Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1994 Jun;6(6):863–874. doi: 10.1105/tpc.6.6.863

Immediate early transcription activation by salicylic acid via the cauliflower mosaic virus as-1 element.

X F Qin 1, L Holuigue 1, D M Horvath 1, N H Chua 1
PMCID: PMC160484  PMID: 8061520

Abstract

Transgenic tobacco plants carrying a number of regulatory sequences derived from the cauliflower mosaic virus 35S promoter were tested for their response to treatment with salicylic acid (SA), an endogenous signal involved in plant defense responses. beta-Glucuronidase (GUS) gene fusions with the full-length (-343 to +8) 35S promoter or the -90 truncation were found to be induced by SA. Time course experiments revealed that, in the continuous presence of SA, the -90 promoter construct (-90 35S-GUS) displayed rapid and transient induction kinetics, with maximum RNA levels at 1 to 4 hr, which declined to low levels by 24 hr. Induction was still apparent in the presence of the protein synthesis inhibitor cycloheximide (CHX). Moreover, mRNA levels continued to accumulate over 24 hr rather than to decline. By contrast, mRNA from the endogenous pathogenesis-related protein-1a (PR-1a) gene began to accumulate at later times during SA treatment and steadily increased through 24 hr; transcription of this gene was almost completely blocked by the presence of CHX. Further dissection of the region from -90 and -46 of the 35S promoter revealed that the SA-responsive element corresponds to the previously characterized activation sequence-1 (as-1). These results represent a definitive analysis of immediate early responses to SA, relative to the late induction of PR genes, and potentially elucidate the early events of SA signal transduction during the plant defense response.

Full Text

The Full Text of this article is available as a PDF (2.9 MB).

