333c4b92cada64c71dcfCAS | 17798304PubMed |
Spreitzer RJ, Salvucci ME (2002) Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annual Review of Plant Biology 53, 449–475.
| Rubisco: structure, regulatory interactions, and possibilities for a better enzyme.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVWhurk%3D&md5=830ef7c4741011f9f7a53db0a9041b7bCAS | 12221984PubMed |
Steel RG, Torrie JH (1980) ‘Principles and procedures of statistics: A biometrical approach.’ (MacGraw-Hill: New York)
Streeter J (1988) Inhibition of legume nodule formation and N2 fixation by nitrate. Critical Reviews in Plant Sciences 7, 1–23.
| Inhibition of legume nodule formation and N2 fixation by nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXnt1CgtQ%3D%3D&md5=37ace1bd09c65f524e89c56d82f10b37CAS |
Swinnen J, Vanveen JA, Merckx R (1994) Rhizosphere carbon fluxes in field-grown spring wheat: Model-calculations based on 14C partitioning after pulse-labeling. Soil Biology & Biochemistry 26, 171–182.
| Rhizosphere carbon fluxes in field-grown spring wheat: Model-calculations based on 14C partitioning after pulse-labeling.Crossref | GoogleScholarGoogle Scholar |
Thies JE, Singleton PW, Benbohlool B (1991) Influence of the size of indigenous rhizobial populations on establishment and symbiotic performance of introduced rhizobia on field-grown legumes. Applied and Environmental Microbiology 57, 19–28.
Thies JE, Singleton PW, Bohlool BB (1995) Phenology, growth, and yield of field-grown soybean and bush bean as a function of varying modes of N nutrition. Soil Biology & Biochemistry 27, 575–583.
| Phenology, growth, and yield of field-grown soybean and bush bean as a function of varying modes of N nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlt12rtro%3D&md5=c65ece2861e7ac1fdbb9fc4946e447e5CAS |
Unkovich M (2013) Isotope discrimination provides new insight into biological nitrogen fixation. New Phytologist 198, 643–646.
| Isotope discrimination provides new insight into biological nitrogen fixation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvVyku7o%3D&md5=1648199e72bd8edc7c4af9b2f2cb3e43CAS | 23461709PubMed |
van Kessel C, Hartley C (2000) Agricultural management of grain legumes: has it led to an increase in nitrogen fixation? Field Crops Research 65, 165–181.
| Agricultural management of grain legumes: has it led to an increase in nitrogen fixation?Crossref | GoogleScholarGoogle Scholar |
Vitousek PM, Naylor R, Crews T, David MB, Drinkwater LE, Holland E, Johnes PJ, Katzenberger J, Martinelli LA, Matson PA, Nziguheba G, Ojima D, Palm CA, Robertson GP, Sanchez PA, Townsend AR, Zhang FS (2009) Nutrient imbalances in agricultural development. Science 324, 1519–1520.
| Nutrient imbalances in agricultural development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnvVKju7o%3D&md5=9c0f5d17160d2b1235ddefaea478c99dCAS | 19541981PubMed |
Werner RA, Brand WA (2001) Referencing strategies and techniques in stable isotope ratio analysis. Rapid Communications in Mass Spectrometry 15, 501–519.
| Referencing strategies and techniques in stable isotope ratio analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXivFOjsb4%3D&md5=95870e552630ac9e2ab693b28a7bdbe9CAS | 11268135PubMed |
Xin LJ, Li XB, Tan MH (2012) Temporal and regional variations of China’s fertilizer consumption by crops during 1998–2008. Journal of Geographical Sciences 22, 643–652.
| Temporal and regional variations of China’s fertilizer consumption by crops during 1998–2008.Crossref | GoogleScholarGoogle Scholar |
Yan J, Han XZ, Ji ZJ, Li Y, Wang ET, Xie ZH, Chen WF (2014) Abundance and diversity of soybean-nodulating rhizobia in black soil are impacted by land use and crop management. Applied and Environmental Microbiology 80, 5394–5402.
| Abundance and diversity of soybean-nodulating rhizobia in black soil are impacted by land use and crop management.Crossref | GoogleScholarGoogle Scholar | 24951780PubMed |
Zapata F, Danso SKA, Hardarson G, Fried M (1987) Time course of nitrogen-fixation in field-grown soybean using 15N methodology. Agronomy Journal 79, 172–176.
| Time course of nitrogen-fixation in field-grown soybean using 15N methodology.Crossref | GoogleScholarGoogle Scholar |
