Skip to main content

Advertisement

SpringerLink
Log in

Comparative effect of inorganic N on plant growth and N2 fixation of ten legume crops: towards a better understanding of the differential response among species

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

A better understanding of how plant growth, N nutrition and symbiotic nitrogen fixation (SNF) are influenced by soil inorganic N availability, for a wide range of legume species, is crucial to optimise legume productivity, N2 fixation, while limiting environmental risks such as N leaching.

Methods

A comparative analysis was performed for ten legume crops, grown in a field experiment and supplied with four N fertiliser rates. Dry matter, N concentration and SNF were measured. In parallel, root elongation rates were studied in a greenhouse experiment.

Results

For most species, N fertilisation had little effect on plant growth and N accumulation. SNF was reduced by soil inorganic N available at sowing but with large differences in the magnitude of the response among species. The response varied according to plant N requirements for growth and plant ability to retrieve inorganic N. Accordingly, root lateral expansion rate measured in RhizoTubes was highly correlated with plant ability to retrieve inorganic N measured in the field experiment.

Conclusion

Combining SNF response to soil inorganic N, shoot N and plant ability to retrieve inorganic N, allowed a robust evaluation of differential response to soil inorganic N among a wide range of legume species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

% Nc:

Critical shoot N concentration

% Ndfa:

Proportion of N derived from symbiotic fixation

% Ndf (soil + fertiliser):

Proportion of N derived from soil and fertiliser

DM:

Dry matter

Dpr:

Depth penetration rate

isoNUEf+s:

Curves of iso-inorganic N uptake efficiency from soil and fertiliser

Ler:

Lateral expansion rate

N50:

Amount of inorganic N available at sowing for which % Ndfa was reduced to 50%

Ndf (soil + fertiliser):

Amount of inorganic N from the soil and fertiliser retrieved by legumes over the growth cycle

NUEf:

N uptake efficiency of the fertiliser

NUEf+s:

N uptake efficiency of soil and fertiliser

SNF:

Symbiotic nitrogen fixation

References

  • Amarger N (1981) Selection of Rhizobium strains on their competitive ability for nodulation. Soil Biol. Biochem. 13:481–486

    Article  Google Scholar 

  • Benjamin JG, Nielsen DC (2006) Water deficit effects on root distribution of soybean, field pea and chickpea. Field Crop Res. 97:248–253

    Article  Google Scholar 

  • Bordeleau LM, Prévost D (1994) Nodulation and nitrogen fixation in extreme environments. Plant Soil 161:115–125

    Article  CAS  Google Scholar 

  • Cernay C, Pelzer E, Makowski D (2016) A global experimental dataset for assessing grain legume production. Sci Data 3:160084

    Article  CAS  Google Scholar 

  • Chalifour FP, Nelson LM (1988) Effects of time of nitrate application on nitrate reductase activity, nitrate uptake, and symbiotic dinitrogen fixation in faba bean and pea. Can J Bot-Rev Can Bot 66:1646–1652

    Article  CAS  Google Scholar 

  • Chaudhary MI, Adu-Gyamfi JJ, Saneoka H, Nguyen NT, Suwa R, Kanai S, El-Shemy HA, Lightfoot DA, Fujita K (2008) The effect of phosphorus deficiency on nutrient uptake, nitrogen fixation and photosynthetic rate in mashbean, mungbean and soybean. Acta Physiol. Plant. 30:537–544

    Article  CAS  Google Scholar 

  • Dayoub E, Naudin C, Piva G, Shirtliffe SJ, Fustec J, Corre-Hellou G (2017) Traits affecting early season nitrogen uptake in nine legume species. Heliyon 3:e00244

    Article  Google Scholar 

  • Devienne-Barret F, Justes E, Machet JM, Mary B (2000) Integrated control of nitrate uptake by crop growth rate and soil nitrate availability under field conditions. Ann. Bot. 86:995–1005

    Article  CAS  Google Scholar 

  • Dunbabin V, Diggle A, Rengel Z (2003) Is there an optimal root architecture for nitrate capture in leaching environments? Plant Cell Environ. 26:835–844

