Skip to main content

Advertisement

SpringerLink
Log in

Proline accumulation has prevalence over polyamines in nodules of Medicago sativa in symbiosis with Sinorhizobium meliloti during the initial response to salinity

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

Abstract

Background and aims

Polyamines are cationic molecules that play an important role in the plant response to environmental stresses. The aim of this work is to determine the role of these compounds in the response to salinity of Medicago sativa plants in symbiosis with the soil bacteria Sinorhizobium meliloti.

Methods

M. sativa plants inoculated with S. meliloti were subjected to 100 and 150 mM NaCl treatments. The concentration of nodular polyamines was determined in relation to the nitrogen fixation parameters, proline accumulation, and oxidative damage. In addition, polyamines concentrations were analyzed in different nodular fractions as well as the effect of exogenous polyamines in the nodulation response.

Results

The concentration of nodular polyamines decreased by the salinity in correlation with the nitrogenase activity after 2 and 4 weeks of salt treatment while spermine accumulated after 6 weeks. On the contrary, proline accumulation was induced by the salinity at all time points. The analysis of different nodular fractions showed the highest polyamines concentration in bacteroids being homospermidine the most abundant.

Conclusion

Proline accumulation had prevalence over polyamines at the earliest response to salinity probably due to nitrogen limitation under salt stress conditions and the existence of a common precursor for both compounds in the nodule. Nevertheless, after long salt exposure, spermine was also accumulated. The analysis of different nodular fractions indicated the bacteroidal origin of polyamines in nodules being homoespermidine, one of the most abundant.

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

Similar content being viewed by others

Abbreviations

PAs:

Polyamines

Put:

Putrescine

Sdp:

Spermidine

Spm:

Spermine

Homspd:

Homospermidine

Pro:

Proline

DAO:

Diamine oxidase

PAO:

Polyamine oxidase

MDA:

Malondialdehyde

References

  • Alcazar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    Article  CAS  PubMed  Google Scholar 

  • An Z, Jing W, Liu Y, Zhang W (2008) Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J Exp Bot 59:815–825

    Article  CAS  PubMed  Google Scholar 

  • Aziz A, Martin-Tanguy J, Larher F (1998) Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. Physiol Plant 104:195–202

    Article  CAS  Google Scholar 

  • Bachrach U (2010) The early history of polyamine research. Plant Physiol Biochem 48:490–495

    Article  CAS  PubMed  Google Scholar 

  • Benavides MP, Aizencang G, Tomaro ML (1997) Polyamines in Helianthus annuus L. during germination under salt stress. J Plant Growth Regul 16:205–211

    Article  CAS  Google Scholar 

  • Beringer JE (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84:188–198

    Article  CAS  PubMed  Google Scholar 

  • Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125

    Article  CAS  Google Scholar 

  • Burris RH (1984) The fundamentals of nitrogen fixation. Am Sci 72:517–517

    Google Scholar 

  • Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11:80–88

    Article  CAS  PubMed  Google Scholar 

  • Cordovilla MD, Berrido SI, Ligero F, Lluch C (1999) Rhizobium strain effects on the growth and nitrogen assimilation in Pisum sativum and Vicia faba plant growth under salt stress. J Plant Physiol 154:127–131

    Article  Google Scholar 

  • Dalton DA, Joyner SL, Becana M, Iturbe-Ormaetxe I, Chatfield JM (1998) Antioxidant defenses in the peripheral cell layers of legume root nodules. Plant Physiol 116:37–43

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223

    Article  CAS  Google Scholar 

  • Flores HE, Galston AW (1982) Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiol 69:701–706

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fujihara S (2009) Biogenic amines in rhizobia and legume root nodules. Microbes Environ 24:1–13

    Article  PubMed  Google Scholar 

  • Fujihara S, Abe H, Minakawa Y, Akao S, Yoneyama T (1994) Polyamines in nodules from various plant–microbe symbiotic associations. Plant Cell Physiol 35:1127–1134

