Skip to main content

Some NLM-NCBI services and products are experiencing heavy traffic, which may affect performance and availability. We apologize for the inconvenience and appreciate your patience. For assistance, please contact our Help Desk at info@ncbi.nlm.nih.gov.

The Plant Cell logoLink to The Plant Cell
. 1998 Jun;10(6):1021–1030. doi: 10.1105/tpc.10.6.1021

PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis.

N Zhou 1, T L Tootle 1, F Tsui 1, D F Klessig 1, J Glazebrook 1
PMCID: PMC144042  PMID: 9634589

Abstract

The Arabidopsis PAD4 gene was previously shown to be required for synthesis of camalexin in response to infection by the virulent bacterial pathogen Pseudomonas syringae pv maculicola ES4326 but not in response to challenge by the non-host fungal pathogen Cochliobolus carbonum. In this study, we show that pad4 mutants exhibit defects in defense responses, including camalexin synthesis and pathogenesis-related PR-1 gene expression, when infected by P. s. maculicola ES4 326. No such defects were observed in response to infection by an isogenic avirulent strain carrying the avirulence gene avrRpt2. In P. s. maculicola ES4 326-infected pad4 plants, synthesis of salicylic acid (SA) was found to be reduced and delayed when compared with SA synthesis in wild-type plants. Moreover, treatment of pad4 plants with SA partially reversed the camalexin deficiency and PR-1 gene expression phenotypes of P. s. maculicola ES4 326-infected pad4 plants. These findings support the hypothesis that PAD4 acts upstream from SA accumulation in regulating defense response expression in plants infected with P. s. maculicola ES4 326. A working model of the role of PAD4 in governing expression of defense responses is presented.

Full Text

The Full Text of this article is available as a PDF (198.9 KB).

