Skip to main content
Log in

Temporal evolution of the Arabidopsis oxidative stress response

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

We have carried out a detailed analysis of the changes in gene expression levels in Arabidopsis thaliana ecotype Columbia (Col-0) plants during and for 6 h after exposure to ozone (O3) at 350 parts per billion (ppb) for 6 h. This O3 exposure is sufficient to induce a marked transcriptional response and an oxidative burst, but not to cause substantial tissue damage in Col-0 wild-type plants and is within the range encountered in some major metropolitan areas. We have developed analytical and visualization tools to automate the identification of expression profile groups with common gene ontology (GO) annotations based on the sub-cellular localization and function of the proteins encoded by the genes, as well as to automate promoter analysis for such gene groups. We describe application of these methods to identify stress-induced genes whose transcript abundance is likely to be controlled by common regulatory mechanisms and summarized our findings in a temporal model of the stress response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • E.M. Aro I. Ohad (2003) ArticleTitleRedox regulation of thylakoid protein phosphorylation Antioxid. Redox Signal. 5 55–67 Occurrence Handle10.1089/152308603321223540 Occurrence Handle1:CAS:528:DC%2BD3sXhslGrsLc%3D Occurrence Handle12626117

    Article  CAS  PubMed  Google Scholar 

  • F. Azuaje (2002) ArticleTitleA cluster validity framework for genome expression data Bioinformatics 18 319–320 Occurrence Handle10.1093/bioinformatics/18.2.319 Occurrence Handle1:CAS:528:DC%2BD38XitFensb0%3D Occurrence Handle11847080

    Article  CAS  PubMed  Google Scholar 

  • B. Baker P. Zambryski B. Staskawicz S.P. Dinesh-Kumar (1997) ArticleTitleSignaling in plant-microbe interactions Science 276 726–733 Occurrence Handle10.1126/science.276.5313.726 Occurrence Handle1:CAS:528:DyaK2sXivFOltLg%3D Occurrence Handle9115193

    Article  CAS  PubMed  Google Scholar 

  • C.J. Baker E.W. Orlandi (1995) ArticleTitleActive oxygen in plant pathogenesis Annu. Rev. Phytopathol. 33 299–321 Occurrence Handle10.1146/annurev.py.33.090195.001503 Occurrence Handle1:CAS:528:DyaK2MXosFWisLg%3D

    Article  CAS  Google Scholar 

  • C.J. Baker E.W. Orlandi (1999) Sources and effect of reactive oxygen species in plants D.L. Gilbert C.A. Colton (Eds) Reactive Oxygen Species in Biological Systems: An Interdisciplinary Approach Kluwer New York 481–501

    Google Scholar 

  • J.M. Baldasano E. Valera P. Jimenez (2003) ArticleTitleAir quality data from large cities Sci. Total Environ. 307 141–165 Occurrence Handle10.1016/S0048-9697(02)00537-5 Occurrence Handle1:CAS:528:DC%2BD3sXjtFGntb4%3D Occurrence Handle12711431

    Article  CAS  PubMed  Google Scholar 

  • D. Barnes S.P. Mayfield (2003) ArticleTitleRedox control of posttranscriptional processes in the chloroplast Antioxid. Redox. Signal. 5 89–94 Occurrence Handle10.1089/152308603321223577 Occurrence Handle1:CAS:528:DC%2BD3sXhslGrs7g%3D Occurrence Handle12626120

    Article  CAS  PubMed  Google Scholar 

  • M. Beier J.D. Hoheisel (1999) ArticleTitleVersatile derivatisation of solid support media for covalent bonding on DNA-microchips Nucl. Acids Res. 27 1970–1977 Occurrence Handle10.1093/nar/27.9.1970 Occurrence Handle1:CAS:528:DyaK1MXjtV2ltr0%3D Occurrence Handle10198429

    Article  CAS  PubMed  Google Scholar 

  • E. Bell R.A. Creelman J.E. Mullet (1995) ArticleTitleA chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis Proc Natl Acad Sci USA 92 8675–8679 Occurrence Handle1:CAS:528:DyaK2MXotVGru7s%3D Occurrence Handle7567995

    CAS  PubMed  Google Scholar 

  • A. Ben-Hur D. Horn H.T. Siegelmann V. Vapnik (2002) ArticleTitleSupport vector clustering J. Mach. Learn. Res. 2 125–137 Occurrence Handle10.1162/15324430260185565