    CAS  Google Scholar 

  • Hernández-Lucero E, Ruiz O, Jimenez-Bremont JF (2008) Effect of salt stress on polyamine metabolism in two bean cultivars. Plant Stress 2:96–102

    Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Hu X, Zhang Y, Shi Y, Zhang Z, Zou Z, Zhang H, Zhao J (2012) Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity–alkalinity mixed stress. Plant Physiol Biochem 57:200–209

    Article  CAS  PubMed  Google Scholar 

  • Jiménez-Bremont JF, Ruiz OA, Rodríguez-Kessler M (2007) Modulation of spermidine and spermine levels in maize seedlings subjected to long-term salt stress. Plant Physiol Biochem 45:812–821

    Article  PubMed  Google Scholar 

  • Khadri M, Tejera NA, Lluch C (2006) Alleviation of salt stress in common bean (Phaseolus vulgaris) by exogenous abscisic acid supply. J Plant Growth Regul 25:110–119

    Article  CAS  Google Scholar 

  • Lahiri K, Chattopadhyay S, Ghosh B (2004) Correlation of endogenous free polyamine levels with root nodule senescence in different genotypes in Vigna mungo L. J Plant Physiol 161:563–571

    Article  CAS  PubMed  Google Scholar 

  • Läuchli A (1984) Salt exclusion: an adaptation of legume for crops and pastures under saline conditions. In: Staples RC, Toenniessen GH (eds) Salinity tolerance in plants. Strategies for crop improvement. John Wiley and Sons, New York, pp 171–187

    Google Scholar 

  • Lefevre I, Gratia E, Lutts S (2001) Discrimination between the ionic and osmotic components of salt stress in relation to free polyamine level in rice (Oryza sativa). Plant Sci 161:943–952

    Article  CAS  Google Scholar 

  • Lopez M, Herrera-Cervera JA, Iribarne C, Tejera NA, Lluch C (2008) Growth and nitrogen fixation in Lotus japonicus and Medicago truncatula under NaCl stress: nodule carbon metabolism. J Plant Physiol 165:641–650

    Article  CAS  PubMed  Google Scholar 

  • Moschou PN, Paschalidis KA, Roubelakis-Angelakis KA (2008) Plant polyamine catabolism: the state of the art. Plant signal behavior 3:1061–1066

    Article  Google Scholar 

  • Pang X, Zhang Z, Wen X, Ban Y, Moriguchi T (2007) Polyamines, all-purpose players in response to environmental stresses in plants. Plant Stress 1:173–178

    Google Scholar 

  • Puppo A, Rigaud J (1975) Indole-3-acetic-acid (IAA) oxidation by leghemoglobin from soybean nodules. Physiol Plant 35:181–185

    Article  CAS  Google Scholar 

  • Quinet M, Ndayiragije A, Lefevre I, Lambillotte B, Dupont-Gillain CC, Lutts S (2010) Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. J Exp Bot 61:2719–2733

    Article  CAS  PubMed  Google Scholar 

  • Roy P, Niyogi K, SenGupta DN, Ghosh B (2005) Spermidine treatment to rice seedlings recovers salinity stress-induced damage of plasma membrane and PM-bound H+-ATPase in salt-tolerant and salt-sensitive rice cultivars. Plant Sci 168:583–591

    Article  CAS  Google Scholar 

  • Su GX, Bai X (2008) Contribution of putrescine degradation to proline accumulation in soybean leaves under salinity. Biol Plant 52:796–799

    Article  CAS  Google Scholar 

  • Tang W, Newton RJ (2005) Polyamines reduce salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine. Plant Growth Regul 46:31–43

    Article  CAS  Google Scholar 

  • Toumi I, Moschou PN, Paschalidis KA, Bouamama B, Ben Salem-Fnayou A, Ghorbel AW, Mliki A, Roubelakis-Angelakis KA (2010) Abscisic acid signals reorientation of polyamine metabolism to orchestrate stress responses via the polyamine exodus pathway in grapevine. J Plant Physiol 167:519–525

