Uncoupling salicylic acid-dependent cell death and defense-related responses from disease resistance in the Arabidopsis mutant acd5 (original) (raw)

Abstract

Salicylic acid (SA) is required for resistance to many diseases in higher plants. SA-dependent cell death and defense-related responses have been correlated with disease resistance. The accelerated cell death 5 mutant of Arabidopsis provides additional genetic evidence that SA regulates cell death and defense-related responses. However, in acd5, these events are uncoupled from disease resistance. acd5 plants are more susceptible to Pseudomonas syringae early in development and show spontaneous SA accumulation, cell death, and defense-related markers later in development. In acd5 plants, cell death and defense-related responses are SA dependent but they do not confer disease resistance. Double mutants with acd5 and nonexpressor of PR1, in which SA signaling is partially blocked, show greatly attenuated cell death, indicating a role for NPR1 in controlling cell death. The hormone ethylene potentiates the effects of SA and is important for disease symptom development in Arabidopsis. Double mutants of acd5 and ethylene insensitive 2, in which ethylene signaling is blocked, show decreased cell death, supporting a role for ethylene in cell death control. We propose that acd5 plants mimic P. syringae-infected wild-type plants and that both SA and ethylene are normally involved in regulating cell death during some susceptible pathogen infections.

Full Text

The Full Text of this article is available as a PDF (505.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aarts N., Metz M., Holub E., Staskawicz B. J., Daniels M. J., Parker J. E. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10306–10311. doi: 10.1073/pnas.95.17.10306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bent A. F., Innes R. W., Ecker J. R., Staskawicz B. J. Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens. Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):372–378. doi: 10.1094/mpmi-5-372. [DOI] [PubMed] [Google Scholar]
  3. Bowling S. A., Guo A., Cao H., Gordon A. S., Klessig D. F., Dong X. A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell. 1994 Dec;6(12):1845–1857. doi: 10.1105/tpc.6.12.1845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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. 1994 Nov;6(11):1583–1592. doi: 10.1105/tpc.6.11.1583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cao H., Glazebrook J., Clarke J. D., Volko S., Dong X. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell. 1997 Jan 10;88(1):57–63. doi: 10.1016/s0092-8674(00)81858-9. [DOI] [PubMed] [Google Scholar]
  6. Century K. S., Shapiro A. D., Repetti P. P., Dahlbeck D., Holub E., Staskawicz B. J. NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science. 1997 Dec 12;278(5345):1963–1965. doi: 10.1126/science.278.5345.1963. [DOI] [PubMed] [Google Scholar]
  7. Delaney T. P., Friedrich L., Ryals J. A. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6602–6606. doi: 10.1073/pnas.92.14.6602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dietrich R. A., Delaney T. P., Uknes S. J., Ward E. R., Ryals J. A., Dangl J. L. Arabidopsis mutants simulating disease resistance response. Cell. 1994 May 20;77(4):565–577. doi: 10.1016/0092-8674(94)90218-6. [DOI] [PubMed] [Google Scholar]
  9. Glazebrook J., Ausubel F. M. Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8955–8959. doi: 10.1073/pnas.91.19.8955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Greenberg J. T., Guo A., Klessig D. F., Ausubel F. M. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell. 1994 May 20;77(4):551–563. doi: 10.1016/0092-8674(94)90217-8. [DOI] [PubMed] [Google Scholar]
  11. Greenberg Jean T. PROGRAMMED CELL DEATH IN PLANT-PATHOGEN INTERACTIONS. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):525–545. doi: 10.1146/annurev.arplant.48.1.525. [DOI] [PubMed] [Google Scholar]
  12. Guzmán P., Ecker J. R. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell. 1990 Jun;2(6):513–523. doi: 10.1105/tpc.2.6.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Konieczny A., Ausubel F. M. A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 1993 Aug;4(2):403–410. doi: 10.1046/j.1365-313x.1993.04020403.x. [DOI] [PubMed] [Google Scholar]
  14. Rao M. V., Davis K. R. Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J. 1999 Mar;17(6):603–614. doi: 10.1046/j.1365-313x.1999.00400.x. [DOI] [PubMed] [Google Scholar]
  15. Rate D. N., Cuenca J. V., Bowman G. R., Guttman D. S., Greenberg J. T. The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. Plant Cell. 1999 Sep;11(9):1695–1708. doi: 10.1105/tpc.11.9.1695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ryals J. A., Neuenschwander U. H., Willits M. G., Molina A., Steiner H. Y., Hunt M. D. Systemic Acquired Resistance. Plant Cell. 1996 Oct;8(10):1809–1819. doi: 10.1105/tpc.8.10.1809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Sharma Y. K., Davis K. R. The effects of ozone on antioxidant responses in plants. Free Radic Biol Med. 1997;23(3):480–488. doi: 10.1016/s0891-5849(97)00108-1. [DOI] [PubMed] [Google Scholar]
  18. Silva H., Yoshioka K., Dooner H. K., Klessig D. F. Characterization of a new Arabidopsis mutant exhibiting enhanced disease resistance. Mol Plant Microbe Interact. 1999 Dec;12(12):1053–1063. doi: 10.1094/MPMI.1999.12.12.1053. [DOI] [PubMed] [Google Scholar]
  19. Thomma B. P., Nelissen I., Eggermont K., Broekaert W. F. Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant J. 1999 Jul;19(2):163–171. doi: 10.1046/j.1365-313x.1999.00513.x. [DOI] [PubMed] [Google Scholar]
  20. Weymann K., Hunt M., Uknes S., Neuenschwander U., Lawton K., Steiner H. Y., Ryals J. Suppression and Restoration of Lesion Formation in Arabidopsis lsd Mutants. Plant Cell. 1995 Dec;7(12):2013–2022. doi: 10.1105/tpc.7.12.2013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Yu I. C., Parker J., Bent A. F. Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7819–7824. doi: 10.1073/pnas.95.13.7819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Zhou N., Tootle T. L., Tsui F., Klessig D. F., Glazebrook J. PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell. 1998 Jun;10(6):1021–1030. doi: 10.1105/tpc.10.6.1021. [DOI] [PMC free article] [PubMed] [Google Scholar]