    Article  Google Scholar 

  • C. Bowler R. Fluhr (2000) ArticleTitleThe role of calcium and activated oxygens as signals for controlling cross-tolerance Trends Plant Sci. 5 241–246 Occurrence Handle10.1016/S1360-1385(00)01628-9 Occurrence Handle1:STN:280:DC%2BD3czpsVahtw%3D%3D

    Article  CAS  Google Scholar 

  • A. Brazma P. Hingamp J. Quackenbush G. Sherlock P. Spellman C. Stoeckert J. Aach W. Ansorge C.A. Ball H.C. Causton T. Gaasterland P. Glenisson F.C.P. Holstege I.F. Kim V. Markowitz J.C. Matese H. Parkinson A. Robinson U. Sarkans S. Schulze-Kremer J. Stewart R. Taylor J. Vilo M. Vingron (2001) ArticleTitleMinimum information about a microarray experiment (MIAME) – toward standards for microarray data Nat. Genet. 29 365–371

    Google Scholar 

  • P. Campbell J. Braam (1998) ArticleTitleCo- and/or post-translational modifications are critical for TCH4 XET activity Plant J. 15 553–561 Occurrence Handle10.1046/j.1365-313X.1998.00239.x Occurrence Handle1:CAS:528:DyaK1cXmtFOit7k%3D Occurrence Handle9753780

    Article  CAS  PubMed  Google Scholar 

  • I. Carlberg M. Hansson T. Kieselbach W.P. Schroder B. Andersson A.V. Vener (2003) ArticleTitleA novel plant protein undergoing light-induced phosphorylation and release from the photosynthetic thylakoid membranes Proc. Natl. Acad. Sci. USA 100 757–762 Occurrence Handle10.1073/pnas.0235452100 Occurrence Handle1:CAS:528:DC%2BD3sXnvVKrsg%3D%3D Occurrence Handle12524456

    Article  CAS  PubMed  Google Scholar 

  • C.S. Chan L. Guo M.C. Shih (2001) ArticleTitlePromoter analysis of the nuclear gene encoding the chloroplast glyceraldehyde-3-phosphate dehydrogenase B subunit of Arabidopsis thaliana Plant Mol. Biol. 46 131–141 Occurrence Handle10.1023/A:1010602031070 Occurrence Handle1:CAS:528:DC%2BD3MXltVeisLo%3D Occurrence Handle11442054

    Article  CAS  PubMed  Google Scholar 

  • P.L. Conklin R.L. Last (1995) ArticleTitleDifferential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone Plant Physiol. 109 203–212 Occurrence Handle10.1104/pp.109.1.203 Occurrence Handle1:CAS:528:DyaK2MXotFWmsL0%3D Occurrence Handle7480322

    Article  CAS  PubMed  Google Scholar 

  • R.A. Creelman J.E. Mullet (1997) ArticleTitleBiosynthesis and action of jasmonates in plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 355–381 Occurrence Handle10.1146/annurev.arplant.48.1.355 Occurrence Handle1:CAS:528:DyaK2sXjs1enu7s%3D Occurrence Handle15012267

    Article  CAS  PubMed  Google Scholar 

  • M. Cruz Castillo C. Martinez A. Buchala J.P. Metraux J. Leon (2004) ArticleTitleGene-specific involvement of beta-oxidation in wound-activated responses in Arabidopsis Plant Physiol. 135 85–94 Occurrence Handle10.1104/pp.104.039925 Occurrence Handle1:STN:280:DC%2BD2c3nvFOruw%3D%3D Occurrence Handle15141068

    Article  CAS  PubMed  Google Scholar 

  • R. Desikan S.A.H. Mackerness J.T. Hancock S.J. Neill (2001) ArticleTitleRegulation of the Arabidopsis transcriptome by oxidative stress Plant Physiol. 127 159–172 Occurrence Handle10.1104/pp.127.1.159 Occurrence Handle1:CAS:528:DC%2BD3MXmvFCrt7g%3D Occurrence Handle11553744

    Article  CAS  PubMed  Google Scholar 

  • C. Despres C. Chubak A. Rochon R. Clark T. Bethune D. Desveaux P.R. Fobert (2003) ArticleTitleThe Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1 Plant Cell 15 2181–2191 Occurrence Handle10.1105/tpc.012849 Occurrence Handle1:CAS:528:DC%2BD3sXnsV2gurY%3D Occurrence Handle12953119

