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. 1998 Feb 15;330(Pt 1):115–120. doi: 10.1042/bj3300115

Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defence gene expression in Arabidopsis suspension cultures.

R Desikan 1, A Reynolds 1, J T Hancock 1, S J Neill 1
PMCID: PMC1219116  PMID: 9461499

Abstract

Programmed cell death is increasingly viewed as a key component of the hypersensitive disease resistance response of plants. The generation of reactive oxygen species (ROS) such as H2O2 triggers a cell death programme in Arabidopsis suspension cultures following challenge with the bacterial elicitor harpin. Both harpin and exogenous H2O2 initiate a cell death pathway that requires gene expression, and also act as signalling molecules to induce the expression of plant defence genes encoding enzymes such as phenylalanine ammonia-lyase (PAL), glutathione S-transferase (GST) and anthranilate synthase (ASA1), an enzyme of phytoalexin biosynthesis in Arabidopsis. H2O2 induces the expression of PAL1 and GST but not that of ASA1. Harpin initiates two signalling pathways, one leading to increased ROS generation and expression of PAL1 and GST mRNA, and another leading to increased GST and ASA1 expression, independent of H2O2.

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Selected References

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  1. Alfano J. R., Bauer D. W., Milos T. M., Collmer A. Analysis of the role of the Pseudomonas syringae pv. syringae HrpZ harpin in elicitation of the hypersensitive response in tobacco using functionally non-polar hrpZ deletion mutations, truncated HrpZ fragments, and hrmA mutations. Mol Microbiol. 1996 Feb;19(4):715–728. doi: 10.1046/j.1365-2958.1996.415946.x. [DOI] [PubMed] [Google Scholar]
  2. Auh C. K., Murphy T. M. Plasma Membrane Redox Enzyme Is Involved in the Synthesis of O2- and H2O2 by Phytophthora Elicitor-Stimulated Rose Cells. Plant Physiol. 1995 Apr;107(4):1241–1247. doi: 10.1104/pp.107.4.1241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baldwin A. S., Jr, Sharp P. A. Two transcription factors, NF-kappa B and H2TF1, interact with a single regulatory sequence in the class I major histocompatibility complex promoter. Proc Natl Acad Sci U S A. 1988 Feb;85(3):723–727. doi: 10.1073/pnas.85.3.723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berhane K., Widersten M., Engström A., Kozarich J. W., Mannervik B. Detoxication of base propenals and other alpha, beta-unsaturated aldehyde products of radical reactions and lipid peroxidation by human glutathione transferases. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1480–1484. doi: 10.1073/pnas.91.4.1480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bestwick C. S., Brown I. R., Bennett M. H., Mansfield J. W. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell. 1997 Feb;9(2):209–221. doi: 10.1105/tpc.9.2.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bolwell G. P., Butt V. S., Davies D. R., Zimmerlin A. The origin of the oxidative burst in plants. Free Radic Res. 1995 Dec;23(6):517–532. doi: 10.3109/10715769509065273. [DOI] [PubMed] [Google Scholar]
  7. Chen W., Chao G., Singh K. B. The promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. Plant J. 1996 Dec;10(6):955–966. doi: 10.1046/j.1365-313x.1996.10060955.x. [DOI] [PubMed] [Google Scholar]
  8. Dangl J. L., Dietrich R. A., Richberg M. H. Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. Plant Cell. 1996 Oct;8(10):1793–1807. doi: 10.1105/tpc.8.10.1793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Desikan R., Hancock J. T., Coffey M. J., Neill S. J. Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme. FEBS Lett. 1996 Mar 11;382(1-2):213–217. doi: 10.1016/0014-5793(96)00177-9. [DOI] [PubMed] [Google Scholar]
