The Benefits of Exogenous NO: Enhancing Arabidopsis to Resist Botrytis cinerea
Hongyu Yang, Xiaodan Zhao, Jia Wu, Min Hu, Shaolei Xia
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DOI: 10.4236/ajps.2011.23060   PDF    HTML     5,739 Downloads   9,936 Views   Citations

Abstract

Botrytis cinerea is a necrotrophic fungal pathogen that impacts a wide range of hosts, including Arabidopsis. Pretreatment with nitric oxide (NO) donor sodium nitroprusside (SNP) on Arabidopsis leaves suppressed Botrytis cinerea infection development. Additionally, in this study the dosage levels of SNP applied to the leaves had no direct, toxic impact on the development of the pathogen. The relationship between NO and reactive oxidant species (ROS) was studied by using both spectrophotometrical methods and staining leaf material with fluorescent dyes, nitro blue tetrazolium (NBT), and with 3,3-diaminobenzidine (DAB). The results showed that exogenous NO restrained the generation of ROS, especially H2O2, as the pathogen interacted with the Arabidopsis plant. And this inhibition of reactive oxidant burst coincided with delay infection development in NO-supplied leaves. The influence of elevated level of NO on antioxidant enzymes was investigated in this study. The activities of catalase (CAT) and guaiacol peroxidase (POD) were increased to different degrees in both: 1) SNP treated only leaves, and 2) SNP pretreated leaves that were subsequently inoculateted with pathogens. However, the activity of superoxide dismutase (SOD) was unchanged in the leaves studied. The decrease in H2O2 content probably resulted from the increase in activities of POD and CAT. Our study suggests that NO might trigger some metabolic reactions, i.e. enhanced enzyme activity that restrains H2O2 which ultimately results in resistance to B. cinerea infection.

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Yang, H. , Zhao, X. , Wu, J. , Hu, M. and Xia, S. (2011) The Benefits of Exogenous NO: Enhancing Arabidopsis to Resist Botrytis cinerea. American Journal of Plant Sciences, 2, 511-519. doi: 10.4236/ajps.2011.23060.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] J. Durner and D. F. Klessig, “Nitric Oxide as a Signal in Plants,” Current Opinion in Plant Biology, Vol. 2, No. 5, 1999, pp. 369-374.
[2] M. Delledonne, Y. Xia, R. A. Dixon and C. Lamb, “Nitric Oxide Functions as a Signal in Plant Disease Resistance,” Nature, Vol. 394, No. 6, 1998, pp. 585-588.
[3] M. Arasimowicz and W. J. Floryszak, “Nitric Oxide as a Bioactive Signalling Molecule in Plant Stress Responses,” Plant Science, Vol. 172, No. 5, 2007, pp. 876-887.
[4] M. G. Zhao, Q. Y. Tian and W. H. Zhang, “Nitric Oxide Synthase-Dependent Nitric Oxide Production Is Associated with Salt Tolerance in Arabidopsis,” Plant Physiology, Vol. 144, No. 1, 2007, pp. 206-217.
[5] M. Delledonne, “NO News Is Good News for Plants,” Current Option in Plant Biology, Vol. 8, No. 4, 2005, pp. 390-396.
[6] P. Wojtaszek, “Oxidative Burst, an Early Plant Response to Pathogen Infection,” Biochemical Journal, Vol. 322, No.3, 1997, pp. 681-692.
[7] D. G. Gilchrist, “Programmed Cell Death in Plant Disease, the Purpose and Promise of Cellular Suicide,” Annual Review of Phytopathology, Vol. 36, 1998, pp. 393-414.
[8] E. M. Govrin and A. Levine, “The Hypersensitive Response Facilitates Plant Infection by the Necrotrophic Pathogen Botrytis cinerea,” Current Biology, Vol. 10, No. 13, 2000, pp. 751-757.
[9] A. V. Tiedemann, “Evidence for a Primary Role of Active Oxygen Species in Induction of Host Cell Death during Infection of Bean Leaves with Botrytis cinerea,” Physiological and Molecular Plant Pathology, Vol. 50, No. 3, 1997, 151-166.
[10] A. J. Able, “Role of Reactive Oxygen Species in the Response of Barley to Necrotrophic Pathogens,” Protoplasma, Vol. 221, No. 1-2, 2003, pp. 137-143.
