Effect of Nitric Oxide on Paraquat-Tolerance in Lettuce Leaves

상추잎의 Paraquat 내성에 미치는 Nitric oxide의 영향

  • Lee, Jee-Na (Department of Biological Sciences, Pusan National University) ;
  • Hong, Jung-Hee (Department of Biological Sciences, Pusan National University)
  • Received : 2011.09.10
  • Accepted : 2011.12.10
  • Published : 2011.12.31


The protective effect of nitric oxide (NO) on the antioxidant system under paraquat(PQ) stress was investigated in leaves of 8-week-old lettuce (Lactuca sativa L.) plants. PQ stress caused a decrease of leaf growth including leaf length, width and weight. Application of NO donor, sodium nitroprusside (SNP), significantly alleviated PQ stress induced growth suppression. SNP permitted the survival of more green leaf tissue preventing chlorophyll content reduction and of higher quantum yield for photosystem II than in non-treated controls under PQ exposure, suggesting that NO has protective effect on chloroplast membrane in lettuce leaves. Flavonoids and anthocyanin were significantly accumulated in the leaves upon PQ exposure. However, the rapid increase of these compounds was alleviated in the SNP treated leaves. PQ treatment resulted in lipid peroxidation and induced accumulation of hydrogen peroxide ($H_2O_2$) in the leaves, while SNP prevented PQ induced increase in malondialdehyde (MDA) and $H_2O_2$. These results demonstrate that SNP serves as an antioxidant agent able to scavenge $H_2O_2$ to protect plant cells from oxidative damage. The activities of two antioxidant enzymes that scavenge reactive oxygen species, superoxide dismutase (SOD) and catalase (CAT) in lettuce leaves in the presence of NO donor under PQ stress were higher than those under PQ stress alone. Application of 2-(4-carboxyphenyl)-4, 4, 5, 5-tetramethylimidazoline-1-oxyl-3-oxide (PTIO), a specific NO scavenger, to the lettuce leaves arrested SNP mediated protective effect on leaf growth, photosynthetic pigment and antioxidant systems. However, PTIO had little effect on lettuce leaves under PQ stress compared with that of PQ stress alone. The obtained data suggest that the damage caused by PQ stress is in part due to increased generation of active oxygen by maintaining increased antioxidant enzyme activities and SNP protects plants from oxidative stress. From these results it is suggested that NO might act as a signal in activating active oxygen scavenging system that protects plants from oxidative damage induced by PQ stress and thus confer PQ tolerance.


