Skip to main content
Log in

Salinity induced changes in proline and betaine contents and synthesis in two aquatic macrophytes differing in salt tolerance

  • Original Papers
  • Published:
Biologia Plantarum

Abstract

The present work investigated the effect of NaCl and seawater salinity (SWS) on accumulation of proline and glycinebetaine (betaine) and expression of two key enzymes of their biosynthetic pathway, betainealdehyde dehydrogenase (BADH) and Δ1-pyrroline-5-carboxylate synthetase (P5CS) in two aquatic macrophytes, salt-tolerant Najas gramenia and moderately-salt-tolerant Najas indica. N. gramenia did not show any accumulation of betaine or expression of BADH in response to NaCl or SWS treatments. The content of proline increased significantly in response to the salt treatments. High expression of P5CS was also observed, however, the transcript abundance did not correlate with the amount of proline. N. indica, exhibited significantly greater accumulation of proline in response to SWS, which contained Ca2+ in addition to NaCl, than in response to NaCl alone.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

BADH:

betainealdehyde dehydrogenase

P5CS:

Δ1-pyrroline-5-carboxylate synthetase

SWS:

seawater salinity

References

  • Aziz, A., Martin-Tanguy, J., Larher, F.: Salt stress-induced proline accumulation and changes in tyramine and polyamine levels are linked to ionic adjustment in tomato leaf discs.-Plant Sci. 145: 83–91, 1999.

    Article  CAS  Google Scholar 

  • Bates, L.S., Waldren, R.P., Teare, I.D.: Rapid determination of free proline for water-stress studies.-Plant Soil 39: 205–207, 1973.

    Article  CAS  Google Scholar 

  • Bliss, C.I.: Statistics in Biology. Vol. 1.-McGraw-Hill, New York 1967.

    Google Scholar 

  • Bugos, R.C., Chiang, V.L., Zhang, X.-H., Campbell, E.R., Podila, G.K., Campbell, W.H.: RNA isolation from plant tissues recalcitrant to extraction in guanidine.-BioTechniques 19: 734–737, 1995.

    PubMed  CAS  Google Scholar 

  • Chandra, A., Pathak, P.S., Bhatt, R.K., Dubey, A.: Variation in drought tolerance of different Stylosanthes accessions.-Biol. Plant. 48: 457–460, 2004.

    Article  Google Scholar 

  • Cherian, S., Reddy, M.P., Ferreira, R.B.: Transgenic plants with improved dehydration-stress tolerance: progress and future prospects.-Biol. Plant. 50: 481–495, 2006.

    Article  CAS  Google Scholar 

  • Colmer, T.D., Fan, T.W.-M., Higashi, R.M., Lauchi, A.: Interactive effects of Ca2+ and NaCl salinity on the ionic relations and proline accumulation in primary root tip of Sorghum bicolor.-Physiol. Plant. 97: 421–424, 1996.

    Article  CAS  Google Scholar 

  • Demir, Y., Ozturk, L.: Influence of ethephon and 2,5-norbornadiene on antioxidative enzymes and proline content in salt-stressed spinach leaves.-Biol. Plant. 47: 609–612, 2004.

    Article  Google Scholar 

  • Ding, L., Zhu, J.-K.: Reduced sodium uptake in the salt-hypersensitive sos1 mutant of Arabidopsis thaliana.-Plant Physiol. 113: 795–799, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Grieve, C.M., Grattan, S.R.: Rapid assay for determination of water soluble quaternary ammonium compounds.-Plant Soil 70: 303–307, 1983.

    Article  CAS  Google Scholar 

  • Hare, P.D., Cress, W.A.: Metabolic implications of stress-induced proline accumulation in plants.-Plant Growth Regul. 21: 79–102, 1997.

    Article  CAS  Google Scholar 

  • Hien, D.T., Jacobs, M., Angenon, G., Hermans, C., Thu, R.T., Son, L.V., Roosens, N.H.: Proline accumulation and Δ1-pyrroline-5-carboxylate synthetase gene properties in three rice cultivars differing in salinity and drought tolerance.-Plant Sci. 165: 1059–1068, 2003.