  10. Dietrich R. A., Richberg M. H., Schmidt R., Dean C., Dangl J. L. A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell. 1997 Mar 7;88(5):685–694. doi: 10.1016/s0092-8674(00)81911-x. [DOI] [PubMed] [Google Scholar]
  11. Dwyer S. C., Legendre L., Low P. S., Leto T. L. Plant and human neutrophil oxidative burst complexes contain immunologically related proteins. Biochim Biophys Acta. 1996 Mar 15;1289(2):231–237. doi: 10.1016/0304-4165(95)00156-5. [DOI] [PubMed] [Google Scholar]
  12. Glazener J. A., Orlandi E. W., Baker C. J. The Active Oxygen Response of Cell Suspensions to Incompatible Bacteria Is Not Sufficient to Cause Hypersensitive Cell Death. Plant Physiol. 1996 Mar;110(3):759–763. doi: 10.1104/pp.110.3.759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Groom Q. J., Torres M. A., Fordham-Skelton A. P., Hammond-Kosack K. E., Robinson N. J., Jones J. D. rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. Plant J. 1996 Sep;10(3):515–522. doi: 10.1046/j.1365-313x.1996.10030515.x. [DOI] [PubMed] [Google Scholar]
  14. He S. Y. Elicitation of Plant Hypersensitive Response by Bacteria. Plant Physiol. 1996 Nov;112(3):865–869. doi: 10.1104/pp.112.3.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. He S. Y., Huang H. C., Collmer A. Pseudomonas syringae pv. syringae harpinPss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell. 1993 Jul 2;73(7):1255–1266. doi: 10.1016/0092-8674(93)90354-s. [DOI] [PubMed] [Google Scholar]
  16. Hirst A. D., Stevens J. F. Electrodes in clinical chemistry. Ann Clin Biochem. 1985 Sep;22(Pt 5):460–488. doi: 10.1177/000456328502200503. [DOI] [PubMed] [Google Scholar]
  17. Jabs T., Dietrich R. A., Dangl J. L. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science. 1996 Sep 27;273(5283):1853–1856. doi: 10.1126/science.273.5283.1853. [DOI] [PubMed] [Google Scholar]
  18. Jabs T., Tschope M., Colling C., Hahlbrock K., Scheel D. Elicitor-stimulated ion fluxes and O2- from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc Natl Acad Sci U S A. 1997 Apr 29;94(9):4800–4805. doi: 10.1073/pnas.94.9.4800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jacobson M. D. Reactive oxygen species and programmed cell death. Trends Biochem Sci. 1996 Mar;21(3):83–86. [PubMed] [Google Scholar]
  20. Kieffer F., Simon-Plas F., Maume B. F., Blein J. P. Tobacco cells contain a protein, immunologically related to the neutrophil small G protein Rac2 and involved in elicitor-induced oxidative burst. FEBS Lett. 1997 Feb 17;403(2):149–153. doi: 10.1016/s0014-5793(97)00038-0. [DOI] [PubMed] [Google Scholar]
  21. Kiyosue T., Yamaguchi-Shinozaki K., Shinozaki K. Characterization of two cDNAs (ERD11 and ERD13) for dehydration-inducible genes that encode putative glutathione S-transferases in Arabidopsis thaliana L. FEBS Lett. 1993 Dec 6;335(2):189–192. doi: 10.1016/0014-5793(93)80727-c. [DOI] [PubMed] [Google Scholar]
  22. Levine A., Pennell R. I., Alvarez M. E., Palmer R., Lamb C. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr Biol. 1996 Apr 1;6(4):427–437. doi: 10.1016/s0960-9822(02)00510-9. [DOI] [PubMed] [Google Scholar]
  23. Levine A., Tenhaken R., Dixon R., Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994 Nov 18;79(4):583–593. doi: 10.1016/0092-8674(94)90544-4. [DOI] [PubMed] [Google Scholar]
  24. Mauch-Mani B., Slusarenko A. J. Production of Salicylic Acid Precursors Is a Major Function of Phenylalanine Ammonia-Lyase in the Resistance of Arabidopsis to Peronospora parasitica. Plant Cell. 1996 Feb;8(2):203–212. doi: 10.1105/tpc.8.2.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mittler R., Lam E. Sacrifice in the face of foes: pathogen-induced programmed cell death in plants. Trends Microbiol. 1996 Jan;4(1):10–15. doi: 10.1016/0966-842x(96)81499-5. [DOI] [PubMed] [Google Scholar]
