Cover Image

Not for Sale



View/Hide Left Panel

our results suggest that plants contain a functional NO signaling system whose components and targets are highly analogous to those identified in animals (Fig. 3).

Conclusions

The results presented in this paper strongly argue that both SA and NO play important roles in the activation of plant defense responses after pathogen attack. However, the interrelationship between their respective signaling pathways is currently unclear. NO, as well as other ROS, have been shown to stimulate the accumulation of SA, and SA induces the production of ROS, such as H2O2 and NO (20, 68). Thus, these signals appear to be self-amplifying. One likely role for NO, SA, and ROS is to promote the HR and pathogen killing. Both ROS and SA (or a factor downstream of SA) have been shown to synergize with NO to enhance host cell death in soybean suspension cells ( 21). This situation may parallel that in animals, in which NO collaborates with ROS to regulate apoptosis and produce peroxynitrite, a highly toxic compound that is thought to directly kill the pathogen (20). In addition, SA may mediate and/or potentiate NO's effects by altering the activity of various NO-regulated enzymes, such as aconitase, ascorbate peroxidase, and catalase (ref.62 and D. Clark, J.D., and D.F.K., unpublished results). SA also induces the synthesis of a pathogen-inducible oxygenase in plants that has strong homology to a mammalian cyclooxygenase (69). This enzyme is posttranslationally activated by NO in mammals (70). Thus, SA and NO may work synergistically to transduce the defense signal by targeting the same effector proteins and/or their genes.

In addition to acting synergistically with NO to activate various defense responses, SA may also antagonize the NO signaling pathway. In mammalian cells, salicylates are potent scavengers of NO and its derivatives (71). Moreover, salicylates inhibit the activity and transcription of iNOS (72). In plants, SA may also antagonize NO's ability to inhibit respiration (and thereby cause oxidative stress) by activating the NO-insensitive alternative oxidase (73). Considering the many interactions that are currently emerging between the pleiotropic effectors SA, NO, and other ROS, it is apparent that we are at a very early stage in understanding the complexity of their action in disease resistance.

We thank D'Maris Dempsey for assistance in preparation of this manuscript. This work was supported by Grants MCB 9723952 and MCB 9904660 from the National Science Foundation and 9802200 from the U.S. Department of Agriculture.

1. Flor, H. ( 1971) Annu. Rev. Phytopathol. 9, 275–296.

2. Keen, N. T. ( 1990) Annu. Rev. Genet. 24, 447–463.

3. Baker, C. J. & Orlandi, E. W. ( 1995) Annu. Rev. Phytopathol. 33, 299–321.

4. Lamb, C. & Dixon, R. A. ( 1997) Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251–275.

5. Hammond-Kosack, K. E. & Jones, J. D. G. ( 1996) Plant Cell 8, 1773–1791.

6. Yang, Y., Shah, J. & Klessig, D. F. ( 1997) Genes Dev. 11, 1621–1639.

7. Dangl, J. L., Dietrich, R. A. & Richberg, M. H. ( 1996) Plant Cell 8, 1793–1807.

8. Kombrink, E. & Somssich, I. E. ( 1997) in Plant Relationships, eds. Carroll, G. C. & Tudzynski, P. (Springer-Verlag, Berlin), pp. 107–128.

9. Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H.-Y. & Hunt, M. D. ( 1996) Plant Cell 8, 1809–1819.

10. Dempsey, D., Shah, J. & Klessig, D. F. ( 1999) Crit. Rev. Plant Sci. 18, 547–575.

11. Shah, J. & Klessig, D. F. ( 1999) in Biochemistry and Molecular Biology of Plant Hormones, eds. Hooykaas, P. P. J., Hall, M. A. & Libbenga, K. R. (Elsevier, Amsterdam), pp. 513–541.

