Skip to main content

How nitrogen fixation is modulated in response to different water availability levels and during recovery: A structural and functional study at the whole plant level

Abstract

Aims

The aims of this work were (1) to analyze concomitantly both structural and functional responses of pea plants subjected to decreasing water availability and (2) to evaluate their ability to recover after the drought period.

Methods

A pot experiment compared the growth and the nitrogen nutrition of pea plants exposed, during their vegetative stage, to seven water availability levels.

Results

Our results showed that the plant first reacted to water deprivation by maintaining root growth during drought and secondly to a nitrogen deficiency by allocating more carbon to the nodules responsible for nitrogen acquisition during recovery. The specific activity of nodules was negatively impacted by water stress during drought, fully recovered afterwards except after a severe water stress and the number of nodules initiated during recovery depended on the nitrogen nutritional index of the plant at the end of the drought period. This strategy allowed the plant to recover sufficiently and to maintain high values of yield components at harvest, except after a severe water stress, which reduced seed number.

Conclusion

Our findings revealed that water availability levels did not change plant strategy in response to drought but increased the responses observed.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Bacanamwo M, Harper JE (1997) The feedback mechanism of nitrate inhibition of nitrogenase activity in soybean may involve asparagine and/or products of its metabolism. Plant Physiol 100:371–377. doi:10.1111/j.1399-3054.1997.tb04795.x

    Article  CAS  Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. doi:10.1093/aob/mcn125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cure JD, Raper CD, Patterson RP, Robarge WP (1985) Dinitrogen fixation in soybean in response to leaf water stress and seed growth rate. Crop Sci 25:52–58. doi:10.2135/cropsci1985.0011183X002500010015x

    Article  CAS  PubMed  Google Scholar 

  • Doré T, Meynard JM, Sebillotte M (1998) The role of grain number, nitrogen nutrition and stem number in limiting pea crop (Pisum sativum L.) yields under agricultural conditions. Eur J Agron 8:29–37. doi:10.1016/S1161-0301(97)00006-3

    Article  Google Scholar 

  • Durand JL, Sheehy JE, Minchin FR (1987) Nitrogenase activity, photosynthesis and nodule water potential in soyabean plants experiencing water deprivation. J Exp Bot 38:311–321. doi:10.1093/jxb/38.2.311

    Article  CAS  Google Scholar 

  • Easterling WE, Aggarwal PK, Batima P, Brander KM, Erda L, Howden SM, Kirilenko A, Morton J, Soussana JF, Schmidhuber J, Tubiello FN (2007) Food, fibre and forest products. Climate change 2007: impacts, adaptation and vulnerability. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) Contribution of working group II to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 273–313

    Google Scholar 

  • Francisco PB, Akao S (1993) Autoregulation and nitrate inhibition of nitrate formation in soybean cv. Enrei and its nodulation mutants. J Exp Bot 44:547–553. doi:10.1093/jxb/44.3.547

    Article  CAS  Google Scholar 

  • Gonzàlez EM, Gordon AJ, James C, Arresse-Igor C (1995) The role of sucrose synthase in the response of soybean nodules to drought. J Exp Bot 46:1515–1523. doi:10.1093/jxb/46.10.1515

    Article  Google Scholar 

  • Guilioni L, Wéry J, Lecoeur J (2003) High temperature and water deficit may reduce seed number in field pea purely by decreasing plant growth rate. Funct Plant Biol 30:1151–1164. doi:10.1071/FP03105

    Article  Google Scholar 

  • Jensen ES, Hauggaard-Nielsen H (2003) How can increased use of biological N2 fixation in agriculture benefit the environment? Plant Soil 252:177–186. doi:10.1023/A:1024189029226

    Article  CAS  Google Scholar 

  • Jeudy C, Ruffel S, Freixes S, Tillard P, Santoni AL, Morel S, Journet EP, Duc G, Gojon A, Lepetit M, Salon C (2010) Adaptation of Medicago truncatula to nitrogen limitation is modulated via local and systemic nodule development responses. New Phytol 185:817–828. doi:10.1111/j.1469-8137.2009.03103.x

