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Exogenous proline modifies differential expression of superoxide dismutase genes in UV-B-irradiated Salvia officinalis plants

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Abstract

Grown in water culture 6-week-old Salvia officinalis plants with 4–5 true leaves were exposed to irradiation with UV-B (10 min, 12.3 kJ/m2), subjected to 5 mM exogenous proline in the nutrient solution, and treated with a combination of both factors. The plants responded to short UV-B irradiation by the appearance of oxidative stress, which was manifested in elevated content of malondialdehyde in leaves. Exogenous proline added 24 h before the irradiation inhibited lipid peroxidation. The total activity of superoxide dismutase (SOD) was analyzed in plant leaves, and three SOD isoforms—Mn-SOD, Fe-SOD, and Cu/Zn-SOD—were identified. Activities of these isoforms were measured over time, and the expression of their respective genes was analyzed by reverse transcription polymerase chain reaction (RT-PCR). It is shown that the addition of proline, UV-B irradiation, or combination of both treatments regulated in a differential manner the activities of SOD isoforms localized in various cell compartments. The activity of the cytosolic Cu/Zn-SOD isoform was limited by the presence of its mRNA, the content of which was regulated by mRNA synthesis or decay rate. By contrast, the activity of plastidic Fe-SOD isoform was regulated on the substrate (allosteric) level, not on the level of FSD gene expression. The activity of mitochondrial Mn-SOD isoform was insensitive to UV-B irradiation, addition of proline, or combination of both treatments, even though the level of MSD gene transcripts increased significantly after UV-B irradiation. The results indicate that MSD gene transcripts induced by UV-B were not completely processed to produce mature mRNA or mature mRNA was not capable of translation. It cannot be excluded that the synthesized macromolecule, the Mn-SOD precursor did not undergo posttranslational maturation to produce biologically active enzyme molecules. It appears that proline is involved in the differentially regulated complex expression of various SOD isoforms. This regulation is largely based on various extents of oxidative stress in different cell compartments.

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Abbreviations

RT-PCR:

reverse transcription polymerase chain reaction

SOD:

superoxide dismutase

References

  1. Blokhina, O., Virolainen, E., and Fagerstedt, K.V., Antioxidants, Oxidative Damage and Oxygen Deprivation Stress, Ann. Bot., 2003, vol. 91, pp. 179–194.

    Article  CAS  PubMed  Google Scholar 

  2. Matysik, J., Alia, A., Bhalu, B., and Mohanty, P., Molecular Mechanisms of Quenching of Reactive Oxygen Species by Proline under Stress in Plants, Curr. Sci., 2002, vol. 82, pp. 525–532.

    CAS  Google Scholar 

  3. Baranenko, V.V., Superoxide Dismutase in Plant Cells, Tsitologiya, 2006, vol. 48, pp. 465–474.

    CAS  Google Scholar 

  4. Shevyakova, N.I., Rakitin, V.Yu., Stesenko, L.A., Aronova, E.E., and Kuznetsov, Vl.V., Oxidative Stress and Fluctuations of Free and Conjugated Polyamines in the Halophyte Mesembryanthemum crystallinum L. under NaCl Salinity, Plant Growth Regul., 2006, vol. 50, pp. 69–78.

    Article  CAS  Google Scholar 

  5. Kartashov, A.V., Radyukina, N.L., Ivanov, Yu.V., Pashkovskii, P.P., Shevyakova, N.I., and Kuznetsov, Vl.V., Role of Antioxidant Systems in Wild Plant Adaptation to Salt Stress, Russ. J. Plant Physiol., 2008, vol. 55, pp. 463–468.

    Article  CAS  Google Scholar 

  6. Kuznetsov, Vl.V., Stetsenko, L.A., and Shevyakova, N.I., Exogenous Cadaverine Induces Oxidative Burst and Reduces Cadaverine Conjugate Content in the Common Ice Plant, J. Plant Physiol., 2009, vol. 166, pp. 40–51.

    Article  CAS  PubMed  Google Scholar 

  7. Shevyakova, N.I., Bakulina, E.A., and Kuznetsov, Vl.V., Proline Antioxidant Role in the Common Ice Plant Subjected to Salinity and Paraquat Treatment Inducing Oxidative Stress, Russ. J. Plant Physiol., 2009, vol. 56, pp. 663–669.