    Article  CAS  PubMed  Google Scholar 

  • A. Dievart S.E. Clark (2004) ArticleTitleLRR-containing receptors regulating plant development and defense Development 131 251–261 Occurrence Handle10.1242/dev.00998 Occurrence Handle1:CAS:528:DC%2BD2cXhsVSrtLo%3D Occurrence Handle14701679

    Article  CAS  PubMed  Google Scholar 

  • M. Duval T.F. Hsieh S.Y. Kim T.L. Thomas (2002) ArticleTitleMolecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily Plant Mol. Biol. 50 237–248 Occurrence Handle10.1023/A:1016028530943 Occurrence Handle1:CAS:528:DC%2BD38XkvVagurw%3D Occurrence Handle12175016

    Article  CAS  PubMed  Google Scholar 

  • M.B. Eisen P.T. Spellman P.O. Brown D. Botstein (1998) ArticleTitleCluster analysis and display of genome-wide expression patterns Proc Natl. Acad. Sci. USA 95 14863–14868 Occurrence Handle10.1073/pnas.95.25.14863 Occurrence Handle1:CAS:528:DyaK1cXotVGmurk%3D Occurrence Handle9843981

    Article  CAS  PubMed  Google Scholar 

  • J.M. Escoubas M. Lomas J. LaRoche P.G. Falkowski (1995) ArticleTitleLight intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool Proc. Natl. Acad. Sci. USA 92 10237–10241 Occurrence Handle1:CAS:528:DyaK2MXovFalsLc%3D Occurrence Handle7479759

    CAS  PubMed  Google Scholar 

  • T. Eulgem P.J. Rushton S. Robatzek I.E. Somssich (2000) ArticleTitleThe WRKY superfamily of plant transcription factors Trends Plant Sci. 5 199–206 Occurrence Handle10.1016/S1360-1385(00)01600-9 Occurrence Handle1:STN:280:DC%2BD3c3kvFalsw%3D%3D Occurrence Handle10785665

    Article  CAS  PubMed  Google Scholar 

  • W. Fan X. Dong (2002) ArticleTitleIn vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis Plant Cell 14 1377–1379 Occurrence Handle10.1105/tpc.001628 Occurrence Handle1:CAS:528:DC%2BD38Xlt1alsLk%3D Occurrence Handle12084833

    Article  CAS  PubMed  Google Scholar 

  • V. Fotopoulos M.J. Gilbert J.K. Pittman A.C. Marvier A.J. Buchanan N. Sauer J.L. Hall L.E. Williams (2003) ArticleTitleThe monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atbetafruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum Plant Physiol. 132 821–829 Occurrence Handle10.1104/pp.103.021428 Occurrence Handle1:CAS:528:DC%2BD3sXkslert7Y%3D Occurrence Handle12805612

    Article  CAS  PubMed  Google Scholar 

  • B. Gillissen L. Burkle B. Andre C. Kuhn D. Rentsch B. Brandl W.B. Frommer (2000) ArticleTitleA new family of high-affinity transporters for adenine, cytosine, and purine derivatives in Arabidopsis Plant Cell 12 291–300 Occurrence Handle10.1105/tpc.12.2.291 Occurrence Handle1:CAS:528:DC%2BD3cXktFagtb0%3D Occurrence Handle10662864

    Article  CAS  PubMed  Google Scholar 

  • J.C. Gray J.A. Sullivan J.H. Wang C.A. Jerome D. MacLean (2003) ArticleTitleCoordination of plastid and nuclear gene expression Philos. Trans. R Soc. Lond. B Biol. Sci. 358 135–144; discussion 144–145 Occurrence Handle10.1098/rstb.2002.1180 Occurrence Handle1:CAS:528:DC%2BD3sXktVWhsrs%3D Occurrence Handle12594922

    Article  CAS  PubMed  Google Scholar 

  • J.T. Greenberg (1996) ArticleTitleProgrammed cell death: a way of life for plants Proc. Natl. Acad. Sci. USA 93 12094–12097 Occurrence Handle10.1073/pnas.93.22.12094 Occurrence Handle1:CAS:528:DyaK28Xms1Cqu7w%3D Occurrence Handle8901538

