biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 55:297-304, 2011 | DOI: 10.1007/s10535-011-0042-6

Role of endogenous salicylic acid in Arabidopsis response to elevated sulfur dioxide concentration

L. Hao1,*, Y. Wang1, J. Xu1, S.-D. Feng2, C.-Y. Ma1, C. Liu1, X. Xu1, G.-Z. Li1, S. J. Herbert3
1 College of Chemistry and Life Sciences, Shenyang Normal University, Shenyang, P.R. China
2 College of Life Science and Technology, Harbin Normal University, Harbin, P.R. China
3 Department of Plant, Soil, and Insect Sciences, University of Massachusetts, Amherst, USA

The response of Arabidopsis thaliana plants to elevated sulfur dioxide could be related to their endogenous salicylic acid (SA) content and signaling. The wild type (WT, ecotype Columbia) and its mutant snc1 with high SA content, npr1-1 with a blockage in SA signaling, transgenic line nahG with low SA content and double mutant snc1nahG plants were exposed to 0.5 mm3 dm-3 SO2 for 3 h d-1 for 14 d in a growth chamber. Under unstressed conditions, total SA contents in snc1 and npr1-1 were 7- and 2-fold higher than those in WT, respectively, but in nahG SA content was only 28 % of that in WT. The expression of nahG in snc1 plants decreased SA content to the WT level. Increased SA contents were observed in snc1, npr1-1 and WT after 12-h SO2 exposure, whereas no major changes were detected in nahG and snc1nahG plants. The snc1 plants exhibited higher tolerance to SO2 exposure than snc1nahG plants and especially nahG and npr1-1 plants according to plant biomass, total chlorophyll content and photosynthetic rate. The SO2 exposure decreased net photosynthetic rate, maximum photochemical efficiency (Fv/Fm) and actual quantum efficiency of photosystem 2 (ΦPS2). SO2-induced oxidative damage in the tested plants was confirmed by increased malondialdehyde (MDA) content and electrolyte leakage. Increases in superoxide dismutase (SOD) and peroxidase (POD) activity, reduced glutathione (GSH) content and a ratio of reduced/oxidized glutathione (GSSG) might be responsible for the decreased contents of H2O2 and alleviation of oxidative injury in snc1 plants compared with other lines exposed to SO2. These observations implied that endogenous SA content and signaling may play an essential role in plant responses to SO2 stress.

Keywords: chlorophyll fluorescence; lipid peroxidation; net photosynthetic rate; redox homeostasis; stomatal conductance