Selected References

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

  1. Beffa R., Szell M., Meuwly P., Pay A., Vögeli-Lange R., Métraux J. P., Neuhaus G., Meins F., Jr, Nagy F. Cholera toxin elevates pathogen resistance and induces pathogenesis-related gene expression in tobacco. EMBO J. 1995 Dec 1;14(23):5753–5761. doi: 10.1002/j.1460-2075.1995.tb00264.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. 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]
  5. Cuppels D. A. Generation and Characterization of Tn5 Insertion Mutations in Pseudomonas syringae pv. tomato. Appl Environ Microbiol. 1986 Feb;51(2):323–327. doi: 10.1128/aem.51.2.323-327.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Delaney T. P., Uknes S., Vernooij B., Friedrich L., Weymann K., Negrotto D., Gaffney T., Gut-Rella M., Kessmann H., Ward E., Ryals J. A central role of salicylic Acid in plant disease resistance. Science. 1994 Nov 18;266(5188):1247–1250. doi: 10.1126/science.266.5188.1247. [DOI] [PubMed] [Google Scholar]
  8. Dong X., Mindrinos M., Davis K. R., Ausubel F. M. Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell. 1991 Jan;3(1):61–72. doi: 10.1105/tpc.3.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gaffney T., Friedrich L., Vernooij B., Negrotto D., Nye G., Uknes S., Ward E., Kessmann H., Ryals J. Requirement of salicylic Acid for the induction of systemic acquired resistance. Science. 1993 Aug 6;261(5122):754–756. doi: 10.1126/science.261.5122.754. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Glazebrook J., Rogers E. E., Ausubel F. M. Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics. 1996 Jun;143(2):973–982. doi: 10.1093/genetics/143.2.973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Glazebrook J., Rogers E. E., Ausubel F. M. Use of Arabidopsis for genetic dissection of plant defense responses. Annu Rev Genet. 1997;31:547–569. doi: 10.1146/annurev.genet.31.1.547. [DOI] [PubMed] [Google Scholar]
  13. Glazebrook J., Zook M., Mert F., Kagan I., Rogers E. E., Crute I. R., Holub E. B., Hammerschmidt R., Ausubel F. M. Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics. 1997 May;146(1):381–392. doi: 10.1093/genetics/146.1.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. Lawton K., Weymann K., Friedrich L., Vernooij B., Uknes S., Ryals J. Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant Microbe Interact. 1995 Nov-Dec;8(6):863–870. doi: 10.1094/mpmi-8-0863. [DOI] [PubMed] [Google Scholar]
  17. Malamy J., Carr J. P., Klessig D. F., Raskin I. Salicylic Acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science. 1990 Nov 16;250(4983):1002–1004. doi: 10.1126/science.250.4983.1002. [DOI] [PubMed] [Google Scholar]
  18. Molders W., Buchala A., Metraux J. P. Transport of Salicylic Acid in Tobacco Necrosis Virus-Infected Cucumber Plants. Plant Physiol. 1996 Oct;112(2):787–792. doi: 10.1104/pp.112.2.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Niyogi K. K., Fink G. R. Two anthranilate synthase genes in Arabidopsis: defense-related regulation of the tryptophan pathway. Plant Cell. 1992 Jun;4(6):721–733. doi: 10.1105/tpc.4.6.721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Parker J. E., Holub E. B., Frost L. N., Falk A., Gunn N. D., Daniels M. J. Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell. 1996 Nov;8(11):2033–2046. doi: 10.1105/tpc.8.11.2033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Reuber T. L., Ausubel F. M. Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes. Plant Cell. 1996 Feb;8(2):241–249. doi: 10.1105/tpc.8.2.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ritter C., Dangl J. L. Interference between Two Specific Pathogen Recognition Events Mediated by Distinct Plant Disease Resistance Genes. Plant Cell. 1996 Feb;8(2):251–257. doi: 10.1105/tpc.8.2.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rogers E. E., Ausubel F. M. Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. Plant Cell. 1997 Mar;9(3):305–316. doi: 10.1105/tpc.9.3.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Ryals J., Weymann K., Lawton K., Friedrich L., Ellis D., Steiner H. Y., Johnson J., Delaney T. P., Jesse T., Vos P. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B. Plant Cell. 1997 Mar;9(3):425–439. doi: 10.1105/tpc.9.3.425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shah J., Tsui F., Klessig D. F. Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol Plant Microbe Interact. 1997 Jan;10(1):69–78. doi: 10.1094/MPMI.1997.10.1.69. [DOI] [PubMed] [Google Scholar]
  27. Shirasu K., Nakajima H., Rajasekhar V. K., Dixon R. A., Lamb C. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell. 1997 Feb;9(2):261–270. doi: 10.1105/tpc.9.2.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shulaev V., Leon J., Raskin I. Is Salicylic Acid a Translocated Signal of Systemic Acquired Resistance in Tobacco? Plant Cell. 1995 Oct;7(10):1691–1701. doi: 10.1105/tpc.7.10.1691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Uknes S., Mauch-Mani B., Moyer M., Potter S., Williams S., Dincher S., Chandler D., Slusarenko A., Ward E., Ryals J. Acquired resistance in Arabidopsis. Plant Cell. 1992 Jun;4(6):645–656. doi: 10.1105/tpc.4.6.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Vernooij B., Friedrich L., Morse A., Reist R., Kolditz-Jawhar R., Ward E., Uknes S., Kessmann H., Ryals J. Salicylic Acid Is Not the Translocated Signal Responsible for Inducing Systemic Acquired Resistance but Is Required in Signal Transduction. Plant Cell. 1994 Jul;6(7):959–965. doi: 10.1105/tpc.6.7.959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Weiss B. D., Capage M. A., Kessel M., Benson S. A. Isolation and characterization of a generalized transducing phage for Xanthomonas campestris pv. campestris. J Bacteriol. 1994 Jun;176(11):3354–3359. doi: 10.1128/jb.176.11.3354-3359.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Whalen M. C., Innes R. W., Bent A. F., Staskawicz B. J. Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell. 1991 Jan;3(1):49–59. doi: 10.1105/tpc.3.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Zhao J., Last R. L. Coordinate regulation of the tryptophan biosynthetic pathway and indolic phytoalexin accumulation in Arabidopsis. Plant Cell. 1996 Dec;8(12):2235–2244. doi: 10.1105/tpc.8.12.2235. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES