Skip to main content
SpringerLink
Log in

Exogenous Proline Application Reduces Phytotoxic Effects of Selenium by Minimising Oxidative stress and Improves Growth in Bean (Phaseolus vulgaris L.) Seedlings

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Bean (Phaseolus vulgaris L.) seedlings were subjected to varying selenium levels (1, 2, 4, and 6 ppm) in a hydroponic culture. The germination reached 100% in 48 h in all Se levels except 6 ppm, where it took 72 h. The root and shoot growth was stimulated at 1 and 2 ppm Se levels that was commensurate with increase in chlorophyll content, leaf water content, and cellular respiration. At 4 and 6 ppm Se levels, the growth was inhibited appreciably, which was associated with increase in stress injury measured as damage to membranes and decrease in cellular respiration, chlorophyll, and leaf water content. The oxidative injury as elevation of lipid peroxidation was larger compared to hydrogen peroxide accompanied by reduced levels of enzymatic (superoxide dismutase, catalase, ascorbate peroxidase, and glutathione reductase) and non-enzymatic (ascorbic acid and glutathione) antioxidants. Proline content was significantly higher at 1 and 2 ppm Se but diminished considerably at 4 and 6 ppm levels concomitant with the reduced growth. Exogenous application of proline (50 µM) resulted in substantiation of its endogenous levels that antagonised the toxic effects of Se by improving the growth of seedlings. The stress injury was reduced significantly with simultaneous increase in enzymatic and non-enzymatic antioxidants. Especially the components of ascorbate–glutathione cycle showed larger stimulation with proline application. The role of proline in mitigating the toxic effects of Se is discussed.

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

Similar content being viewed by others

References

  1. Germ M, Stilbilj V, Kreft I (2007) Metabolic importance of selenium for plants. Eur J Plant Sci Biotechnol 1:91–97

    Google Scholar 

  2. Zhang L, Ackley AR, Pilon-Smits EAH (2007) Varaiation in selenium tolerance and accumulation among 19 Arabidopsis thaliana accessions. J Plant Physiol 164:327–336

    Article  PubMed  CAS  Google Scholar 

  3. Lyons GH, Genc Y, Soole K, Stangoulis JCR, Liu F, Graham RD (2009) Selenium increases seed production in Brassica. Plant Soil 318:73–80

    Article  CAS  Google Scholar 

  4. Harrtikainen H, Xue T, Piironen V (2000) Selenium as an antioxidant and pro- oxidant in ryegrass. Plant Soil 225:193–200

    Article  Google Scholar 

  5. Yokota A, Shigeoka S, Onishi T, Kitaoka S (1998) Selenium as inducer of glutathione peroxidase in low-CO2 grown Chlamydomonas reinharditii. Plant Physiol 86:649–651

    Article  Google Scholar 

  6. Xue TL, Hartikainen H, Piironen V (2001) Antioxidative and growth-promoting effects of selenium on senescing lettuce. Plant Soil 237:55–61

    Article  CAS  Google Scholar 

  7. Djanaguiraman M, Devi DD, Shanker AK, Sheeba JA, Bangarusamy U (2005) Selenium—an antioxidative protectant in soybean during senescence. Plant Soil 272:77–86

    Article  CAS  Google Scholar 

  8. Shardendu Salhani N, Boulyga SF, Stengel E (2003) Phytoremediation of selenium by two helophyte species in subsurface flow constructed wetland. Chemosphere 50:967–973

    Article  Google Scholar 

  9. Dhillon KS, Dhillon SK (2003) Distribution and management of seleniferous soils. Adv Agron 79:119–184

    Article  CAS  Google Scholar 

  10. Padmaja K, Prasad DD, Prasad ARK (1989) Effect of selenium on chlorophyll biosynthesis in mung bean seedlings. Phytochem 28:3321–3324

    Article  CAS  Google Scholar 

  11. Terry N, Zayed AM, deSouza MP, Tarun A (2000) Selenium in higher plants. Ann Rev Plant Physiol Mol Biol 51:401–432

    Article  CAS  Google Scholar 

  12. Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726

    Article  PubMed  CAS  Google Scholar 

  13. Xu J, Yin H, Li X (2009) Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep 28:325–333

    Article  PubMed  CAS  Google Scholar 

  14. Kavi Kishore PB, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438

    Google Scholar 

  15. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  16. Srinivas V, Balasubramanian D (1995) Proline is a protein-compatible hydrotrope. Langmuir 11:2830–2833

    Article  CAS  Google Scholar 

  17. Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553

    Article  CAS  Google Scholar 

  18. Siripornadulsil S, Traina S, Verma DP, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847

    Article  PubMed  CAS  Google Scholar 

  19. El-Enany AE, Issa AA (2001) Proline alleviates heavy metal stress in Scenedesmus armatus. Folia Microbiol 46:227–230

    Article  CAS  Google Scholar 

  20. Kaul S, Sharma S, Mehta IK (2008) Free radical scavenging potential of L-proline: evidence from in vitro assays. Amino Acids 34:315–320