    Article  Google Scholar 

  • Evans J, O'Connor GE, Turner GL, Bergersen FJ (1987) Influence of mineral nitrogen on nitrogen fixation by lupin (Lupinus angustifolius) as assessed by 15N isotope dilution methods. Field Crop Res. 17:109–120

    Article  Google Scholar 

  • Fageria NK, Melo LC, Carvalho MCS (2015) Influence of nitrogen on growth, yield, and yield components and nitrogen uptake and use efficiency in dry bean genotypes. Commun. Soil Sci. Plant Anal. 46:2395–2410

    Article  CAS  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

    Article  Google Scholar 

  • Garnett T, Conn V, Kaiser BN (2009) Root based approaches to improving nitrogen use efficiency in plants. Plant Cell Environ. 32:1272–1283

    Article  CAS  Google Scholar 

  • George T, Singleton PW (1992) Nitrogen assimilation traits and dinitrogen fixation in soybean and common bean. Agron. J. 84:020–1028

    Article  Google Scholar 

  • Hartwig UA (1998) The regulation of symbiotic N2 fixation: a conceptual model of N feedback from the ecosystem to the gene expression level. Perspect Plant Ecol Evol Syst 1:92–120

    Article  Google Scholar 

  • Hauggaard-Nielsen H, Ambus P, Jensen ES (2001) Temporal and spatial distribution of roots and competition for nitrogen in pea-barley intercrops–a field study employing 32P technique. Plant Soil 236:63–74

    Article  CAS  Google Scholar 

  • Hauggaard-Nielsen H, Gooding M, Ambus P, Corre-Hellou G, Crozat Y, Dahlmann C, Dibet A, Von Fragstein P, Pristeri A, Monti M (2009) Pea–barley intercropping for efficient symbiotic N2-fixation, soil N acquisition and use of other nutrients in European organic cropping systems. Field Crop Res. 113:64–71

    Article  Google Scholar 

  • Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18

    Article  CAS  Google Scholar 

  • IUSS Working Group WRB (2006). World reference base for soil resources 2006, world soil resources reports no. 103. FAO, Rome. 132p

  • Jensen ES (1986) The influence of rate and time of nitrate supply on nitrogen fixation and yield in pea (Pisum sativum L.). Fertil Res 10:193–202

    Article  Google Scholar 

  • Jensen ES (1997). The role of grain legume N2 fixation in the nitrogen cycling of temperate cropping systems. D. Sc. Thesis. Risoe national laboratory

  • Jeudy C, Adrian M, Baussard C, Bernard C, Bernaud E, Bourion V, Busset H, Cabrera-Bosquet L, Cointault F, Han S (2016) RhizoTubes as a new tool for high throughput imaging of plant root development and architecture: test, comparison with pot grown plants and validation. Plant Methods 12:31

    Article  Google Scholar 

  • Jeuffroy MH, Warembourg FR (1991) Carbon transfer and partitioning between vegetative and reproductive organs in Pisum sativum L. Plant Physiol. 97:440–448

    Article  CAS  Google Scholar 

  • Ju C, Buresh RJ, Wang Z, Zhang H, Liu L, Yang J, Zhang J (2015) Root and shoot traits for rice varieties with higher grain yield and higher nitrogen use efficiency at lower nitrogen rates application. Field Crop Res. 175:47–55

    Article  Google Scholar 

  • Justes E, Mary B, Meynard JM, Machet JM, Thelier-Huché L (1994) Determination of a critical nitrogen dilution curve for winter wheat crops. Ann. Bot. 74:397–407

    Article  CAS  Google Scholar 

  • Kingsley MT, Bohlool BB (1983) Characterization of Rhizobium sp. (Cicer arietinum L.) by immunofluorescence, immunodiffusion, and intrinsic antibiotic resistance. Can. J. Microbiol. 29:518–526

    Article  Google Scholar 

  • Lagacherie B, Hugot R, Amarger N (1977) Selection de souches de Rhizobium japonicum d'après leur competitivite pour l'infection. Ann Agron 28:379–389