    Article  CAS  PubMed  Google Scholar 

  • K. Higo Y. Ugawa M. Iwamoto H. Higo (1998) ArticleTitlePLACE: a database of plant cis-acting regulatory DNA elements Nucl. Acids Res. 26 358–359 Occurrence Handle10.1093/nar/26.1.358 Occurrence Handle1:CAS:528:DyaK1cXovVCksg%3D%3D Occurrence Handle9399873

    Article  CAS  PubMed  Google Scholar 

  • A.K. Hull J.L. Celenza (2000) ArticleTitleBacterial expression and purification of the Arabidopsis NADPH-cytochrome P450 reductase ATR2 Protein Expr. Purif. 18 310–315 Occurrence Handle10.1006/prep.1999.1195 Occurrence Handle1:CAS:528:DC%2BD3cXhvFCmtL8%3D Occurrence Handle10733884

    Article  CAS  PubMed  Google Scholar 

  • M. Ikura M. Osawa J.B. Ames (2002) ArticleTitleThe role of calcium-binding proteins in the control of transcription: structure to function Bioessays 24 625–636 Occurrence Handle10.1002/bies.10105 Occurrence Handle1:CAS:528:DC%2BD38XlvVSntr4%3D Occurrence Handle12111723

    Article  CAS  PubMed  Google Scholar 

  • P. Jarvis (2003) ArticleTitleIntracellular signalling: the language of the chloroplast Curr. Biol. 13 R314–R316 Occurrence Handle10.1016/S0960-9822(03)00235-5 Occurrence Handle1:CAS:528:DC%2BD3sXksVyiurs%3D Occurrence Handle12699643

    Article  CAS  PubMed  Google Scholar 

  • M.W. Jones-Rhoades D.P. Bartel (2004) ArticleTitleComputational identification of plant microRNAs and their targets, including a stress-induced miRNA Mol. Cell 14 787–799 Occurrence Handle10.1016/j.molcel.2004.05.027 Occurrence Handle1:CAS:528:DC%2BD2cXlslemtrs%3D Occurrence Handle15200956

    Article  CAS  PubMed  Google Scholar 

  • J.H. Joo Y.S. Bae J.S. Lee (2001) ArticleTitleRole of auxin-induced reactive oxygen species in root gravitropism Plant Physiol. 126 1055–1060 Occurrence Handle10.1104/pp.126.3.1055 Occurrence Handle1:CAS:528:DC%2BD3MXlsVarur8%3D Occurrence Handle11457956

    Article  CAS  PubMed  Google Scholar 

  • Joo, J.H., Wang, S., Chen, J.G., Jones, A.M. and Fedoroff, N.V. 2005. Different signaling and cell-death roles of heterotrimeric G protein α and β subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell. 17: 957--970

    Google Scholar 

  • S. Karpinski H. Gabrys A. Mateo B. Karpinska P.M. Mullineaux (2003) ArticleTitleLight perception in plant disease defence signalling Curr. Opin. Plant Biol. 6 390–396 Occurrence Handle10.1016/S1369-5266(03)00061-X Occurrence Handle1:CAS:528:DC%2BD3sXlsValtbc%3D Occurrence Handle12873535

    Article  CAS  PubMed  Google Scholar 

  • T. Kiyosue H. Abe K. Yamaguchi-Shinozaki K. Shinozaki (1998) ArticleTitleERD6, a cDNA clone for an early dehydration-induced gene of Arabidopsis, encodes a putative sugar transporter Biochim. Biophys. Acta. 1370 187–191 Occurrence Handle1:CAS:528:DyaK1cXhvVSjsbY%3D Occurrence Handle9545564

    CAS  PubMed  Google Scholar 

  • C.J. Lamb R.A. Dixon (1994) ArticleTitleMolecular mechanisms underlying induction of plant defence gene transcription Biochem. Soc. Symp. 60 241–248 Occurrence Handle1:CAS:528:DyaK2MXns1Cku7w%3D Occurrence Handle7639783

    CAS  PubMed  Google Scholar 

  • C.J. Lamb R.A. Dixon (1997) ArticleTitleThe oxidative burst in plant disease resistance Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 251–275

