Abstract
Changes in gene expression induced in tobacco leaves by the harpin HrpN protein elicitor were examined, and a new cDNA, piox (for pathogen-induced oxygenase), with homology to genes encoding cyclooxygenase or prostaglandin endoperoxide synthase (PGHS), was identified. In addition to the amino acid identity determined, the protein encoded by piox is predicted to have a structural core similar to that of ovine PGHS-1. Moreover, studies of protein functionality demonstrate that the PIOX recombinant protein possesses at least one of the two enzymatic activities of PGHSs, that of catalyzing the oxygenation of polyunsaturated fatty acids. piox transcripts accumulated after protein elicitor treatment or inoculation with bacteria. Expression of piox was induced in tissues responding to inoculation with both incompatible and compatible bacteria, but RNA and protein accumulation differed for both types of interactions. We show that expression of piox is rapidly induced in response to various cellular signals mediating plant responses to pathogen infection and that activation of piox expression is most likely related to the oxidative burst that takes place during the cell death processes examined. Cyclooxygenase catalyzes the first committed step in the formation of prostaglandins and thromboxanes, which are lipid-derived signal molecules that mediate many cellular processes, including the immune response in vertebrates. The finding of tobacco PIOX suggests that more similarities than hitherto expected will be found between the lipid-based responses for plant and animal systems.
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- Alfano J. R., Collmer A. Bacterial Pathogens in Plants: Life up against the Wall. Plant Cell. 1996 Oct;8(10):1683–1698. doi: 10.1105/tpc.8.10.1683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Alfano J. R., Klm H. S., Delaney T. P., Collmer A. Evidence that the Pseudomonas syringae pv. syringae hrp-linked hrmA gene encodes an Avr-like protein that acts in an hrp-dependent manner within tobacco cells. Mol Plant Microbe Interact. 1997 Jul;10(5):580–588. doi: 10.1094/MPMI.1997.10.5.580. [DOI] [PubMed] [Google Scholar]
- Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
- Baker C. J., Orlandi E. W., Mock N. M. Harpin, An Elicitor of the Hypersensitive Response in Tobacco Caused by Erwinia amylovora, Elicits Active Oxygen Production in Suspension Cells. Plant Physiol. 1993 Aug;102(4):1341–1344. doi: 10.1104/pp.102.4.1341. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bergey D. R., Howe G. A., Ryan C. A. Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12053–12058. doi: 10.1073/pnas.93.22.12053. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
- Chandra S., Martin G. B., Low P. S. The Pto kinase mediates a signaling pathway leading to the oxidative burst in tomato. Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13393–13397. doi: 10.1073/pnas.93.23.13393. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen Z., Malamy J., Henning J., Conrath U., Sánchez-Casas P., Silva H., Ricigliano J., Klessig D. K. Induction, modification, and transduction of the salicylic acid signal in plant defense responses. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4134–4137. doi: 10.1073/pnas.92.10.4134. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Croft KPC., Juttner F., Slusarenko A. J. Volatile Products of the Lipoxygenase Pathway Evolved from Phaseolus vulgaris (L.) Leaves Inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiol. 1993 Jan;101(1):13–24. doi: 10.1104/pp.101.1.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeWitt D. L., Smith W. L. Primary structure of prostaglandin G/H synthase from sheep vesicular gland determined from the complementary DNA sequence. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1412–1416. doi: 10.1073/pnas.85.5.1412. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeWitt D. L., el-Harith E. A., Kraemer S. A., Andrews M. J., Yao E. F., Armstrong R. L., Smith W. L. The aspirin and heme-binding sites of ovine and murine prostaglandin endoperoxide synthases. J Biol Chem. 1990 Mar 25;265(9):5192–5198. [PubMed] [Google Scholar]
- 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]
- Farmer E. E., Ryan C. A. Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7713–7716. doi: 10.1073/pnas.87.19.7713. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Feng L., Sun W., Xia Y., Tang W. W., Chanmugam P., Soyoola E., Wilson C. B., Hwang D. Cloning two isoforms of rat cyclooxygenase: differential regulation of their expression. Arch Biochem Biophys. 1993 Dec;307(2):361–368. doi: 10.1006/abbi.1993.1601. [DOI] [PubMed] [Google Scholar]
- Fletcher B. S., Kujubu D. A., Perrin D. M., Herschman H. R. Structure of the mitogen-inducible TIS10 gene and demonstration that the TIS10-encoded protein is a functional prostaglandin G/H synthase. J Biol Chem. 1992 Mar 5;267(7):4338–4344. [PubMed] [Google Scholar]
- Gheysen G., Inzé D., Soetaert P., Van Montagu M., Castresana C. Sequence of a Nicotiana plumbaginifolia beta(1,3)-glucanase gene encoding a vacuolar isoform. Nucleic Acids Res. 1990 Nov 25;18(22):6685–6685. doi: 10.1093/nar/18.22.6685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gopalan S., Bauer D. W., Alfano J. R., Loniello A. O., He S. Y., Collmer A. Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death. Plant Cell. 1996 Jul;8(7):1095–1105. doi: 10.1105/tpc.8.7.1095. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gopalan S., Wei W., He S. Y. hrp gene-dependent induction of hin1: a plant gene activated rapidly by both harpins and the avrPto gene-mediated signal. Plant J. 1996 Oct;10(4):591–600. doi: 10.1046/j.1365-313x.1996.10040591.x. [DOI] [PubMed] [Google Scholar]