    Google Scholar 

  • Laguerre G, Geniaux E, Mazurier SI, Casartelli RR, Amarger N (1993) Conformity and diversity among field isolates of Rhizobium leguminosarum bv. viciae, bv. trifolii, and bv. phaseoli revealed by DNA hybridization using chromosome and plasmid probes. Can. J. Microbiol. 39:412–419

    Article  CAS  Google Scholar 

  • Leidi E, Rodriguez-Navarro D (2000) Nitrogen and phosphorus availability limit N2 fixation in bean. New Phytol. 147:337–346

    Article  CAS  Google Scholar 

  • Lemaire G, Cruz P, Gosse G, Chartier M (1985) Etude des relations entre la dynamique de prélèvement d'azote et la dynamique de croissance en matière sèche d'un peuplement de luzerne (Medicago sativa L.). Agronomie 5:685–692

    Article  Google Scholar 

  • Lemaire G, Jeuffroy MH, Gastal F (2008) Diagnosis tool for plant and crop N status in vegetative stage: Theory and practices for crop N management. Eur. J. Agron. 28:614–624

    Article  CAS  Google Scholar 

  • Liu L, Gan Y, Bueckert R, Van Rees K (2011a) Rooting systems of oilseed and pulse crops. II: vertical distribution patterns across the soil profile. Field Crop Res. 122:248–255

    Article  Google Scholar 

  • Liu Y, Wu L, Baddeley JA, Watson CA (2011b) Models of biological nitrogen fixation of legumes. A review. Agron. Sustain. Dev. 31:155–172

    Article  Google Scholar 

  • López-Bellido L, López-Bellido RJ, Castillo J, López-Bellido FJ (2004) Chickpea response to tillage and soil residual nitrogen in a continuous rotation with wheat. I Biomass Seed Yield Field Crop Res 88:191–200

    Article  Google Scholar 

  • Magrini MB, Anton M, Cholez C, Corre-Hellou G, Duc G, Jeuffroy MH, Meynard JM, Pelzer E, Voisin AS, Walrand S (2016) Why are grain-legumes rarely present in cropping systems despite their environmental and nutritional benefits? Analyzing lock-in in the French agrifood system. Ecol Econ 126:152–162

    Article  Google Scholar 

  • Materechera SA, Dexter AR, Alston AM (1991) Penetration of very strong soils by seedling roots of different plant species. Plant Soil 135:31–41

    Article  Google Scholar 

  • Materechera S, Alston A, Kirby J, Dexter A (1992) Influence of root diameter on the penetration of seminal roots into a compacted subsoil. Plant Soil 144:297–303

    Article  Google Scholar 

  • Matlab (2015). MATLAB and statistics toolbox release 2015a. The MathWorks, Inc., Natick, Massachusetts, United States

  • Mazurier SI (1989). Diversite de populations naturelles nodulantes de Rhizobium leguminosarum. These de doctorat. Université Claude Bernard Lyon 1, Lyon, France

  • Mi GH, Chen FJ, Wu QP, Lai NW, Yuan LX, Zhang FS (2010) Ideotype root architecture for efficient nitrogen acquisition by maize in intensive cropping systems. Sci. China Life Sci. 53:1369–1373

    Article  Google Scholar 

  • Moreau D, Voisin AS, Salon C, Munier-Jolain N (2008) The model symbiotic association between Medicago truncatula cv. Jemalong and rhizobium meliloti strain 2011 leads to N-stressed plants when symbiotic N2 fixation is the main N source for plant growth. J. Exp. Bot. 59:3509–3522

    Article  CAS  Google Scholar 

  • Muller B, Touraine B (1992) Inhibition of NO3 uptake by various phloem-translocated amino acids in soybean seedlings. J. Exp. Bot. 43:617–623

    Article  CAS  Google Scholar 

  • Naudin C, Corre-Hellou G, Pineau S, Crozat Y, Jeuffroy M-H (2010) The effect of various dynamics of N availability on winter pea–wheat intercrops: crop growth, N partitioning and symbiotic N2 fixation. Field Crop Res. 119:2–11