    Article  PubMed  CAS  Google Scholar 

  21. Islam M, Hoque MA, Okuma E, Banu MNA, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 165:1587–1597

    Article  Google Scholar 

  22. Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398

    Article  CAS  Google Scholar 

  23. Arnon D (1949) Copper enzymes in isolated chloroplasts; polyphenol oxidases in Beta vulgaris. Plant Physiol 24:1–15

    Article  PubMed  CAS  Google Scholar 

  24. Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity techniques for estimating water deficits in leaves. Aust J Biol Sci 15:413–428

    Google Scholar 

  25. Nayyar H, Bains T, Kumar S (2005) Low temperature induced floral abortion in chickpea: relationship to abscisic acid and cryoprotectants in reproductive organs. Environ Exp Bot 53:39–48

    Article  CAS  Google Scholar 

  26. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stochiometery of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  PubMed  CAS  Google Scholar 

  27. Teranishi Y, Tanaka A, Osumi M, Fukui S (1974) Catalase activity of hydrocarbon utilising Candida yeast. Agric Biol Chem 38:1213–1216

    CAS  Google Scholar 

  28. Nayyar H, Kaushal SK (2002) Chilling induced oxidative stress in germinating wheat grains as affected by water stress and calcium. Biol Plant 45:601–604

    Article  CAS  Google Scholar 

  29. Giannopolities CN, Ries SK (1977) Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  Google Scholar 

  30. Change B, Maehly AC (1955) Assay of catalases and peroxidase. Meth Enzymol 2:764–775

    Article  Google Scholar 

  31. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  32. Mukherjee SP, Choudhuri MA (1983) Implications of water stress induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plant 58:166–170

    Article  CAS  Google Scholar 

  33. Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  Google Scholar 

  34. Griffth OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2 vinyl pyridine. Anal Biochem 106:207–212

    Article  Google Scholar 

  35. Bates LS, Woldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–208

    Article  CAS  Google Scholar 

  36. Turakainen M, Hartikainen H, Seppänen MM (2004) Effects of selenium treatments on potato (Solanum tuberosum L.) growth and concentrations of soluble sugars and starch. J Agric Food Chem 52:5378–5382

    Article  PubMed  CAS  Google Scholar 

  37. Yao X, Chu J, Wang G (2009) Effects of selenium on wheat seedlings under drought stress. Biol Trace Elem Res 130:283–290

    Article  PubMed  CAS  Google Scholar 

  38. Harrtikainen H, Xue T (1999) The promotive effect of selenium on plant growth as triggered by ultraviolet irradiation. J Environ Qual 28:1372–1375

    Article  Google Scholar 

  39. Pennanen A, Xue T, Hartikainen H (2002) Protective role of selenium in plant subjected to severe UV irradiation stress. J Appl Bot 76:66–76

    CAS  Google Scholar 

  40. Banuelos GS, Ajwa HA, Wu L, Xun G, Akohoue S, Zambrzuski S (1997) Selenium-induced growth reduction in Brassica land races considered for phytoremediation. Ecotoxicol Environ Saf 36:282–287

    Article  PubMed  CAS  Google Scholar 

  41. Wu L, Huang ZZ (1992) Selenium assimilation and nutrient element uptake in white clover and tall fescue under the influence of sulphate concentration and selenium tolerance of the plants. J Exp Bot 43:549–555

    Article  CAS  Google Scholar 

  42. Azevedo H, Gomes C, Pinto G, Santos C (2005) Cadmium effects in sunflower: membrane permeability and changes in catalase and peroxidase activity in leaves and calluses. J Plant Nut 28:2233–2241

    Article  CAS  Google Scholar 

  43. Chen TF, Zheng WJ, Wong YS, Yang F (2008) Selenium-induced changes in activities of antioxidant enzymes and content of photosynthetic pigments in Spirulina platensis. J Integr Plant Biol 50:40–48

    Article  PubMed  CAS  Google Scholar 

  44. Kostopoulou P, Barbayiannis N, Noitsakis B (2009) Water relations of yellow sweetclover under the synergy of drought and selenium addition. Plant Soil 330:1104–1109

    Google Scholar 

  45. Germ M, Oswald J (2005) Selenium treatment affected respiratory potential in Eruca sativa. Acta Agric Slov 85:329–335

    CAS  Google Scholar 

  46. Chu J, Yao X, Zhang Z (2010) Responses of wheat seedlings to exogenous selenium supply under cold stress. Biol Trace Elem Res. doi:10.1007/s12011-009-8542-3