    Article  CAS  Google Scholar 

  8. Ozturk, L. and Demir, Y., In Vivo and In Vitro Protective Role of Proline, Plant Growth Regul., 2002, vol. 38, pp. 259–264.

    Article  CAS  Google Scholar 

  9. Lutts, S. and Guerrier, G., Peroxidase Activities of Two Rice Cultivars Differing in Salinity Tolerance as Affected by Proline and NaCl, Biol. Plant., 1995, vol. 37, pp. 577–586.

    Article  CAS  Google Scholar 

  10. Radyukina, N.L., Shashukova, A.V., Shevyakova, N.I., and Kuznetsov, Vl.V., Proline Involvement in the Common Sage Antioxidant System in the Presence of NaCl and Paraquat, Russ. J. Plant Physiol., 2008, vol. 55, pp. 649–656.

    Article  CAS  Google Scholar 

  11. Beauchamp, Ch. and Fridovich, I., Superoxide Dismutase Improved Assays and an Assay Applicable to Acrylamide Gels, Anal. Biochem., 1971, vol. 44, pp. 276–287.

    Article  CAS  PubMed  Google Scholar 

  12. Esen, A., A Simple Method for Quantitative, Semi-quantitative, and Qualitative Assay of Protein, Anal. Biochem., 1978, vol. 89, pp. 264–273.

    Article  CAS  PubMed  Google Scholar 

  13. Bates, L.S., Waldren, R.P., and Teare, I.D., Rapid Determination of Free Proline for Water Stress Studies, Plant Soil, 1973, vol. 39, pp. 205–207.

    Article  CAS  Google Scholar 

  14. Heath, R.L. and Packer, L., Photoperoxidation in Isolated Cloroplasts: 1. Kinetics and Stoichiometry of Fatty Acid Peroxidation, Arch. Biochem. Biophys., 1968, vol. 125, pp. 189–198.

    Article  CAS  PubMed  Google Scholar 

  15. Kliebenstein, D.J., Monde, R.-A., and Last, R.L., Superoxide Dismutase in Arabidopsis: An Eclectic Enzyme Family with Disparate Regulation and Protein Localization, Plant Physiol., 1998, vol. 118, pp. 637–650.

    Article  CAS  PubMed  Google Scholar 

  16. Miszalski, Z., Slesak, E., Niewiadomska, R., Baczek-Kwinta, R., Luttge, U., and Ratajczak, R., Subcellular Localization and Stress Responses of Superoxide Dismutase Isoforms from Leaves in the C3-CAM Intermediate Halophyte Mesembryanthemum crystallinum, L., Plant Cell Environ., 1998, vol. 21, pp. 169–179.

    Article  CAS  Google Scholar 

  17. Bradford, M.M., A Rapid and Sensitive Method for the Quantitations of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.

    Article  CAS  PubMed  Google Scholar 

  18. Krapp, A., Hofmann, B., Schafer, C., and Stitt, M., Regulation of the Expression of rbcS and Other Photosynthetic Genes by Carbohydrates: A Mechanism for the Sink Regulation of Photosynthesis, Plant J., 1993, vol. 3, pp. 817–828.

    Article  CAS  Google Scholar 

  19. Kuznetsov, Vl.V. and Shevyakova, N.I., Proline under Stress: Biological Role, Metabolism, and Regulation, Russ. J. Plant Physiol., 1999, vol. 46, pp. 274–289.

    CAS  Google Scholar 

  20. Hellmann, H., Funck, D., Rentsch, D., and Frommer, W.B., Hypersensitivity of an Arabidopsis Sugar Signaling Mutant toward Exogenous Proline Application, Plant Physiol., 2000, vol. 122, pp. 357–367.

    Article  CAS  PubMed  Google Scholar 

  21. Verbruggen, N. and Hermans, C., Proline Accumulation in Plants: A Review, Amino Acids, 2008, vol. 35, pp. 753–759.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to N. L. Radyukina.

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Original Russian Text © N.L. Radyukina, A.V. Shashukova, S.S. Makarova, Vl.V. Kuznetsov, 2011, published in Fiziologiya Rastenii, 2011, Vol. 58, No.1, pp. 49–57.

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Radyukina, N.L., Shashukova, A.V., Makarova, S.S. et al. Exogenous proline modifies differential expression of superoxide dismutase genes in UV-B-irradiated Salvia officinalis plants. Russ J Plant Physiol 58, 51–59 (2011). https://doi.org/10.1134/S1021443711010122

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