[11] W. Edlich, G. Lorenz, H. Lyr, E. Nega and E. H. Pommer, “New Aspects on the Infection Mechanism of Botrytis cinerea Pers,” European Journal of Plant Pathology, Vol. 95, Supplement 1, 1989, pp. 53-62.
[12] Y. Elad, “The Use of Antioxidants (Free Radical Scavengers) to Control Grey Mold (Botrytis cinerea) and White Mold (Sclerotinia sclerotiorum) in Various Crops,” Plant Pathology, Vol. 41, No. 4, 1992, pp. 417-426.
[13] P. V. Barrlen, M. Staats and J. A. L. V. Kan, “Induction of Programmed Cell Death in Lily by the Fungal Pathogen Botrytis elliptica,” Molecular Plant Pathology, Vol. 5, No. 6, 2004, pp. 559-574.
[14] U. Ma?olepsza and H. Urbanek, “The Oxidants and Antioxidant Enzymes in Tomato Leaves Treated with O-hydroxyethylorutin and Infected with Botrytis cinerea,” European Journal of Plant Pathology, Vol. 106, No. 7, 2000, pp. 657-665.
[15] J. Floryszak-Wieczorek, M. Arasimowicz, G. Milczarek, H. Jelen and H. Jackowiak, “Only an Early Nitric Oxide Burst and the Following Wave of Secondary Nitric Oxide Generation Enhanced Effective Defence Responses of Pelargonium to a Necrotrophic Pathogen,” New Phytologist, Vol. 175, No. 4, 2007, pp. 718-730.
[16] D. Clark, J. Durner, D. A. Navarre and D. F. Klessig, “Nitric Oxide Inhibition of Tobacco Catalase and Ascorbate Peroxidase,” Molecular Plant Microbe Interaction, Vol. 13, No. 12, 2000, pp. 1380-1384.
[17] U. Ma?olepsza and S. Rózalska, “Nitric Oxide and Hydrogen Peroxide in Tomato Resistance, Nitric Oxide Modulates Hydrogen Peroxide Level in O-Hydroxyethylorutin- Induced Resistance to Botrytis cinerea in Tomato,” Plant Physiology and Biochemistry, Vol. 43, No. 6, 2005, pp. 623-635.
[18] S. L. Murray, C. Thomson, A. Chini, N. D. Read and G. J. Loake, “Characterization of a Novel, Defense-Related Arabidopsis Mutant, cir1, Isolated by Luciferase Imagin,” Molecular Plant―Microbe Interactions, Vol. 15, No. 6, 2002, pp. 57-566.
[19] M. Becana, P. Aparicio-Tejo, J. J. Irigoyen and D. M. Sanchez, “Some Enzymes of Hydrogen Peroxide Metabolism in Leaves and Root Nodules of Medicago sativa,” Plant Physiology, Vol. 82, No. 4, 1986, pp. 1169-1171.
[20] M. L. Orozco-Cardenas and C. A. Ryan, “Hydrogen Pperoxide Is Generated Systemically in Plant Leaves by Wounding and Systemin via the Octadecanoid Pathway,” Proceedings of the National Academy of Sciences in the USA, Vol. 96, No. 11, 1999, pp. 6553-6557.
[21] P. Brodersen, M. Petersen, H. M. Pike, B. Olszak, S. Skov, N. dum, L. B. J?rgensen, R. E. Brown and J. Mundy, “Knockout of Arabidopsis ACCELERATED-CELL-DEATH11 Encoding a Sphingosine Transfer Protein Causes Activation of Programmed Cell Death and Defense,” Genes & Development, Vol. 16, No. 4, 2002, pp. 490-502.
[22] I. Cakmak and H. Marschner, “Magnesium Deficiency and High Light Intensity Enhance Activities of Superoxide Dismutase, Ascorbate Peroxidase, and Glutathione Rreducatse in Bean Leaves,” Plant Physiology, Vol. 98, No. 4, 1992, pp. 1222-1227.
[23] C. Beauchamp and I. Fridovich, “Superoxide Dismutase, Improved Assays and Assay Applicable to Acrylamide Gels,” Analytical Biochemistry, Vol. 44, No. 1, 1971, pp. 276-287.