    Article  Google Scholar 

  • Naudin C, Corre-Hellou G, Voisin AS, Oury V, Salon C, Crozat Y, Jeuffroy MH (2011) Inhibition and recovery of symbiotic N2 fixation by peas (Pisum sativum L.) in response to short-term nitrate exposure. Plant Soil 346:275–287

    Article  CAS  Google Scholar 

  • Ney B, Doré T, and Sagan M (1997) The nitrogen requirements of major agricultural crops: Grain legumes. In: Lemaire G (ed) Diagnosis of the nitrogen status in crops. Springer-Verlag, Heigelberg, pp. 107–117

    Chapter  Google Scholar 

  • Pate JS, Layzell DB, Atkins CA (1979) Economy of carbon and nitrogen in a nodulated and nonnodulated (NO3-grown) legume. Plant Physiol. 64:1083–1088

    Article  CAS  Google Scholar 

  • Peoples MB, Turner GL, Shah Z, Shah SH, Aslam M, Ali S, Maskey SL, Bhattarai S, Afandi F, Schwenke GD (1997) Evaluation of the 15N natural abundance technique for measuring N2 fixation in experimental plots and farmers' fields. In: Rupela O, Johansen C, Herridge D (eds) Extending nitrogen fixation research to Farmers' fields. ICRISAT, India, pp 57–75

    Google Scholar 

  • Plaza-Bonilla D, Nolot JM, Raffaillac D, Justes E (2015) Cover crops mitigate nitrate leaching in cropping systems including grain legumes: field evidence and model simulations. Agric. Ecosyst. Environ. 212:1–12

    Article  CAS  Google Scholar 

  • Plénet D, and Cruz P (1997) Maize and sorghum. In: Lemaire G (ed) Diagnosis of the nitrogen status in crops. Springer-Verlag, Heigelberg, pp 93–106

    Chapter  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  Google Scholar 

  • RCore T (2014). R: a language and environment for statistical computing. R Foundation for statistical Computing, Vienna

  • Redden RJ, Herridge DF (1999) Evaluation of genotypes of navy and culinary bean (Phaseolus vulgaris L.) selected for superior growth and nitrogen fixation. Aust. J. Exp. Agric. 39:975–980

    Article  Google Scholar 

  • Reich PB (2014) The world-wide ‘fast–slow’plant economics spectrum: a traits manifesto. J. Ecol. 102:275–301

    Article  Google Scholar 

  • Rennie RJ, Rennie DA (1983) Techniques for quantifying N2 fixation in association with nonlegumes under field and greenhouse conditions. Can. J. Microbiol. 29:1022–1035

    Article  Google Scholar 

  • Salon C, Avice JC, Larmure A, Ourry A, Prudent M, and Voisin AS (2011) Plant N fluxes and modulation by nitrogen, heat and water stresses: a review based on comparison of legumes and non legume plants. In: Shanker A, Venkateswarlu B (ed) Abiotic stress in plants-mechanisms and adaptations. InTech, Rikeja, pp. 79–118

  • 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

    Article  Google Scholar 

  • Schwenke GD, Peoples MB, Turner GL, Herridge DF (1998) Does nitrogen fixation of commercial, dryland chickpea and faba bean crops in north-West New South Wales maintain or enhance soil nitrogen? Aust. J. Exp. Agric. 38:61–70

    Article  Google Scholar 

  • Sprent JI, Stephens JH, Rupela OP (1988) Environmental effects on nitrogen fixation. In: Sumerfield RJ (ed) World crops: cool season food legumes. Kluwer Academic publishers, Dordrecht, pp 801–810

    Chapter  Google Scholar 

  • Streeter JG (2003) Effects of drought on nitrogen fixation in soybean root nodules. Plant Cell Environ. 26:1199–1204

    Article  CAS  Google Scholar 

  • Sulieman S, Fischinger SA, Gresshoff PM, Schulze J (2010) Asparagine as a major factor in the N-feedback regulation of N2 fixation in Medicago truncatula. Physiol. Plant. 140:21–31

