Skip to main content

Antioxidant Defenses of Mycorrhizal Fungus Infection Against SO2-Induced Oxidative Stress in Avena nuda Seedlings

Abstract

Colonization of arbuscular mycorrhizal fungi Glomus mosseae increased Avena nuda seedling tolerance to SO2 exposure, as indicated by elevated total plant biomass and ameliorative photosynthetic rate, when compared to the non-mycorrhizal plants. This is associated with an improved antioxidant capacity as shown by enhanced superoxide dismutase and catalase activity, increased ascorbic acid and glutathione content, and reduced malondialdehyde and hydrogen peroxide level in the mycorrhizal plants relative to the non-mycorrhizal plants under SO2 exposure. The mycorrhizal fungi colonization had no effect on the stomatal conductance. To our knowledge, this is the first finding of this sort.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Aebi HE (1983) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analyses. Verlag Chemie, Weinheim, pp 273–282

    Google Scholar 

  2. Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plant 100:224–233. doi:10.1111/j.1399-3054.1997.tb04778.x

    Article  CAS  Google Scholar 

  3. Asada K (1980) Formation and scavenging of superoxide in chloroplasts with relation to injury by sulfur oxides in studies on the effects of air pollutants on plants and mechanisms of phytotoxicity. Res Rep Natt Inst-Environ Stud 11:165–179

    CAS  Google Scholar 

  4. Asada K, Kiso K (1973) Initiation of aerobic oxidation of sulphite by illuminated spinach chloroplasts. Eur J Biochem 33:253–257. doi:10.1111/j.1432-1033.1973.tb02677.x

    Article  CAS  Google Scholar 

  5. Azcón-Aguilar C, Barea JM (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens – an overview of the mechanisms involved. Mycorrhiza 6:457–464. doi:10.1007/s005720050147

    Article  Google Scholar 

  6. Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566. doi:10.1016/0003-2697(87)90489-1

    Article  CAS  Google Scholar 

  7. Bowler C, Van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116. doi:10.1146/annurev.pp.43.060192.000503

    Article  CAS  Google Scholar 

  8. Bradford MM (1976) 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. doi:10.1016/0003-2697(76)90527-3

    Article  CAS  Google Scholar 

  9. Dubey RS (2005) Photosynthesis in plants under stressful conditions. In: Pessarakli M (ed) Hand book of photosynthesis, 2nd edn. CRC Press, Taylor and Francis Group, New York, pp 717–737

    Google Scholar 

  10. Feng G, Zhang FS, Li LX, Tian CY, Tang C, Rengel Z (2002) Improved tolerance of maize plants to salt sress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 12:185–190. doi:10.1007/s00572-002-0170-0

    Article  CAS  Google Scholar 

  11. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. doi:10.1111/j.1469-8137.1980.tb04556.x

    Article  Google Scholar 

  12. Giri B, Kapoor R, Mukerji KG (2007) Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus Fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 54:753–760. doi:10.1007/s00248-007-9239-9

    Article  CAS  Google Scholar 

  13. Goyal SK (2001) Use of rosaniline hydrochloride dye for atmospheric SO2 determination and method sensitivity analysis. J Environ Monit 3:666–670. doi:10.1039/b106209n

    Article  CAS  Google Scholar 

  14. Griffith OW, Meister A (1979) Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (s-n-butyl-homocysteine sulfoximine). J Biol Chem 254:7558–7560

    CAS  Google Scholar 

  15. Hao L, Zhang HW, Xu X, Tao SY, Yu L (2005) SO2-caused oxidative stress and modulation of some signal molecules in wheat. Chin J Appl Ecol 16:1038–1042

    CAS  Google Scholar 

  16. Hao L, Zhou LN, Xu X, Cao J, Xi T (2006) The role of salicylic acid and carrot embryogenic callus extracts in somatic embryogenesis of naked oat (Avena nuda). Plant Cell Tiss Org Cult 85:109–113. doi:10.1007/s11240-005-9052-4

    Article  CAS  Google Scholar 

  17. Hetrick BA, Wilson GW, Figge DA (1994) The influence of mycorrhizal symbiosis and fertilizer amendments on establishment of vegetation in heavy metal mine spoil. Environ Pollut 86:171–179. doi:10.1016/0269-7491(94)90188-0

    Article  CAS  Google Scholar 

  18. Keller T, Schwager H (1977) Air pollution and ascorbic acid. Eur J Forest Pathol 7:338–350. doi:10.1111/j.1439-0329.1977.tb00603.x

    Article  CAS  Google Scholar 

  19. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–505

    Google Scholar 

  20. Lambais MR, Rios-Ruiz WE, Andrade RM (2003) Antioxidant responses in bean (Phaseolus vulgaris) roots colonized by arbuscular mycorrhizal fungi. New Phytol 160:421–428. doi:10.1046/j.1469-8137.2003.00881.x

    Article  CAS  Google Scholar 

  21. Li B, Xing D, Zhang LR (2007) Involvement of NADPH oxidase in sulfur dioxide-induced oxidative stress in plant cells. Nat Prod Rep 6:628–634

    CAS  Google Scholar 

  22. Lüttge U, Osmond CB, Ball E, Brinckmann E, Kinze G (1972) Bisulfite compounds as metabolic inhibitors: nonspecific effects on membranes. Plant Cell Physiol 13:505–514