Received: May 4, 2009; Accepted: May 12, 2010; Published: June 1, 2011  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Hao, L., Wang, Y., Xu, J., Feng, S.-D., Ma, C.-Y., Liu, C., ... Herbert, S.J. (2011). Role of endogenous salicylic acid in Arabidopsis response to elevated sulfur dioxide concentration. Biologia plantarum, 55(2), 297-304. doi: 10.1007/s10535-011-0042-6
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Aebi, H.: Catalase. - In: Bergmeyer, H.U. (ed.): Methods of Enzymatic Analysis. 3rd Ed. Pp. 273-282. Verlag-Chemie, Weinheim 1983.
    2. Ananieva, E.A., Christov, K.N., Popova, L.P.: Exogenous treatment with salicylic acid leads to increased antioxidant capacity in leaves of barley plants exposed to paraquat. - J. Plant Physiol. 161: 319-328, 2004. Go to original source...
    3. Ball, L., Accotto, G.P., Bechtold, U., Creissen, G., Funck, D., Jimenez, A., Kular, B., Leyland, N., Mejia-Carranza, J., Reynolds, H., Karpinski, S., Mullineauxc, P.M.: Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. - Plant Cell 16: 2448-2462, 2004. Go to original source...
    4. Baker, N.R., Oxborough, K., Lawson, T., Morison, J.I.: High resolution imaging of photosynthetic activities of tissues, cells and chloroplasts in leaves. - J. exp. Bot. 52: 615-621, 2001. Go to original source...
    5. Beyer, W.F., Fridovich, I.: Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. - Anal. Biochem. 161: 559-566, 1987. Go to original source...
    6. Bowler, C., Van Montagu, M., Inzé, D.: Superoxide dismutase and stress tolerance. - Annu. Rev. Plant Physiol. Plant mol. Biol. 43: 83-116, 1992. Go to original source...
    7. Bowling, S.A., Clarke, J.D., Liu, Y., Klessig, D.F., Dong, X.: The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. - Plant Cell 9: 1573-1584, 1997. Go to original source...
    8. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
    9. Cao, H., Bowling, S.A., Gordon, A.S., Dong, X.: Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. - Plant Cell 6: 1583-1592, 1994. Go to original source...
    10. Chen, Z., Silva, H., Klessig, D.F.: Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. - Science 262: 1883-1886, 1993. Go to original source...
    11. Dat, J., Vandenabeele, S., Vranová, E., Van Montagu, M., Inzé, D., Van Breusegem, F.: Dual action of active oxygen species during plant stress responses. - Cell. Mol. Life Sci. 57: 779-795, 2000. Go to original source...
    12. Delaney, T.P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., Ward, E., Ryals, J.: A central role of salicylic acid in plant disease resistance. - Science 266: 1247-1250, 1994. Go to original source...
    13. Foyer, C.H., Lopez-Delgado, H., Dat, J.F., Scott, I.M.: Hydrogen peroxide- and glutathione-associated mechanisms of acclamatory stress tolerance and signaling. - Physiol. Plant. 100: 241-254, 1997. Go to original source...
    14. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., Shinozak, K.: Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. - Curr. Opin. Plant Biol. 9: 436-442, 2006. Go to original source...
    15. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H., Ryals, J.: Requirement of salicylic acid for the induction of systemic acquired resistance. - Science 261: 754-756, 1993. Go to original source...
    16. Goyal, S.K.: Use of rosaniline hydrochloride dye for atmospheric SO2 determination and method sensitivity analysis. - J. Environ. Monitoring 3: 666-670, 2001. Go to original source...
    17. Griffith, O.W., Meister, A.: Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (s-n-butylhomocysteine sulfoximine). - J. biol. Chem. 254: 7558-7560, 1979. Go to original source...
    18. Hao, L., Zhang, H., Xu, X., Tao, S., Yu, L.: SO2-caused oxidative stress and modulation of some signal molecules in wheat. - Chin. J. appl. Ecol. 16: 1038-1042, 2005.
    19. Hemeda, H.M., Klein, B.P.: Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. - J. Food Sci. 55: 184-185, 1990. Go to original source...
    20. Horvath, E., Pal, M., Szalai, G., Paldi, E., Janda, T.: Exogenous 4-hydroxybenzoic acid and salicylic acid modulate the effect of short-term drought and freezing stress on wheat plants. - Biol. Plant. 51: 480-487, 2007. Go to original source...
    21. Kubo, A., Saji, H., Tanaka, K., Kondo, N.: Expression of Arabidopsis cytosolic ascorbate peroxidase gene in response to ozone or sulfur dioxide. - Plant mol. Biol. 29: 479-489, 1995. Go to original source...
    22. Legge, A.H., Krupa, S.V.: Effects of sulphur dioxide. - In: Bell, J.N.B., Treshow, M. (ed.): Air Pollution and Plant Life. Pp. 135-162. Wiley, Chichester 2002.