    Article  CAS  Google Scholar 

  • Turpin JE, Herridge DF, Robertson MJ (2002) Nitrogen fixation and soil nitrate interactions in field-grown chickpea (Cicer arietinum) and fababean (Vicia faba). Crop Pasture Sci 53:599–608

    Article  CAS  Google Scholar 

  • Unkovich MJ, Pate JS (2000) An appraisal of recent field measurements of symbiotic N2 fixation by annual legumes. Field Crop Res. 65:211–228

    Article  Google Scholar 

  • Vance CP, Heichel GH (1991) Carbon in N2 fixation: limitation or exquisite adaptation. Annu. Rev. Plant Biol. 42:373–390

    Article  CAS  Google Scholar 

  • Voisin AS, and Gastal F (2015) Nutrition azotée et fonctionnement agrophysologique spécifique des légumineuses. In: Editions Quæ (ed) Les légumineuses pour des systèmes agricoles et alimentaires durables (Schneider, A., Huyghe, C., coord.), Versailles, pp. 79–137

  • Voisin AS, Salon C, Munier-Jolain NG, Ney B (2002a) Effect of mineral nitrogen on nitrogen nutrition and biomass partitioning between the shoot and roots of pea (Pisum sativum L.). Plant Soil 242:251–262

    Article  CAS  Google Scholar 

  • Voisin AS, Salon C, Munier-Jolain NG, Ney B (2002b) Quantitative effects of soil nitrate, growth potential and phenology on symbiotic nitrogen fixation of pea (Pisum sativum L.). Plant Soil 243:31–42

    Article  CAS  Google Scholar 

  • Voisin AS, Salon C, Jeudy C, Warembourg FR (2003) Seasonal patterns of 13C partitioning between shoots and Nodulated roots of N2 or nitrate-fed Pisum sativum L. Ann. Bot. 91:539–546

    Article  CAS  Google Scholar 

  • Voisin AS, Munier-Jolain NG, Salon C (2010) The nodulation process is tightly adjusted to plant growth. An analysis using environmentally and genetically induced variation of nodule number and biomass in pea. Plant Soil 337:399–412

    Article  CAS  Google Scholar 

  • Zhu J, Ingram PA, Benfey PN, Elich T (2011) From lab to field, new approaches to phenotyping root system architecture. Curr. Opin. Plant Biol. 14:310–317

    Article  Google Scholar 

Download references

Acknowledgements

M. Guinet was granted by INRA and the Ministry in charge of Agriculture. This experimental work was supported by the ANR LEGITIMES, INRA Bourgogne-Franche-Comté Region (PSDR project ProSys), the European Community under the grant agreement n°FP7-613551 (LEGATO project), and Terres Inovia. We thank G. Adeux, F. Bizouard, M. Chanis, A. Coffin, M. Dourneau, C. Ducourtieux, S. Girodet, C. Jeudy, M Lefebvre, F. Lombard, P. Mathey, E. Pimet for their excellent technical assistance, M. Lamboeuf for his help in image analysis.

Author information

Authors and Affiliations

  1. Agroécologie, AgroSup Dijon, INRA, University Bourgogne Franche Comté, F-21000, Dijon, France

    Maé Guinet, Bernard Nicolardot, Cécile Revellin, Vincent Durey & Anne-Sophie Voisin

  2. Department of Biosystems and Technology, Swedish University of Agricultural Sciences, Alnarp, Sweden

    Georg Carlsson

Authors
  1. Maé Guinet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bernard Nicolardot
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cécile Revellin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vincent Durey
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Georg Carlsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anne-Sophie Voisin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anne-Sophie Voisin.

Additional information

Responsible Editor: Euan K. James

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guinet, M., Nicolardot, B., Revellin, C. et al. Comparative effect of inorganic N on plant growth and N2 fixation of ten legume crops: towards a better understanding of the differential response among species. Plant Soil 432, 207–227 (2018). https://doi.org/10.1007/s11104-018-3788-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-018-3788-1

Keywords

Search

Navigation