    Google Scholar 

  • K. Lee J. Lee Y. Kim D. Bae K.Y. Kang S.C. Yoon D. Lim (2004) ArticleTitleDefining the plant disulfide proteome Electrophoresis 25 532–541 Occurrence Handle10.1002/elps.200305677 Occurrence Handle1:CAS:528:DC%2BD2cXhsFaqs70%3D Occurrence Handle14760647

    Article  CAS  PubMed  Google Scholar 

  • B. Louerat-Oriou A. Perret D. Pompon (1998) ArticleTitleDifferential redox and electron-transfer properties of purified yeast, plant and human NADPH-cytochrome P-450 reductases highly modulate cytochrome P-450 activities Eur. J. Biochem. 258 1040–1049 Occurrence Handle10.1046/j.1432-1327.1998.2581040.x Occurrence Handle1:CAS:528:DyaK1MXisFehuw%3D%3D Occurrence Handle9990323

    Article  CAS  PubMed  Google Scholar 

  • P.S. Low J.R. Merida (1996) ArticleTitleThe oxidative burst in plant defense: function and signal transduction Physiol. Plant. 96 533–542 Occurrence Handle10.1034/j.1399-3054.1996.960326.x Occurrence Handle1:CAS:528:DyaK28XivV2qtLc%3D

    Article  CAS  Google Scholar 

  • R. Mahalingam A. Gomez-Buitrago N. Eckardt N. Shah A. Guevara-Garcia P. Day R. Raina N.V. Fedoroff (2003) ArticleTitleCharacterizing the stress/defense transcriptome of Arabidopsis Gen. Biol. 4 R20 Occurrence Handle10.1186/gb-2003-4-3-r20

    Article  Google Scholar 

  • R. Mahalingam N.V. Fedoroff (2003) ArticleTitleStress response, cell death and signaling: the many faces of reactive oxygen species Physiol. Plant. 119 56–68 Occurrence Handle10.1034/j.1399-3054.2003.00156.x Occurrence Handle1:CAS:528:DC%2BD3sXnt1Wqtr4%3D

    Article  CAS  Google Scholar 

  • B.C. Meyers A.W. Dickerman R.W. Michelmore S. Sivaramakrishnan B.W. Sobral N.D. Young (1999) ArticleTitlePlant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily [In Process Citation] Plant J. 20 317–332 Occurrence Handle1:CAS:528:DC%2BD3cXjsF2kug%3D%3D Occurrence Handle10571892

    CAS  PubMed  Google Scholar 

  • B.C. Meyers A. Kozik A. Griego H. Kuang R.W. Michelmore (2003) ArticleTitleGenome-wide analysis of NBS-LRR-encoding genes in Arabidopsis Plant Cell 15 809–834 Occurrence Handle10.1105/tpc.009308 Occurrence Handle1:CAS:528:DC%2BD3sXjtFSlsLo%3D Occurrence Handle12671079

    Article  CAS  PubMed  Google Scholar 

  • W. Moeder C.S. Barry A.A. Tauriainen C. Betz J. Tuomainen M. Utriainen D. Grierson H. Sandermann C. Langebartels J. Kangasjarvi (2002) ArticleTitleEthylene synthesis regulated by biphasic induction of 1-aminocyclopropane-1-carboxylic acid synthase and 1-aminocyclopropane-1-carboxylic acid oxidase genes is required for hydrogen peroxide accumulation and cell death in ozone-exposed tomato Plant Physiol. 130 1918–1926 Occurrence Handle10.1104/pp.009712 Occurrence Handle1:CAS:528:DC%2BD3sXktlKh Occurrence Handle12481074

    Article  CAS  PubMed  Google Scholar 

  • M.H. Montane F. Tardy K. Kloppstech M. Havaux (1998) ArticleTitleDifferential control of xanthophylls and light-induced stress proteins, as opposed to light-harvesting chlorophyll a/b proteins, during photosynthetic acclimation of barley leaves to light irradiance Plant Physiol. 118 227–235 Occurrence Handle10.1104/pp.118.1.227 Occurrence Handle1:CAS:528:DyaK1cXmtV2mu7w%3D Occurrence Handle9733542

    Article  CAS  PubMed  Google Scholar 

  • Z. Mou W. Fan X. Dong (2003) ArticleTitleInducers of plant systemic acquired resistance regulate NPR1 function through redox changes Cell 113 1–20 Occurrence Handle10.1016/S0092-8674(03)00429-X Occurrence Handle12679025

    Article  PubMed  Google Scholar 

  • P. Mullineaux L. Ball C. Escobar B. Karpinska G. Creissen S. Karpinski (2000) ArticleTitleAre diverse signalling pathways integrated in the regulation of Arabidopsis antioxidant defence gene expression in response to excess excitation energy? Philos. Trans. R Soc. Lond. B Biol. Sci. 355 1531–1540 Occurrence Handle10.1098/rstb.2000.0713 Occurrence Handle1:CAS:528:DC%2BD3cXovFOisLw%3D Occurrence Handle11128006

    Article  CAS  PubMed  Google Scholar 

  • P. Mullineaux S. Karpinski (2002) ArticleTitleSignal transduction in response to excess light: getting out of the chloroplast Curr. Opin. Plant Biol. 5 43–48 Occurrence Handle10.1016/S1369-5266(01)00226-6 Occurrence Handle1:CAS:528:DC%2BD38XitlejtA%3D%3D Occurrence Handle11788307

    Article  CAS  PubMed  Google Scholar 

  • C. Nawrath S. Heck N. Parinthawong J.P. Metraux (2002) ArticleTitleEDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family Plant Cell 14 275–286 Occurrence Handle10.1105/tpc.010376 Occurrence Handle1:CAS:528:DC%2BD38Xht1SrtrY%3D Occurrence Handle11826312

    Article  CAS  PubMed  Google Scholar 

  • K. Overmyer H. Tuominen R. Kettunen C. Betz C. Langebartels H. Sandermann Particle Jr. J. Kangasjarvi (2000) ArticleTitleOzone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death Plant Cell 12 1849–1862 Occurrence Handle10.1105/tpc.12.10.1849 Occurrence Handle1:CAS:528:DC%2BD3cXotFaisL8%3D Occurrence Handle11041881

    Article  CAS  PubMed  Google Scholar 

  • T. Pfannschmidt (2003) ArticleTitleChloroplast redox signals: how photosynthesis controls its own genes Trends Plant Sci. 8 33–41 Occurrence Handle10.1016/S1360-1385(02)00005-5 Occurrence Handle1:CAS:528:DC%2BD3sXnvFer Occurrence Handle12523998

    Article  CAS  PubMed  Google Scholar 

  • S. Pursiheimo P. Mulo E. Rintamaki E.M. Aro (2001) ArticleTitleCoregulation of light-harvesting complex II phosphorylation and lhcb mRNA accumulation in winter rye Plant J. 26 317–327 Occurrence Handle10.1046/j.1365-313X.2001.01033.x Occurrence Handle1:CAS:528:DC%2BD3MXlt1Ohtbw%3D Occurrence Handle11439120

    Article  CAS  PubMed  Google Scholar 

  • L.D. Pysh J.W. Wysocka-Diller C. Camilleri D. Bouchez P.N. Benfey (1999) ArticleTitleThe GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes Plant J. 18 111–119 Occurrence Handle10.1046/j.1365-313X.1999.00431.x Occurrence Handle1:CAS:528:DyaK1MXjtVyqtbg%3D Occurrence Handle10341448

    Article  CAS  PubMed  Google Scholar 

  • M.V. Rao H. Lee R.A. Creelman J.E. Mullet K.R. Davis (2000) ArticleTitleJasmonic acid signaling modulates ozone-induced hypersensitive cell death Plant Cell 12 1633–1646 Occurrence Handle10.1105/tpc.12.9.1633 Occurrence Handle1:CAS:528:DC%2BD3cXnsVyltrs%3D Occurrence Handle11006337

    Article  CAS  PubMed  Google Scholar 

  • E. Richly A. Dietzmann A. Biehl J. Kurth C. Laloi K. Apel F. Salamini D. Leister (2003) ArticleTitleCovariations in the nuclear chloroplast transcriptome reveal a regulatory master-switch EMBO Rep. 4 491–498 Occurrence Handle10.1038/sj.embor.embor828 Occurrence Handle1:CAS:528:DC%2BD3sXjtlaksLg%3D Occurrence Handle12776738

    Article  CAS  PubMed  Google Scholar 

  • E. Rintamaki P. Martinsuo S. Pursiheimo E.M. Aro (2000) ArticleTitleCooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin–thioredoxin system in chloroplasts Proc. Natl. Acad. Sci. USA 97 11644–11649 Occurrence Handle10.1073/pnas.180054297 Occurrence Handle1:CAS:528:DC%2BD3cXnsF2qtrw%3D Occurrence Handle11005828