Antioxidant enzymes;Lactuca sativa L.;Nitric oxide;Oxidative stress;Paraquat


  1. Beligni, M. V., Lamattina, L., 2000, Nitric acid protects against cellular damage produced by methyl viologen herbicides in potato plants, Nitric Oxide Biol. Chem., 3, 199-208.
  2. Beligni, M. V., Lamattina, L., 1999, Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues, Planta, 208, 337-344.
  3. Bjorkman, O., Demmig, B., 1987, Photon yield of oxygen evolution and chlorophyll fluorescence characteristics at $77^{\circ}K$ among vascular plants of diverse organ, Planta, 170, 489-504.
  4. Clark, D., Dunar, J., Navarre, D. A., Klessig, D. F., 2000, Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase, Mol. Plant-Microbe Interact., 14, 1380-1384.
  5. Durner, J., Klessing, D. F., 1996, Salicylic acid is a modulator of tobacco and mammalian catalases, J. Biol. Chem., 271, 28492-28502.
  6. Hsu, Y. T., Kao, C. H., 2004, Cadmium toxicity is reduced by nitric oxide in rice leaves, Plant Growth Regul., 42, 227-238.
  7. Hung, K. T., Chang, C. J., Kao, C. H., 2002, Paraquat toxicity is reduced by nitric oxide in rice leaves, J. Plant Physiol., 159, 159-166.
  8. Inskeep, W. P., Bloom, P. R., 1985, Extinction coefficients of chlorophyll a and b in N, N-dimethylformamide and 80% acetone, Plant Physiol., 77, 483-485.
  9. Kraus, T. E., Fletcher, R. A., 1994, Paclobutrazol protects wheat seedlings from heat and paraquat injury: Is detoxification of active oxygen involved?, Plant Cell Physiol., 35, 45-52.
  10. Kraus, T. E., McKersie, B. D., Fletcher, R. A., 1995, Paclobutrazol-induced tolerance of wheat leaves to paraquat may involve increased antioxidant enzyme activity, J. Plant Physiol., 145, 570-576.
  11. Leshem, Y. Y., 1996, Nitric oxide in biological systems, Plant Growth Regul., 18, 155-159.
  12. Leshem, Y. Y., Haramaty, E., 1996, The characterization and contrasting effects of the nitric oxide free radical in vegetative stress and senescence of Pisum sativum Linn. foliage, J. Plant Physiol., 148, 258-263.
  13. Mirecki, R. M., Teramura, A. H., 1984, Effects of ultraviolet-B irradiance on soybean, Plant Physiol., 74, 475-480.
  14. Neill, S. J., Desikan, R., Hancock, J. T., 2003, Nitric oxide signaling in plants, New Phytol., 159, 11-35.
  15. Orozco-Cardenas, M., Ryan, C. A., 2002, Nitric oxide negatively modulate wound signaling in tomato plants, Plant Physiol., 130, 487-493.
  16. Qiao, W., Fan, L. -M., 2008, Nitric oxide signaling in plant response to abiotic stresses, J. Int. Plant Biol., 50, 1238-1246.
  17. Schmidt, A, Kunert, K. J., 1986, Lipid peroxidation in higher plants : The role of glutathione reductase, Plant Physiol., 82, 700-702.
  18. Scandalios, J. G., 1993, Oxygen stress and superoxide dismutases, Plant Physiol., 101, 7-12.
  19. Schreiber, U., Schliwa, U., Bilger, W., 1986, Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quencing with a new type of modulation fluorometer, Photosynth. Res., 10, 51-62.
  20. Shaaltiel, Y., Gressel, J., 1986, Multienzyme oxygen radical detoxifying system correlated with paraquat resistance in Conyza bonariensis, Pestic. Biochem. Physiol., 26, 22-28.
  21. Shevyakova, N. I., Bakulina, E. A., Kuznetsov, VI, V., 2009, Proline antioxidant role in the common ice plant subjected to salinity and paraquat treatment inducing oxidative stress, Russian Jour. Plant Physiol., 56, 663-669.
  22. Spychalla, J. P., Desborough, S. L., 1990, Superoxide dismutase, catalase and alpha tocopherol content of stored potato tubers. Plant Physiol., 94 : 1214-1218.
  23. Steyn, W. J., Wand, S. J. E., Holcroft, D. M., Jacob, G., 2002, Anthocyanins in vegetative tissues : A proposed unified function in photoprotection, New Phytol., 155, 349-361.
  24. Tattini, M., Galardi, C., Pinelli, P., Massai, R., Remorini, D., Agati, G., 2004, Differential accumulation of flavonoids and hydroxycinnainates in leaves of Ligustrum vulgare under excess light and drought stress, New Phytol., 163, 547-561.
  25. Tossi, V., Lamattina, L., Cassia, R., 2009, An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation, New Phytol., 181, 871-879.
  26. Tu, J., Shen, Y. B., Xu, L. L., 2003, Regulation of nitric oxide on the aging process of wheat leaves, Acta. Bot. Sin., 45, 1055-1062.
  27. Uchida, A., Jagendorf, A. T., Hibino, T., Takabe, T., Takabe, T., 2002, Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice, Plant Sci., 163, 515-523.
  28. Veljovic-Jovanovic, S., Noctor, G., Foyer, C. H., 2002, Are leaf hydrogen peroxide concentration commonly overestimated? The potential influence of artefactual interference by tissue phenolics and ascorbate, Plant Physiol. Biochem., 40, 501-507.
  29. Wendehenne, D., Pulgin, A., Klessing, D. F., Durner, J., 2001, Nitric acid : comparative synthesis and signaling in animal and plant cell, Trends Plant Sci., 6, 177-186.
  30. Zhao, M. -G., Tian Q. -Y. Zhang, W. -H,, 2007, Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis, Plant Physiol., 144, 206-217.
  31. Zhao, S. J., Xu, C. C., Zhou, Q., Meng, Q. W., 1994, Improvement of method for measurement of malondialdehyde in plant tissues, Plant Physiol., Comm., 30, 207-210.