    Article  CAS  PubMed  Google Scholar 

  • Trinchant JC, Boscari A, Spermato G, Van de Sype G, Le Rudulier D (2004) Proline betaine accumulation and metabolism in alfalfa plants under sodium chloride stress. Exploring its compartmentalization in nodules. Plant Physiol 135:1583–1594

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Troll W, Lindsley J (1955) A photometric method for the determination of proline. J Biol Chem 215:655–660

    CAS  PubMed  Google Scholar 

  • Vassileva V, Ignatov G (1999) Polyamine-induced changes in symbiotic parameters of the Galega orientalis–Rhizobium galegae nitrogen-fixing system. Plant Soil 210:83–91

    Article  CAS  Google Scholar 

  • Vinod Kumar S, Sharma ML, Rajam MV (2006) Polyamine biosynthetic pathway as a novel target for potential applications in plant biotechnology. Physiol Mol Biol Plant 12:13–28

    Google Scholar 

  • Wisniewski JP, Brewin NJ (2000) Construction of transgenic pea lines with modified expression of diamine oxidase and modified nodulation responses with exogenous putrescine. Mol Plant Microbe Interact 13:922–928

    Article  CAS  PubMed  Google Scholar 

  • Witty JF, Minchin FR (1998) Hydrogen measurements provide direct evidence for a variable physical barrier to gas diffusion in legume nodules. J Exp Bot 49:1015–1020

    CAS  Google Scholar 

  • Xing SG, Jun YB, Hau ZW, Liang LY (2007) Higher accumulation of γ-aminobutyric acid induced by salt stress through stimulating the activity of diamine oxidases in Glycine max (L.) Merr. roots. Plant Physiol Biochem 45:560–566

    Article  CAS  PubMed  Google Scholar 

  • Xu Y, Shi GX, Ding CX, Xu XY (2011) Polyamine metabolism and physiological responses of Potamogeton crispus leaves under lead stress. Rus J Plant Physiol 58:460–466

    Article  CAS  Google Scholar 

  • Xue B, Zhang A, Jiang M (2009) Involvement of polyamine oxidase in abscisic acid-induced cytosolic antioxidant defense in leaves of maize. J Int Plant Biol 51:225–234

    Article  CAS  Google Scholar 

  • Yazici I, Tuerkan I, Sekmen AH, Demiral T (2007) Salinity tolerance of purslane (Portulaca oleracea L.) is achieved by enhanced antioxidative system, lower level of lipid peroxidation and proline accumulation. Environ Exp Bot 61:49–57

    Article  CAS  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 Central  PubMed  Google Scholar 

  • Zhao FG, Sun C, Liu YL (2001) Ornithine pathway in proline biosynthesis activated by salt stress in barley seedlings. A Bot Sin 43:36–40

    Google Scholar 

Download references

Acknowledgments

This work was supported by the Andalusian Research Program (AGR-139) and the Spanish Ministry of Science and Technology AGL2009-09223.

Author information

Authors and Affiliations

  1. Departamento de Fisiología Vegetal, Facultad de Ciencias, Universidad de Granada, Campus de Fuentenueva s/n, 18071, Granada, Spain

    Miguel López-Gómez, Javier Hidalgo-Castellanos, Carmen Iribarne & Carmen Lluch

Authors
  1. Miguel López-Gómez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Javier Hidalgo-Castellanos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carmen Iribarne
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carmen Lluch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Miguel López-Gómez.

Additional information

Responsible Editor: Euan K. James.

Rights and permissions

Reprints and permissions

About this article

Cite this article

López-Gómez, M., Hidalgo-Castellanos, J., Iribarne, C. et al. Proline accumulation has prevalence over polyamines in nodules of Medicago sativa in symbiosis with Sinorhizobium meliloti during the initial response to salinity. Plant Soil 374, 149–159 (2014). https://doi.org/10.1007/s11104-013-1871-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-013-1871-1

Keywords

Search

Navigation