  26. Mittler R., Shulaev V., Seskar M., Lam E. Inhibition of Programmed Cell Death in Tobacco Plants during a Pathogen-Induced Hypersensitive Response at Low Oxygen Pressure. Plant Cell. 1996 Nov;8(11):1991–2001. doi: 10.1105/tpc.8.11.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Ohl S., Hedrick S. A., Chory J., Lamb C. J. Functional properties of a phenylalanine ammonia-lyase promoter from Arabidopsis. Plant Cell. 1990 Sep;2(9):837–848. doi: 10.1105/tpc.2.9.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pickett C. B., Lu A. Y. Glutathione S-transferases: gene structure, regulation, and biological function. Annu Rev Biochem. 1989;58:743–764. doi: 10.1146/annurev.bi.58.070189.003523. [DOI] [PubMed] [Google Scholar]
  30. Rogers K. R., Albert F., Anderson A. J. Lipid peroxidation is a consequence of elicitor activity. Plant Physiol. 1988 Feb;86(2):547–553. doi: 10.1104/pp.86.2.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rusterucci C., Stallaert V., Milat M. L., Pugin A., Ricci P., Blein J. P. Relationship between Active Oxygen Species, Lipid Peroxidation, Necrosis, and Phytoalexin Production Induced by Elicitins in Nicotiana. Plant Physiol. 1996 Jul;111(3):885–891. doi: 10.1104/pp.111.3.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Ryerson D. E., Heath M. C. Cleavage of Nuclear DNA into Oligonucleosomal Fragments during Cell Death Induced by Fungal Infection or by Abiotic Treatments. Plant Cell. 1996 Mar;8(3):393–402. doi: 10.1105/tpc.8.3.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schreck R., Rieber P., Baeuerle P. A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 1991 Aug;10(8):2247–2258. doi: 10.1002/j.1460-2075.1991.tb07761.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sharma Y. K., Léon J., Raskin I., Davis K. R. Ozone-induced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defense-related transcripts and induced resistance. Proc Natl Acad Sci U S A. 1996 May 14;93(10):5099–5104. doi: 10.1073/pnas.93.10.5099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sugimoto A., Hozak R. R., Nakashima T., Nishimoto T., Rothman J. H. dad-1, an endogenous programmed cell death suppressor in Caenorhabditis elegans and vertebrates. EMBO J. 1995 Sep 15;14(18):4434–4441. doi: 10.1002/j.1460-2075.1995.tb00122.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tsuji J., Jackson E. P., Gage D. A., Hammerschmidt R., Somerville S. C. Phytoalexin Accumulation in Arabidopsis thaliana during the Hypersensitive Reaction to Pseudomonas syringae pv syringae. Plant Physiol. 1992 Apr;98(4):1304–1309. doi: 10.1104/pp.98.4.1304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Vaux D. L., Strasser A. The molecular biology of apoptosis. Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2239–2244. doi: 10.1073/pnas.93.6.2239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wang H., Li J., Bostock R. M., Gilchrist D. G. Apoptosis: A Functional Paradigm for Programmed Plant Cell Death Induced by a Host-Selective Phytotoxin and Invoked during Development. Plant Cell. 1996 Mar;8(3):375–391. doi: 10.1105/tpc.8.3.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Williams J., Bulman M., Huttly A., Phillips A., Neill S. Characterization of a cDNA from Arabidopsis thaliana encoding a potential thiol protease whose expression is induced independently by wilting and abscisic acid. Plant Mol Biol. 1994 May;25(2):259–270. doi: 10.1007/BF00023242. [DOI] [PubMed] [Google Scholar]
  41. Wojtaszek P. Oxidative burst: an early plant response to pathogen infection. Biochem J. 1997 Mar 15;322(Pt 3):681–692. doi: 10.1042/bj3220681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Xing T., Higgins V. J., Blumwald E. Race-specific elicitors of Cladosporium fulvum promote translocation of cytosolic components of NADPH oxidase to the plasma membrane of tomato cells. Plant Cell. 1997 Feb;9(2):249–259. doi: 10.1105/tpc.9.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]

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