- 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]
- Hammond-Kosack K. E., Jones J. D. Resistance gene-dependent plant defense responses. Plant Cell. 1996 Oct;8(10):1773–1791. doi: 10.1105/tpc.8.10.1773. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Inoue H., Nojima H., Okayama H. High efficiency transformation of Escherichia coli with plasmids. Gene. 1990 Nov 30;96(1):23–28. doi: 10.1016/0378-1119(90)90336-p. [DOI] [PubMed] [Google Scholar]
- 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]
- Jacobson M. D. Reactive oxygen species and programmed cell death. Trends Biochem Sci. 1996 Mar;21(3):83–86. [PubMed] [Google Scholar]
- Jones J. D., Dunsmuir P., Bedbrook J. High level expression of introduced chimaeric genes in regenerated transformed plants. EMBO J. 1985 Oct;4(10):2411–2418. doi: 10.1002/j.1460-2075.1985.tb03949.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Liang P., Pardee A. B. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science. 1992 Aug 14;257(5072):967–971. doi: 10.1126/science.1354393. [DOI] [PubMed] [Google Scholar]
- Logemann J., Schell J., Willmitzer L. Improved method for the isolation of RNA from plant tissues. Anal Biochem. 1987 May 15;163(1):16–20. doi: 10.1016/0003-2697(87)90086-8. [DOI] [PubMed] [Google Scholar]
- May M. J., Hammond-Kosack K. E., Jones JDG. Involvement of Reactive Oxygen Species, Glutathione Metabolism, and Lipid Peroxidation in the Cf-Gene-Dependent Defense Response of Tomato Cotyledons Induced by Race-Specific Elicitors of Cladosporium fulvum. Plant Physiol. 1996 Apr;110(4):1367–1379. doi: 10.1104/pp.110.4.1367. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mehdy M. C. Active Oxygen Species in Plant Defense against Pathogens. Plant Physiol. 1994 Jun;105(2):467–472. doi: 10.1104/pp.105.2.467. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nelson M. J., Seitz S. P. The structure and function of lipoxygenase. Curr Opin Struct Biol. 1994 Dec;4(6):878–884. doi: 10.1016/0959-440x(94)90270-4. [DOI] [PubMed] [Google Scholar]
- O'Banion M. K., Winn V. D., Young D. A. cDNA cloning and functional activity of a glucocorticoid-regulated inflammatory cyclooxygenase. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):4888–4892. doi: 10.1073/pnas.89.11.4888. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Penninckx I. A., Eggermont K., Terras F. R., Thomma B. P., De Samblanx G. W., Buchala A., Métraux J. P., Manners J. M., Broekaert W. F. Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell. 1996 Dec;8(12):2309–2323. doi: 10.1105/tpc.8.12.2309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Picot D., Loll P. J., Garavito R. M. The X-ray crystal structure of the membrane protein prostaglandin H2 synthase-1. Nature. 1994 Jan 20;367(6460):243–249. doi: 10.1038/367243a0. [DOI] [PubMed] [Google Scholar]
- Reinbothe S., Mollenhauer B., Reinbothe C. JIPs and RIPs: the regulation of plant gene expression by jasmonates in response to environmental cues and pathogens. Plant Cell. 1994 Sep;6(9):1197–1209. doi: 10.1105/tpc.6.9.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Segal A. W., Abo A. The biochemical basis of the NADPH oxidase of phagocytes. Trends Biochem Sci. 1993 Feb;18(2):43–47. doi: 10.1016/0968-0004(93)90051-n. [DOI] [PubMed] [Google Scholar]
- Serhan C. N., Haeggström J. Z., Leslie C. C. Lipid mediator networks in cell signaling: update and impact of cytokines. FASEB J. 1996 Aug;10(10):1147–1158. doi: 10.1096/fasebj.10.10.8751717. [DOI] [PubMed] [Google Scholar]
- Shimizu T., Honda Z., Miki I., Seyama Y., Izumi T., Rådmark O., Samuelsson B. Potato arachidonate 5-lipoxygenase: purification, characterization, and preparation of 5(S)-hydroperoxyeicosatetraenoic acid. Methods Enzymol. 1990;187:296–306. doi: 10.1016/0076-6879(90)87034-z. [DOI] [PubMed] [Google Scholar]
- Tenhaken R., Levine A., Brisson L. F., Dixon R. A., Lamb C. Function of the oxidative burst in hypersensitive disease resistance. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4158–4163. doi: 10.1073/pnas.92.10.4158. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van den Ackerveken G., Marois E., Bonas U. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell. 1996 Dec 27;87(7):1307–1316. doi: 10.1016/s0092-8674(00)81825-5. [DOI] [PubMed] [Google Scholar]
- Véronési C., Rickauer M., Fournier J., Pouénat M. L., Esquerré-Tugayé M. T. Lipoxygenase gene expression in the tobacco-Phytophthora parasitica nicotianae interaction. Plant Physiol. 1996 Nov;112(3):997–1004. doi: 10.1104/pp.112.3.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Wei Z. M., Laby R. J., Zumoff C. H., Bauer D. W., He S. Y., Collmer A., Beer S. V. Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science. 1992 Jul 3;257(5066):85–88. doi: 10.1126/science.1621099. [DOI] [PubMed] [Google Scholar]
- Yahraus T., Chandra S., Legendre L., Low P. S. Evidence for a Mechanically Induced Oxidative Burst. Plant Physiol. 1995 Dec;109(4):1259–1266. doi: 10.1104/pp.109.4.1259. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhou J., Tang X., Martin G. B. The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J. 1997 Jun 2;16(11):3207–3218. doi: 10.1093/emboj/16.11.3207. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van der Biezen E. A., Brandwagt B. F., van Leeuwen W., Nijkamp H. J., Hille J. Identification and isolation of the FEEBLY gene from tomato by transposon tagging. Mol Gen Genet. 1996 Jun 12;251(3):267–280. doi: 10.1007/BF02172517. [DOI] [PubMed] [Google Scholar]