[24] N. Doke, “Involvement of Superoxide Generation in the Hypersensitive Response of Potato Tuber Tissues to Infection with an Incompatible Race of Phytophthora infestans and to Hyphal Wall Components,” Physiological Plant Pathology, Vol. 23, No. 3, 1983, pp. 345-357.
[25] M. W. Sutherland, “The Generation of Oxygen Radicals during Host Plant Responses to Infection,” Physiological and Molecular Plant Pathology, Vol. 39, No. 2, 1991, pp. 79-93.
[26] M. C. Mehdy, “Active Oxygen Species in Plant Defense against Pathogens,” Plant Physiology, Vol. 105, No. 2, 1994, pp. 467-472.
[27] M. C. Mehdy, Y. K. Sharma, K. Sathasivan and N. W. Bays, “The Role of Activated Oxygen Species in Plant Disease Resistance,” Physiology Plant, Vol. 98, 1996, pp. 365-374.
[28] R. Tenhaken, A. Levine, L. F. Brisson, R. A. Dixon and C. Lamb, “Function of the Oxidative Burst in Hypersensitive Disease Resistance,” Proceedings of the National Academy of Sciences USA, Vol. 92, No. 10, 1995, pp. 4158-4163.
[29] T. Mengiste, X. Chen, J. Salmeron and R. Dietrich, “The BOTRYTIS SUSCEPTIBLE1 Gene Encodes an R2R3MYB Transcription Factor Protein that Is Required for Biotic and Abiotic Stress Responses in Arabidopsis,” Plant Cell, Vol. 15, No. 11, 2003, pp. 2551-2565.
[30] P. Veronese, X. Chen, B. Bluhm, J. Salmeron, R. Dietrich and T. Mengiste, “The BOS Loci of Arabidopsis Are Required for Resistance to Botrytis cinerea Infection,” The Plant Journal, Vol. 40, No. 4, 2004, pp. 558-574.
[31] C. H. Unger, S. Kleta, G. Janell and A. Tiedemann, “Suppression of the Defence-Related Oxidative Burst in Leaf Tissue and Bean Suspension Cells by the Necrotrophic Pathogen Botrytis cinerea,” Journal of Phytopathology, Vol. 153, No. 1, 2005, pp. 15-26.
[32] Y. Tada, T. Mori, T. Shinogi, N. Yao, S. Takahashi, S. Betsuyaku, M. Sakamoto, P. Park, H. Nakayashiki, Y. Tosa and S. Mayama, “Nitric Oxide and Reactive Oxygen Species Do Not Elicit Hypersensitive Cell Death but Induce Apoptosis in the Adjacent Cells during the Defense Response of Oats,” Molecular Plant―Microbe Interact, Vol. 17, No. 3, 2004, pp. 245-253.
[33] R. P. Pratt, A. E. Brown and P. C. Mercer, “A Role for Hydrogen Peroxide in Degradation of Flax Fibre by Botrytis cinerea,” Transactions of the British Mycological Society, Vol. 91, No. 3, 1988, pp. 481-488.
[34] Y. Rolke, S. liu, T. Quidde, B. Williamson, A. Schouten, K. M Weltring, V. Siewers, K. B. Tenberge, B. Tudzynski and P. Tudzydki, “Functional Analysis of H2O2-Generating Systems in Botrytis cinerea, the Major Cu-Zn-Superoxide Dismutase (BCSOD1) Contributes to Virulence on French bean, whereas a Glucose Oxidase (BCGOD1) Is Dispensable,” Molecular Plant Pathology, Vol. 5, No. 1, 2004, pp. 17-27.
[35] M. Weigend and H. Lyr, “The Involvement of Oxidative Stress in the Pathogenesis of Botrytis cinerea on Vicia faba Leaves,” Journal of Plant Diseases and Protection, Vol. 103, 1996, pp. 310-320.
[36] R. E. Rij and C. F. Forney, “Phytotoxicity of Vapour Phase Hydrogen Peroxide to Thompson Seedless Grapes and Botrytis cinerea Spores,” Crop Protection, Vol. 14, No. 2, 1995, pp. 131-135.
[37] M. A. Ferrer and A. R. Barcelo, “Differential Effects of Nitric Oxide on Peroxidase and H2O2 Production by the Xylem of Zinnia elegans,” Plant, Cell & Environment, Vol. 22, No. 7, 1999, pp. 891-897.

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