    Google Scholar 

  23. Madamanchi NR, Alscher RG (1991) Metabolic bases for differences in sensitivity of two pea cultivars to sulfur dioxide. Plant Physiol 97:88–93

    CAS  Google Scholar 

  24. Marulanda A, Porcel R, Barea JM, Azcon R (2007) Drought tolerance and antioxidant activities in lavender plants colonized by native drought-tolerant or drought-sensitive Glomus species. Microb Ecol 54:543–552. doi:10.1007/s00248-007-9237-y

    Article  CAS  Google Scholar 

  25. Miszalski Z, Niewiadomska E (1993) SO2 oxidation during greening of Avena sativa seedlings. Photosynthetica 28:577–581

    CAS  Google Scholar 

  26. 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. doi:10.1111/j.1399-3054.1983.tb04162.x

    Article  CAS  Google Scholar 

  27. Peiser GD, Yang SF (1985) Biochemical and physiological effects of SO2 on non-photosynthetic processes in plants. In: Winner WE, Mooney HA, Goldstein RA (eds) Sulphur dioxide and vegetation. Stanford University Press, Stanford, pp 148–161

    Google Scholar 

  28. Pfanz H, Heber U (1986) Buffer capacities of leaves, leaf cells, and leaf cell organelles in relation to fluxes of potentially acidic gases. Plant Physiol 81:597–602

    CAS  Google Scholar 

  29. Pfanz H, Martinoia E, Otto-Ludwig L, Heber U (1987) Flux of SO2 into leaf cells and cellular acidification by SO2. Plant Physiol 85:928–933

    CAS  Google Scholar 

  30. Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Physiol 157:135–143. doi:10.1046/j.1469-8137.2003.00658.x

    Article  CAS  Google Scholar 

  31. Rosendahl CN, Rosendahl S (1991) Influence of vesicular-arbuscular mycorrhizal fungi (Glomus spp.) on the response of cucumber (Cucumis sativus L.) to salt stress. Environ Exp Bot 3:313–318. doi:10.1016/0098-8472(91)90055-S

    Article  Google Scholar 

  32. Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress, new perspectives for molecular studies. Mycorrhiza 13:309–317. doi:10.1007/s00572-003-0237-6

    Article  Google Scholar 

  33. Ruiz-Lozano JM, Collados C, Barea JM, Azcón R (2001a) Cloning of cDNAs encoding SODs from lettuce plants which show differential regulation by arbuscular mycorrhizal symbiosis and by drought stress. J Exp Bot 52:2241–2242

    CAS  Google Scholar 

  34. Ruiz-Lozano JM, Collados C, Barea JM, Azcón R (2001b) Arbuscular mycorrhizal symbiosis can alleviate drought-induced nodule senescence in soybean plants. New Phytol 151:493–502. doi:10.1046/j.0028-646x.2001.00196.x

    Article  CAS  Google Scholar 

  35. Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365. doi:10.1093/jexbot/53.372.1351

    Article  Google Scholar 

  36. Shalata A, Tal M (1998) 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. doi:10.1034/j.1399-3054.1998.1040204.x

    Article  Google Scholar 

  37. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, San Diego, p 605

    Google Scholar 

  38. Surówka E, Karolewski P, Niewiadomska E, Libik M, Miszalski Z (2007) Antioxidative response of Mesembryanthemum crystallinum plants to exogenous SO2 application. Plant Sci 172:76–84. doi:10.1016/j.plantsci.2006.07.018

    Article  CAS  Google Scholar 

  39. Tanka K, Sugahara K (1980) Role of superoxide dismutase in defense against SO2 toxicity and an increase in superoxide dismutase activity with SO2 fumigation. Plant Cell Physiol 21:601–611

    Google Scholar 

  40. Wingsle G, Gardestrom P, Hallgren JE, Karpinski S (1991) Isolation, purification, and subcellular localization of superoxide dismutase from Scots pine (Pinus silvestris L.) needles. Plant Physiol 95:21–28

    CAS  Article  Google Scholar 

  41. Wu QS, Xia RX, Zou YN (2006) Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliata) seedlings subjected to water stress. J Plant Physiol 163:1101–1110. doi:10.1016/j.jplph.2005.09.001

    Article  CAS  Google Scholar 

  42. Xu Q, Xu X, Zhao Y, Jiao K, Herbert SJ, Hao L (2008) 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. doi:10.1007/s10725-007-9247-2

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Natural Science Foundation of China (30570445), Natural Science Foundation of Liaoning Province (No. 20021022), Tackle Key Problem of Science and Technology, Education Department of Liaoning Province (2004D005) and Director Foundation of Experimental Centre, Shenyang Normal University (SY200406).

Author information

Affiliations

Authors

Corresponding author

Correspondence to L. Hao.

Additional information

L. L. Huang and C. Yang contributed equally to this work.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Huang, L.L., Yang, C., Zhao, Y. et al. Antioxidant Defenses of Mycorrhizal Fungus Infection Against SO2-Induced Oxidative Stress in Avena nuda Seedlings. Bull Environ Contam Toxicol 81, 440 (2008). https://doi.org/10.1007/s00128-008-9521-7

Download citation

Keywords

  • Avena nuda
  • Sulfur dioxide
  • Arbuscular mycorrhizal symbiosis
  • Antioxidant defense