12. Dong, X. ( 1998) Curr. Opin. Plant Biol. 1, 316–323.

13. Pieterse, C. M. J. & van Loon, L. C. ( 1999) Trends Plant Sci. 4, 52–58.

14. Xu, Y., Chang, P. F. L., Liu, D., Narasimhan, M. L., Raghothanma, K. G., Gasegawa, P. M. & Bressan, R. A. ( 1994) Plant Cell 6, 1077–1085.

15. Lawton, K. A., Potter, S. L., Uknes, S. & Ryals, J. ( 1994) Plant Cell 6, 581–588.

16. Pieterse, C. M. J., Wees, S. C. M., van Hoffland, E., Pelt, J. A. & van Loon, L. C. ( 1996) Plant Cell 8, 1225–1237.

17. Penninckx, I. A. M. A., Eggermont, K., Terras, F. R. G., Thomma, B. P. H. J., De Samblanx, G. W., Buchala, A., Metraux, J.-P., Manners, J. M. & Broekaert, W. F. ( 1996) Plant Cell 8, 2309–2323.

18. Schmidt, H. H. & Walter, U. ( 1994) Cell 78, 919–925.

19. Stamler, J. S. ( 1994) Cell 78, 931–936.

20. Durner, J. & Klessig, D. F. ( 1999) Curr. Opin. Plant Sci. 2, 369–374.

21. Delledonne, M., Xia, Y., Dixon, R. A. & Lamb, C. ( 1998) Nature ( London) 394, 585–588.

22. Durner, J., Wendehenne, D. & Klessig, D. F. ( 1998) Proc. Natl. Acad. Sci. USA 95, 10328–10333.

23. Chen, Z., Silva, H. & Klessig, D. F. ( 1993) Science 262, 1883–1886.

24. Conrath, U., Chen, Z., Ricigliano, J. W. & Klessig, D. F. ( 1995) Proc. Natl. Acad. Sci. USA 92, 7143–7147.

25. Wendehenne, D., Durner, J., Chen, Z. & Klessig, D. F. ( 1998) Phytochemistry 47, 651–657.

26. Durner, J. & Klessig, D. F. ( 1995) Proc. Natl. Acad. Sci. USA 92, 11312–11316.

27. Du, H. & Klessig, D. F. ( 1997) Mol. Plant–Microbe Interact. 10, 922–925.

28. Takahashi, H., Chen, Z., Du, H., Liu, Y. & Klessig, D. F. ( 1997) Plant J. 11, 993–1005.

29. Bi, Y. M., Kenton, P., Mur, L., Darby, R. & Draper, J. ( 1995) Plant J. 8, 235–245.

30. Neuenschwander, U., Vernooij, B., Friedrich, L., Uknes, S., Kessmann, H. & Ryals, J. ( 1995) Plant J. 8, 227–233.

31. Chamnongpol, S., Willekens, H., Moeder, W., Langebartels, C., Sandermann Jr., H., Van Montagu, M., Inzé, D. & Van Camp, W. ( 1998) Proc. Natl. Acad. Sci. USA 95, 5818–5823.

32. Durner, J. & Klessig, D. F. ( 1996) J. Biol. Chem. 271, 28492–28501.

33. Anderson, M. D., Chen, Z. & Klessig, D. F. ( 1998) Phytochemistry 47, 555–566.

34. Du, H. & Klessig, D. F. ( 1997) Plant Physiol. 113, 1319–1327.

35. Conrath, U., Silva, H. & Klessig, D. F. ( 1997) Plant J. 11, 747–757.

36. Zhang, S. & Klessig, D. F. ( 1997) Plant Cell 9, 809–824.

37. Zhang, S., Du, H. & Klessig, D. F. ( 1998) Plant Cell 10, 435–449.

38. Hoyos, M. E., Zhang, S., Johal, G. S., Klessig, D. F., Hirt, H., Pike, S. M. & Novacky, A. J. ( 1998) Plant Physiol., Suppl., 46–47.