Selected References

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

  1. Benfey P. N., Chua N. H. The Cauliflower Mosaic Virus 35S Promoter: Combinatorial Regulation of Transcription in Plants. Science. 1990 Nov 16;250(4983):959–966. doi: 10.1126/science.250.4983.959. [DOI] [PubMed] [Google Scholar]
  2. Benfey P. N., Ren L., Chua N. H. Tissue-specific expression from CaMV 35S enhancer subdomains in early stages of plant development. EMBO J. 1990 Jun;9(6):1677–1684. doi: 10.1002/j.1460-2075.1990.tb08291.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bouchez D., Tokuhisa J. G., Llewellyn D. J., Dennis E. S., Ellis J. G. The ocs-element is a component of the promoters of several T-DNA and plant viral genes. EMBO J. 1989 Dec 20;8(13):4197–4204. doi: 10.1002/j.1460-2075.1989.tb08605.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chen Z., Silva H., Klessig D. F. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science. 1993 Dec 17;262(5141):1883–1886. doi: 10.1126/science.8266079. [DOI] [PubMed] [Google Scholar]
  5. Dietrich A., Mayer J. E., Hahlbrock K. Fungal elicitor triggers rapid, transient, and specific protein phosphorylation in parsley cell suspension cultures. J Biol Chem. 1990 Apr 15;265(11):6360–6368. [PubMed] [Google Scholar]
  6. Enyedi A. J., Yalpani N., Silverman P., Raskin I. Signal molecules in systemic plant resistance to pathogens and pests. Cell. 1992 Sep 18;70(6):879–886. doi: 10.1016/0092-8674(92)90239-9. [DOI] [PubMed] [Google Scholar]
  7. Fang R. X., Nagy F., Sivasubramaniam S., Chua N. H. Multiple cis regulatory elements for maximal expression of the cauliflower mosaic virus 35S promoter in transgenic plants. Plant Cell. 1989 Jan;1(1):141–150. doi: 10.1105/tpc.1.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fromm H., Katagiri F., Chua N. H. An octopine synthase enhancer element directs tissue-specific expression and binds ASF-1, a factor from tobacco nuclear extracts. Plant Cell. 1989 Oct;1(10):977–984. doi: 10.1105/tpc.1.10.977. [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. Greenberg M. E., Hermanowski A. L., Ziff E. B. Effect of protein synthesis inhibitors on growth factor activation of c-fos, c-myc, and actin gene transcription. Mol Cell Biol. 1986 Apr;6(4):1050–1057. doi: 10.1128/mcb.6.4.1050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hagiwara M., Alberts A., Brindle P., Meinkoth J., Feramisco J., Deng T., Karin M., Shenolikar S., Montminy M. Transcriptional attenuation following cAMP induction requires PP-1-mediated dephosphorylation of CREB. Cell. 1992 Jul 10;70(1):105–113. doi: 10.1016/0092-8674(92)90537-m. [DOI] [PubMed] [Google Scholar]
  12. Hennig J., Malamy J., Grynkiewicz G., Indulski J., Klessig D. F. Interconversion of the salicylic acid signal and its glucoside in tobacco. Plant J. 1993 Oct;4(4):593–600. doi: 10.1046/j.1365-313x.1993.04040593.x. [DOI] [PubMed] [Google Scholar]
  13. Jefferson R. A., Kavanagh T. A., Bevan M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 1987 Dec 20;6(13):3901–3907. doi: 10.1002/j.1460-2075.1987.tb02730.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kim S. R., Kim Y., An G. Identification of methyl jasmonate and salicylic acid response elements from the nopaline synthase (nos) promoter. Plant Physiol. 1993 Sep;103(1):97–103. doi: 10.1104/pp.103.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lam E., Benfey P. N., Gilmartin P. M., Fang R. X., Chua N. H. Site-specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7890–7894. doi: 10.1073/pnas.86.20.7890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lam E., Katagiri F., Chua N. H. Plant nuclear factor ASF-1 binds to an essential region of the nopaline synthase promoter. J Biol Chem. 1990 Jun 15;265(17):9909–9913. [PubMed] [Google Scholar]
  17. Mahadevan L. C., Edwards D. R. Signalling and superinduction. Nature. 1991 Feb 28;349(6312):747–748. doi: 10.1038/349747c0. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Memelink J., Hoge J. H., Schilperoort R. A. Cytokinin stress changes the developmental regulation of several defence-related genes in tobacco. EMBO J. 1987 Dec 1;6(12):3579–3583. doi: 10.1002/j.1460-2075.1987.tb02688.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Métraux J. P., Signer H., Ryals J., Ward E., Wyss-Benz M., Gaudin J., Raschdorf K., Schmid E., Blum W., Inverardi B. Increase in salicylic Acid at the onset of systemic acquired resistance in cucumber. Science. 1990 Nov 16;250(4983):1004–1006. doi: 10.1126/science.250.4983.1004. [DOI] [PubMed] [Google Scholar]
  21. Ohshima M., Itoh H., Matsuoka M., Murakami T., Ohashi Y. Analysis of stress-induced or salicylic acid-induced expression of the pathogenesis-related 1a protein gene in transgenic tobacco. Plant Cell. 1990 Feb;2(2):95–106. doi: 10.1105/tpc.2.2.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rao P., Mufson R. A. Interleukin-3 inhibits cycloheximide induction of C-jun mRNA in human monocytes: possible role for a serine/threonine phosphatase. J Cell Physiol. 1993 Sep;156(3):560–566. doi: 10.1002/jcp.1041560315. [DOI] [PubMed] [Google Scholar]
  23. Shuai K., Schindler C., Prezioso V. R., Darnell J. E., Jr Activation of transcription by IFN-gamma: tyrosine phosphorylation of a 91-kD DNA binding protein. Science. 1992 Dec 11;258(5089):1808–1812. doi: 10.1126/science.1281555. [DOI] [PubMed] [Google Scholar]
  24. Uknes S., Dincher S., Friedrich L., Negrotto D., Williams S., Thompson-Taylor H., Potter S., Ward E., Ryals J. Regulation of pathogenesis-related protein-1a gene expression in tobacco. Plant Cell. 1993 Feb;5(2):159–169. doi: 10.1105/tpc.5.2.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ward E. R., Uknes S. J., Williams S. C., Dincher S. S., Wiederhold D. L., Alexander D. C., Ahl-Goy P., Metraux J. P., Ryals J. A. Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance. Plant Cell. 1991 Oct;3(10):1085–1094. doi: 10.1105/tpc.3.10.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yalpani N., Balke N. E., Schulz M. Induction of UDP-Glucose:Salicylic Acid Glucosyltransferase in Oat Roots. Plant Physiol. 1992 Nov;100(3):1114–1119. doi: 10.1104/pp.100.3.1114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Yalpani N., Raskin I. Salicylic acid: a systemic signal in induced plant disease resistance. Trends Microbiol. 1993 Jun;1(3):88–92. doi: 10.1016/0966-842x(93)90113-6. [DOI] [PubMed] [Google Scholar]
  28. Yalpani N., Schulz M., Davis M. P., Balke N. E. Partial purification and properties of an inducible uridine 5'-diphosphate-glucose-salicylic Acid glucosyltransferase from oat roots. Plant Physiol. 1992 Sep;100(1):457–463. doi: 10.1104/pp.100.1.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Zinck R., Hipskind R. A., Pingoud V., Nordheim A. c-fos transcriptional activation and repression correlate temporally with the phosphorylation status of TCF. EMBO J. 1993 Jun;12(6):2377–2387. doi: 10.1002/j.1460-2075.1993.tb05892.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Zipfel P. F., Irving S. G., Kelly K., Siebenlist U. Complexity of the primary genetic response to mitogenic activation of human T cells. Mol Cell Biol. 1989 Mar;9(3):1041–1048. doi: 10.1128/mcb.9.3.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. van de Rhee M. D., Lemmers R., Bol J. F. Analysis of regulatory elements involved in stress-induced and organ-specific expression of tobacco acidic and basic beta-1,3-glucanase genes. Plant Mol Biol. 1993 Feb;21(3):451–461. doi: 10.1007/BF00028803. [DOI] [PubMed] [Google Scholar]

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

RESOURCES