    Article  CAS  PubMed  Google Scholar 

  • Julkowska MM, Hoefsloot HCJ, Mol S, Feron R, de Boer GJ, Haring MA, Testerink C (2014) Capturing Arabidopsis root architecture dynamics with ROOT-FIT reveals diversity in responses to salinity. Plant Physiol 166:1387–1402. doi:10.1104/pp. 114.248963

    Article  PubMed  PubMed Central  Google Scholar 

  • King CA, Purcell LC (2001) Soybean nodule size and relationship to nitrogen fixation response to water deficit. Crop Sci 41:1099–1107. doi:10.2135/cropsci2001.4141099x

  • King CA, Purcell LC (2005) Inhibition of N2 fixation in soybean is associated with elevated ureides and amino acids. Plant Physiol 137:1389–1396. doi:10.1104/pp. 104.056317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kouchi H, Yoneyama T (1984) Dynamics of carbon photosynthetically assimilated in nodulated soyabean plants under steady-state conditions 2. The Incorporation of 13C into carbohydrates, organic acids, amino acids and some storage compounds. Ann Bot 53:883–896

    CAS  Google Scholar 

  • Lemaire G, van Oosterom E, Sheehy J, Jeuffroy MH, Massignam A, Rossato L (2007) Is crop N demand more closely related to dry matter accumulation or leaf area expansion during vegetative growth? Field Crops Res 100:91–106. doi:10.1016/j.fcr.2006.05.009

    Article  Google Scholar 

  • Mahieu S, Germon F, Aveline A, Hauggaard-Nielsen H, Ambus P, Jensen ES (2009) The influence of water stress on biomass and N accumulation, N partitioning between above and below ground parts and on N rhizodeposition during reproductive growth of pea (Pisum sativum L.). Soil Biol Biochem 41:380–387. doi:10.1016/j.soilbio.2008.11.021

    Article  CAS  Google Scholar 

  • Marino D, Gonzalez EM, Arrese-Igor C (2006) Drought effects on carbon and nitrogen metabolism of pea nodules can be mimicked by paraquat: evidence for the occurrence of two regulation pathways under oxidative stresses. J Exp Bot 57:665–673. doi:10.1093/jxb/erj056

    Article  CAS  PubMed  Google Scholar 

  • Mastrodomenico AT, Purcell LC, King CA (2013) The response and recovery of nitrogen fixation activity in soybean to water stress at different reproductive development stages. Environ Exp Bot 85:16–21. doi:10.1016/j.envexpbot.2012.07.006

    Article  CAS  Google Scholar 

  • Muller B, Pantin F, Génard M, Turc O, Freixes S, Piques M, Gibon Y (2011) Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J Exp Bot 62:1715–1729. doi:10.1093/jxb/erq438

    Article  CAS  PubMed  Google Scholar 

  • Nasr Esfahani M, Sulieman S, Schulze J, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2014) Mechanisms of physiological adjustment of N2 fixation in Cicer arietinum L. (chickpea) during early stages of water deficit: single or multi-factor controls. Plant J 79:964–980. doi:10.1111/tpj.12599

    Article  CAS  PubMed  Google Scholar 

  • Naudin C, Core-Hellou G, Voisin AS, Oury V, Salon C, Crozat Y, Jeuffroy MH (2011) Inhibition and recovery of N2-fixation by peas (Pisum stivum L.) in response to short-term nitrate exposure. Plant Soil 346:275–287. doi:10.1007/s11104-011-0817-8

    Article  CAS  Google Scholar 

  • Neo HH, Layzell DB (1997) Phloem glutamine and the regulation of O2 diffusion in legume nodules. Plant Physiol 113:259–267. doi:10.1104/pp. 113.1.259

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ney B, Duthion C, Turc O (1994) Phenological response of pea to water stress during reproductive development. Crop Sci 34:141–146. doi:10.2135/cropsci1994.0011183X003400010025x

    Article  Google Scholar 

  • Peña-Cabriales JJ, Castellanos JZ (1993) Effect of water stress on N2 fixation and grain yield of Phaseolus vulgaris L. Plant Soil 152:151–155. doi:10.1007/BF00016345