39. Romeis, T., Piedras, P., Zhang, S., Klessig, D. F., Hirt, H. & Jones, J. D. G. ( 1999) Plant Cell 11, 273–287.

40. Zhang, S. & Klessig, D. F. ( 1998) Proc. Natl. Acad. Sci. USA 95, 7433–7438.

41. Zhang, S. & Klessig, D. F. ( 1998) Proc. Natl. Acad. Sci. USA 95, 7225–7230.

42. Seo, S., Okamoto, M., Seto, H., Ishizuka, K., Sano, H. & Ohashi, Y. ( 1995) Science 270, 1988–1992.

43. Zhang, S., Liu, Y. & Klessig, D. F. ( 2000) Plant J., in press.

44. Silva, H., Yoshioka, K., Dooner, H. K. & Klessig, D. F. ( 1999) Mol. PlantMicrobe Interact. 12, 1053–1063.

45. Cao, H., Bowling, S. A., Gordon, A. S. & Dong, X. ( 1994) Plant Cell 6, 1583–1592.

46. Glazebrook, J., Rogers, E. E. & Ausubel, F. M. ( 1996) Genetics 143, 973–982.

47. Delaney, T. P., Friedrich, L. & Ryals, J. A. ( 1995) Proc. Natl. Acad. Sci. USA 92, 6602–6606.

48. Shah, J., Tsui, F. & Klessig, D. F. ( 1997) Mol. Plant–Microbe Interact. 10, 69–78.

49. Cao, H., Glazebrook, J., Clarke, J. D., Volko, S. & Dong, X. ( 1997) Cell 88, 57–63.

50. Ryals, J., Weymann, K., Lawton, K., Friedrich, L., Ellis, D., Steiner, H.-Y., Johnson, J., Delaney, T. P., Jesse, T., Vos, P. & Uknes, S. ( 1997) Plant Cell 9, 425–439.

51. Shah, J., Kachroo, P. & Klessig, D. F. ( 1999) Plant Cell 11, 191–206.

52. Zhou, J.-M., Trifa, Y., Silva, H., Pontier, D., Lam, E., Shah, J. & Klessig, D. F. ( 2000) Mol. Plant–Microbe Interact. 13, 191–202.

53. Lebel, E., Heifetz, P., Thorne, L., Uknes, S., Ryals, J. & Ward, E. ( 1998) Plant J. 16, 223–233.

54. Zhang, Y., Fan, W., Kinkema, M., Li, X. & Dong, X. ( 1999) Proc. Natl. Acad. Sci. USA 96, 6523–6528.

55. Depres, C., DeLong, C., Glaze, S., Liu, E. & Fobert, P. R. ( 2000) Plant Cell 12, 279–290.

56. Malamy, J., Hennig, J. & Klessig, D. F. ( 1992) Plant Cell 4, 359–366.

57. McDonald, L. J. & Murad, F. ( 1995) Adv. Pharmacol. 34, 263–276.

58. Xu, L., Eu, J. P., Meissner, G. & Stamler, J. S. ( 1998) Science 279, 234–237.

59. Murad, F. ( 1994) Adv. Pharmacol. 26, 19–33.

60. Gardner, P. R., Costantino, G., Szabo, C. & Salzman, A. L. ( 1997) J. Biol. Chem. 272, 25071–25076.

61. Domachowske, J. B. ( 1997) Biochem. Mol. Med. 60, 1–7.

62. Navarre, D. A., Wendehenne, D., Durner, J., Noad, R. & Klessig, D. F. ( 2000) Plant Physiol. 122, 573–582.

63. Liochev, S. L. ( 1996) Free Radical Res. 25, 369–384.

64. Rouault, T. & Klausner, R. ( 1997) Curr. Top. Cell. Regul. 35, 1–19.

65. Mott, H. R., Carpenter, J. W. & Campbell, S. L. ( 1997) Biochemistry 36, 3640–3644.



The National Academies | 500 Fifth St. N.W. | Washington, D.C. 20001
Copyright © National Academy of Sciences. All rights reserved.
Terms of Use and Privacy Statement