    23. Li, X., Clarke, J.D., Zhang, Y., Dong, X.: Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. - Mol. Plant Microbe Interact. 14: 1131-1139, 2001. Go to original source...
    24. Luo, M.H., Yuan, S., Chen Y.E., Liu, W.J., Du, J.B., Lei, T., Wang, M.B., Lin H.H.: Effects of salicylic acid on the photosystem 2 of barley seedlings under osmotic stress. - Biol. Plant. 53: 663-669, 2009. Go to original source...
    25. Mateo, A., Funck, D., Mühlenbock, P., Kular, B., Mullineaux, P.M., Karpinski, S.: Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. - J. exp. Bot. 57: 1795-1807, 2006. Go to original source...
    26. Mou, Z.L., Fan, W.H., Dong, X.: Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. - Cell 113: 935-944, 2003. Go to original source...
    27. Mukherjee, S.P., Choudhuri, M.A.: Implications of water stress induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. - Physiol. Plant. 58: 166-170, 1983. Go to original source...
    28. Munné-Bosch, S., Peñuelas, J., Llusià, J.: A deficiency in salicylic acid alters isoprenoid accumulation in water-stresses NahG transgenic Arabidopsis plants. - Plant Sci. 172: 756-762, 2007. Go to original source...
    29. Mutlu, S., Atici, Ö., Nalbantoglu, B.: Effects of salicylic acid and salinity on apoplastic antioxidant enzymes in two wheat cultivars differing in salt tolerance. - Biol. Plant. 53: 334-338, 2009. Go to original source...
    30. Newman, M.A., Van Roepenack-Lahaye, E., Parr, A., Daniels, M.J., Dow, J.M.: Induction of hydroxycinnamoyl-tyramine conjugates in pepper by Xanthomonas campestris: a plant defense response activated by hrp gene-dependent and -independent mechanisms. - Mol. Plant Microbe Interact. 14: 785-792, 2001. Go to original source...
    31. Nouchi, I.: Responses of whole plants to air pollutions. - In: Omasa, K. (ed.) Air Pollution and Plant Biotechnology. Pp. 4-8. Springer-Verlag, Berlin - Tokyo 2002. Go to original source...
    32. Petersen, M., Brodersen, P., Naested, H., Andreasson, E., Lindhart, U., Johansen, B., Nielsen, H.B., Lacy, M., Austin, M.J., Parker, J.E., Sharma, S.B., Klessig, D.F., Martienssen, R., Mattsson, O., Jensen, A.B., Mundy, J.: Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. - Cell 103: 1111-1120, 2000. Go to original source...
    33. Pfanz, H., Heber, U.: Buffer capacities of leaves, leaf cells, and leaf cell organelles in relation to fluxes of potentially acidic gases. - Plant Physiol. 81: 597-602, 1986. Go to original source...
    34. Popova, L.P., Maslenkova, L.T., Yordanova, R.Y., Ivanova, A.P., Krantev, A.P., Szalai, G., Janda, T.: Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. - Plant Physiol. Biochem. 47: 224-231, 2009. Go to original source...
    35. Schaffer, F.Q., Buettner, G.R.: Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. - Free Radical Biol. Med. 30: 1191-1212, 2001. Go to original source...
    36. Scott, I.M., Clarke, S.M., Wood, J.E., Mur, L.A.J.: Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis. - Plant Physiol. 35: 1040-1049, 2004. Go to original source...
    37. Shalata, A., Tal, M.: The effect of salt stress on lipid peroxidation and antioxidants in the leaf of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii. - Physiol. Plant. 104: 167-174, 1998. Go to original source...
    38. Sharma, Y.K., León, J., Raskin, I., Davis, K.R.: Ozone-induced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defense-relative transcripts and induced resistance. - Proc. nat. Acad. Sci. USA 93: 5099-5104, 1996. Go to original source...
    39. Tada, Y., Spoel, S.H., Pajerowska-Mukhtar, K., Mou, Z., Song, J., Wang, C., Zou, J., Dong, X.: Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. - Science 321: 952-956, 2008. Go to original source...
    40. Valko, M., Leibfritz, D., Moncola, J., Cronin, M.T.D., Mazura, M., Telser, J.: Free radicals and antioxidants in normal physiological functions and human disease. - Int. J. Biochem. Cell. Biol. 39: 44-84, 2007. Go to original source...
    41. Wang, D.H., Li, X.X., Su, Z.K., Ren, H.X.: The role of salicylic acid in response of two rice cultivars to chilling stress. - Biol. Plant. 53: 545-552, 2009. Go to original source...
    42. Xu, Q., Xu, X., Zhao, Y., Jiao, K., Herbert, S.J., Hao, L.: Salicylic acid, hydrogen peroxide and calcium-induced saline tolerance associated with endogenous hydrogen peroxide homeostasis in naked oat seedlings. - Plant Growth Regul. 54: 249-259, 2008. Go to original source...
    43. Yuan, S., Lin, H.H.: Role of salicylic acid in plant abiotic stress. - Z. Naturforsch. 63c: 313-320, 2008. Go to original source...
    44. Zhang, Z.L., Qu, W.J.: Guide to Plant Physiology Experiment. 3rd Ed. - Higher Education Press, Beijing 2003.

    Return to the content