  47. Markovska YK, Gorinova NI, Nedkovska MP, Miteva KM (2009) Cadmium-induced oxidative damage and antioxidant responses in Brassica juncea plants. Biol Plant 53:151–154

    Article  CAS  Google Scholar 

  48. Filek M, Keskinen R, Hartikainen H, Szarejko I, Janiak A, Miszalski Z, Golda A (2010) Effect of selenium on characteristics of rape chloroplasts modified by cadmium. J Plant Physiol 167:28–33

    Article  PubMed  CAS  Google Scholar 

  49. Shri M, Kumar S, Chakrabarty D, Trivedi PK, Mallick S, Misra P, Shukla D, Mishra S, Srivastava S, Tripathi RD, Tuli R (2009) Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Eco Environ Saf 72:1102–1110

    Article  CAS  Google Scholar 

  50. Cho UH, Seo NH (2005) Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 168:113–120

    Article  CAS  Google Scholar 

  51. Hawrylak-Nowak B (2009) Beneficial effects of exogenous selenium in cucumber seedlings subjected to salt stress. Biol Trace Elem Res 132:265–269

    Article  Google Scholar 

  52. Trovato M, Mattioli R, Costantino P (2008) Multiple roles of proline in plant stress tolerance and development. Rendiconti Lincei 19:325–346

    Article  Google Scholar 

  53. Hermans C, Verbruggen N (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759

    Article  PubMed  Google Scholar 

  54. Sharma SS, Schat H, Vooijs R (1998) In vitro alleviation of heavy metal-induced enzyme inhibition by proline. Phytochemistry 49:1531–1535

    Article  PubMed  CAS  Google Scholar 

  55. Matysik J, Alia Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plant. Curr Sci 82:525–532

    CAS  Google Scholar 

  56. Webster BD, Leoplod AC (1977) The ultrastructure of dry and imbibed cotyledons of soybean. Am J Bot 64:1286

    Article  Google Scholar 

  57. Ozden M, Demirel U, Kahraman A (2009) Effects of proline on antioxidant system in leaves of grapevine (Vitis vinifera L.) exposed to oxidative stress by H2O2. Sci Hortic 119:163–168

    Article  CAS  Google Scholar 

  58. Huang Y, Bie Z, Liu Z, Ai Z, Wang W (2009) Protective role of proline against salt stress is partially related to the improvement of water status and peroxidase enzyme activity in cucumber. Soil Sci Plant Nutr 55:698–704

    Article  CAS  Google Scholar 

  59. Kaya C, Levent Tuna A, Ashraf M, Altunlu H (2007) Improved salt tolerance of melon (Cucumis melo L.) by the addition of proline and potassium nitrate. Environ Exp Bot 60:397–403

    Article  CAS  Google Scholar 

  60. Gadallah MAA (1999) Effect of proline and glycine betaine on Vicia faba responses to salt stress. Biol Plant 42:247–249

    Article  Google Scholar 

  61. Posmyk MM, Janas KM (2007) Effects of seed hydropriming in presence of exogenous proline on chilling injury limitation in Vigna radiata L. seedlings. Acta Physiol Plant 29:509–517

    Article  CAS  Google Scholar 

  62. Mehta SK, Gaur JP (1999) Heavy-metal-induced proline accumulation and its role in ameliorating metal toxicity in Chlorella vulgaris. New Phytol 143:253–259

    Article  CAS  Google Scholar 

  63. Hoque MA, Okuma E, Banu MN, Nakamura Y, Shimoishi Y, Murata Y (2007) Exogenous proline mitigates the detrimental effects of salt stress more than exogenous betaine by increasing antioxidant enzyme activities. J Plant Physiol 164:553–561

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany, Panjab University, Chandigarh, 160 014, India

    Mini Aggarwal, Suchi Sharma, Navneet Kaur, Dhirender Pathania, Kalpna Bhandhari, Neeru Kaushal, Ramanpreet Kaur, Kamaljit Singh & Harsh Nayyar

  2. Department of Chemistry, Panjab University, Chandigarh, 160 014, India

    Alok Srivastava

Authors
  1. Mini Aggarwal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Suchi Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Navneet Kaur
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dhirender Pathania
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kalpna Bhandhari
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Neeru Kaushal
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ramanpreet Kaur
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kamaljit Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Alok Srivastava
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Harsh Nayyar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Harsh Nayyar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aggarwal, M., Sharma, S., Kaur, N. et al. Exogenous Proline Application Reduces Phytotoxic Effects of Selenium by Minimising Oxidative stress and Improves Growth in Bean (Phaseolus vulgaris L.) Seedlings. Biol Trace Elem Res 140, 354–367 (2011). https://doi.org/10.1007/s12011-010-8699-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-010-8699-9

Keywords

Search

Navigation