    Article  Google Scholar 

  • Peoples MB, Herridge DF, Ladha JK (1995) Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production? Plant Soil 174:3–28. doi:10.1007/BF00032239

    Article  CAS  Google Scholar 

  • R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Salon C, Avice JC, Larmure A, Ourry A, Prudent M, 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 Abiotic Stress in Plants: Mechanisms and Adaptations Eds. A Shanker and B Venkateswarlu. Intech. doi: 10.5772/23474

  • Schulze J, Adgo E, Schilling G (1994) The influence of N2-fixation on the carbon balance of leguminous plants. Experientia 50:906–912. doi:10.1007/BF01923477

    Article  CAS  Google Scholar 

  • Serraj R, Sinclair TR, Purcell LC (1999) Symbiotic N2 fixation response to drought. J Exp Bot 50:143–155. doi:10.1093/jxb/50.331.143

    CAS  Google Scholar 

  • Serraj R, Vadez V, Sinclair TR (2001) Feedback regulation of symbiotic N2 fixation under drought stress. Agronomie 21:621–626. doi:10.1051/agro:2001153

    Article  Google Scholar 

  • Sinclair TR, Zimet AR, Muchow RC (1988) Changes in soybean nodule number and dry weight in response to drought. Fields Crop Res 18:197–202

    Article  Google Scholar 

  • Streeter JG (2003) Effects of drought on nitrogen fixation in soybean root nodules. Plant Cell Environ 26:1199–1204. doi:10.1046/j.1365-3040.2003.01041.x

    Article  CAS  Google Scholar 

  • Tardieu F, Granier C, Muller B (2011) Water deficit and growth. Co-ordinating processes without an orchestrator? Curr Opin Plant Biol 14:283–289. doi:10.1016/j.pbi.2011.02.002

    Article  PubMed  Google Scholar 

  • Voisin AS, Prudent M, Duc G, Salon C (2015). Pea nodule gradients explain N nutrition and limited symbiotic fixation in hypernodulating mutants. Agron Sustain Dev in press. doi: 10.1007/s13593-015-0328-8

  • Voisin AS, Guéguen J, Huyghe C, Jeuffroy MH, Magrini MH, Meynard JM, Mougel C, Pellerin S, Pelzer E (2014) Legumes for feed, food, biomaterials and bioenergy in Europe: a review. Agron Sustain Dev 34:361–380. doi:10.1007/s13593-013-0189-y

    Article  CAS  Google Scholar 

  • Voisin AS, Munier-Jolain N, 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. doi:10.1007/s11104-010-0536-6

    Article  CAS  Google Scholar 

  • Voisin AS, Salon C, Jeudy C, Warembourg FR (2003) Symbiotic N2 fixation activity in relation to C economy of Pisum sativum L. as a function of plant phenology. J Exp Bot 54:2733–2744. doi:10.1093/jxb/erg290

    Article  CAS  PubMed  Google Scholar 

  • Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the greenhouse team for taking care of the plants, as well as Vincent Durey, Christian Jeudy, Lucie Lainé, Patrick Mathey, and Anne-Lise Santoni for their help during harvests. We thank Nathalie Munier-Jolain and Anne-Sophie Voisin for a critical reading of the manuscript and Richard Thompson for English revision of the manuscript. This work was jointly founded by Conseil Régional de Bourgogne, Institut National de la Recherche Agronomique (Project ACCAF-CAQ40) and European Commission (Project FP7-ARIMNet-MediLeg).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marion Prudent.

Additional information

Responsible Editor: Euan K. James.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 23 kb)

ESM 2

(DOCX 29 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Prudent, M., Vernoud, V., Girodet, S. et al. How nitrogen fixation is modulated in response to different water availability levels and during recovery: A structural and functional study at the whole plant level. Plant Soil 399, 1–12 (2016). https://doi.org/10.1007/s11104-015-2674-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-015-2674-3

Keywords

  • Pisum sativum L.
  • Water stress
  • Nodules
  • N2 fixation
  • Roots
  • Rewatering