    Article  CAS  Google Scholar 

  • Igarashi, Y., Yoshiba, Y., Sanada, Y., Yamaguchi-Shinozaki, K., Wada, K., Shinozaki, K.: Characterization of the gene for Δ1-pyrroline-5-carboxylate synthetase and correlation between the expression of the gene and salt tolerance in Oryza sativa L.-Plant mol. Biol. 33: 857–865, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Ishitani, M., Arakawa, K., Mizuno, K., Kishitani, S., Takabe, T.: Betaine aldehyde dehydrogenase in the gramineae: levels in leaves of both betaine-accumulating and non-accumulating cereal plants.-Plant Cell Physiol. 34: 493–495, 1993.

    CAS  Google Scholar 

  • Jiménez-Bremont, J.F., Becerra-Flora, A., Hernández-Lucero, E., Rodríguez-Kessler, M., Acosta-Gallegos, J.A., Ramírez-Pimentel, J.G.: Proline accumulation in two bean cultivars under salt stress and the effect of polyamines and ornithine.-Biol. Plant. 50: 763–766, 2006.

    Article  Google Scholar 

  • Kardpal, R.P., Rao, N.A.: Alteration in the biosynthesis of proteins and nucleic acids in linger millet (Eleucine carocana) seedlings during water stress and effect of proline on protein biosynthesis.-Plant Sci. 40: 73–79, 1985.

    Article  Google Scholar 

  • Khan, M.A., Ungar, I.A., Showalter, A.M., Dewald, H.D.: NaCl-induced accumulation of glycinebetaine in four subtropical halophytes from Pakistan.-Physiol. Plant. 102: 487–492, 1998.

    Article  CAS  Google Scholar 

  • Kishor, P.B.K., Hong, Z., Miao, G.-H., Hu, C.-A.A., Verma, D.P.S.: Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants.-Plant Physiol. 108: 1387–1394, 1995.

    PubMed  CAS  Google Scholar 

  • Kumar, S.G., Reddy, A.M., Sudhakar, C.: NaCl effects on proline metabolism in two high yielding genotypes of mulberry (Morus alba L.) with contrasting salt tolerance.-Plant Sci. 165: 1245–1251, 2003.

    Article  CAS  Google Scholar 

  • Lahaye, P.A., Epstein, E.: Salt toleration by plants: enhancement with calcium.-Science 166: 395–396, 1969.

    Article  CAS  PubMed  Google Scholar 

  • Liu, J., Zhu, J.-K.: Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis.-Plant Physiol. 114: 591–596, 1997.

    Article  PubMed  CAS  Google Scholar 

  • McCue, K.F., Hanson, A.D.: Effects of soil salinity on the expression of betaine aldehyde dehydrogenase in leaves: investigation of hydraulic, ionic and biochemical signals.-Aust. J. Plant Physiol. 19: 555–564, 1992.

    Article  CAS  Google Scholar 

  • McNeil, S.D., Nuccio, M.L., Hanson, A.D.: Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance.-Plant Physiol. 120: 945–949, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Niknam, V., Bagherzadeh, M., Ebrahimzadeh, H., Sokhansanj, A.: Effect of NaCl on biomass and contents of sugars, proline and proteins in seedlings and leaf explants of Nicotiana tabacum grown in vitro.-Biol. Plant. 48: 613–615, 2004.

    Article  CAS  Google Scholar 

  • Paleg, L.G., Stewart, G.R., Bredbeer, J.W.: Proline and glycinebetaine influence protein salvation.-Plant Physiol. 75: 974–978, 1984.

    Article  PubMed  CAS  Google Scholar 

  • Parsons, T.R., Maita, Y., Lalli, C.M.: A Manual of Chemical and Biological Methods for Seawater Analysis. 1st Ed.-Pergamon Press, Oxford 1984.

    Google Scholar 

  • Patnaik, J.K., Debata, B.K.: In vitro selection of NaCl tolerant callus lines of Cymbopogan martini (Roxb.) Wats.-Plant Sci. 124: 203–210, 1997.

    Article  CAS  Google Scholar 

  • Petrusa, L.M., Winicov, I.: Proline status in salt-tolerant and salt-sensitive alfalfa cell lines and plants in response to NaCl.-Plant Physiol. Biochem. 35: 303–310, 1997.

    CAS  Google Scholar 

  • Roger, S.O., Bendich, A.J.: Extraction of DNA from plant tissues.-In: Gelvin, S.B., Schilperoot, R.A. (ed.): Plant Molecular Biology Manual A6. Pp. 1–10. Kluwer AcademicPublishers, Dordrecht 1988.

    Google Scholar 

  • Rout, N.P., Shaw, B.P.: Salinity tolerance in aquatic macrophytes: probable role of proline, the enzymes involved in its synthesis and C4 type of metabolism.-Plant Sci. 136: 121–130, 1998.

    Article  CAS  Google Scholar 

  • Rout, N.P., Shaw, B.P.: Salt tolerance in aquatic macrophytes: ionic relation and interaction.-Biol. Plant. 44: 95–99, 2001a.

    Article  CAS  Google Scholar 

  • Rout, N.P., Shaw, B.P.: Salt tolerance in aquatic macrophytes: possible involvement of the antioxidative enzymes.-Plant Sci. 160: 415–423, 2001b.

    Article  PubMed  CAS  Google Scholar 

  • Rout, N.P., Tripathi, S.B., Shaw, B.P.: Effect of salinity on chlorophyll and proline contents in three aquatic macrophytes.-Biol. Plant. 40: 453–458, 1998.

    Article  Google Scholar 

  • Savouré, A., Jaoua, S., Hua, X.J., Ardiles, W., Van Montagu, M., Verbruggen, N.: Isolation, characterization, and chromosomal location of a gene encoding the Δ1-pyrroline-5-carboxylate synthetase in Arabidopsis thaliana.-FEBS Lett. 372: 13–19, 1995.

    Article  PubMed  Google Scholar 

  • Wood, A.J., Saneoka, H., Rhodes, D., Joly, R.J., Goldsbrough, P.B.: Betain aldehyde dehydrogenase in Sorghum.-Plant Physiol. 110: 1301–1308, 1996.

    Article  PubMed  CAS  Google Scholar 

  • Yoshiba, Y., Kiyosue, T., Katagiri, T., Ueda, H., Mizoguchi, T., Yamaguchi-Shinozaki, K., Wada, K., Harada, Y., Shinozaki, K.: Correlation between the induction of a gene for Δ1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress.-Plant J. 7: 751–760, 1995.

    Article  PubMed  CAS  Google Scholar 

  • Yoshiba, Y., Kiyosue, T., Shinozaki, K.Y., Shinozaki, K.: Regulation of levels of proline as an osmolyte in plants under water stress.-Plant Cell Physiol. 38: 1095–1102, 1997.

    PubMed  CAS  Google Scholar 

  • Zhang, C-S., Lu, Q., Verma, D.P.S.: Characterization of Δ1-pyrroline-5-carboxylate synthetase gene promoter in transgenic Arabidopsis thaliana subjected to water stress.-Plant Sci. 129: 81–89, 1997.

    Article  CAS  Google Scholar 

  • Zhao, Y., Aspinall, D., Paleg, L.G.: Protection of membrane integrity in Medicago sativa L. by glycine betaine against the effects of freezing.-J. Plant Physiol. 140: 541–543, 1992.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to B. P. Shaw.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tripathi, S.B., Gurumurthi, K., Panigrahi, A.K. et al. Salinity induced changes in proline and betaine contents and synthesis in two aquatic macrophytes differing in salt tolerance. Biol Plant 51, 110–115 (2007). https://doi.org/10.1007/s10535-007-0022-z

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-007-0022-z

Additional key words

Navigation