    Article  CAS  PubMed  Google Scholar 

  • J.D. Rochaix (1996) ArticleTitlePost-transcriptional regulation of chloroplast gene expression in Chlamydomonas reinhardtii Plant Mol. Biol. 32 327–341 Occurrence Handle10.1007/BF00039389 Occurrence Handle1:CAS:528:DyaK2sXjslKi Occurrence Handle8980486

    Article  CAS  PubMed  Google Scholar 

  • V.C. Runeckles B.I. Chevonne (1992) Crop responses to ozone A.S. Lefohn (Eds) Surface Level Ozone Exposures and Their Effects on Vegetation Lewis Publishers, Inc. Chelsea, MI 189–270

    Google Scholar 

  • M.L. Salvador U. Klein (1999) ArticleTitleThe redox state regulates RNA degradation in the chloroplast of Chlamydomonas reinhardtii Plant Physiol. 121 1367–1374 Occurrence Handle10.1104/pp.121.4.1367 Occurrence Handle1:CAS:528:DyaK1MXotFyis7g%3D Occurrence Handle10594124

    Article  CAS  PubMed  Google Scholar 

  • J. Sambrook E.F. Fritsch T. Maniatis (1989) Molecular Cloning: A Laboratory Manual Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY

    Google Scholar 

  • H. Sandermann SuffixJr. (2000) ArticleTitleActive oxygen species as mediators of plant immunity: three case studies Biol. Chem. 381 649–653 Occurrence Handle10.1515/BC.2000.085 Occurrence Handle1:CAS:528:DC%2BD3cXntlGmsbw%3D Occurrence Handle11030422

    Article  CAS  PubMed  Google Scholar 

  • H.J. Sandermann E. Ernst W. Heller C. Langebartels (1998) ArticleTitleOzone: an abiotic elicitor of plant defence reactions Trends Plant Sci. 3 47–49 Occurrence Handle10.1016/S1360-1385(97)01162-X

    Article  Google Scholar 

  • H. Sandermann ParticleJr. (1996) ArticleTitleOzone and plant health Annu. Rev. Phytopathol. 34 347–366 Occurrence Handle10.1146/annurev.phyto.34.1.347 Occurrence Handle1:CAS:528:DyaK28XlsFOhsLs%3D Occurrence Handle15012547

    Article  CAS  PubMed  Google Scholar 

  • D. Scheel (2002) Oxidative burst and the role of reactive oxygen species in plant–pathogen interactions D. Inze M. Montagu ParticleVan (Eds) Oxidative Stress in Plants Taylor and Francis New York 137–153

    Google Scholar 

  • P. Schopfer A. Liszkay M. Bechtold G. Frahry A. Wagner (2002) ArticleTitleEvidence that hydroxyl radicals mediate auxin-induced extension growth Planta 214 821–828 Occurrence Handle10.1007/s00425-001-0699-8 Occurrence Handle1:CAS:528:DC%2BD38XisF2qu7o%3D Occurrence Handle11941457

    Article  CAS  PubMed  Google Scholar 

  • J. Shah D.F. Klessig (1996) ArticleTitleIdentification of a salicylic acid-responsive element in the promoter of the tobacco pathogenesis-related beta-1,3-glucanase gene, PR-2d Plant J 10 1089–1101

    Google Scholar 

  • N.H. Shah N.V. Fedoroff (2004) ArticleTitleCLENCH: a program for calculating CLuster ENriCHment using the Gene Ontology Bioinformatics 20 1196–1197 Occurrence Handle10.1093/bioinformatics/bth056 Occurrence Handle1:CAS:528:DC%2BD2cXjs1Wrt70%3D Occurrence Handle14764555

    Article  CAS  PubMed  Google Scholar 

  • N.H. Shah D.C. King P.N. Shah N.V. Fedoroff (2003) ArticleTitleA tool-kit for cDNA microarray and promoter analysis Bioinformatics 19 1846–1848 Occurrence Handle10.1093/bioinformatics/btg253 Occurrence Handle1:CAS:528:DC%2BD3sXot1Cku74%3D Occurrence Handle14512358

    Article  CAS  PubMed  Google Scholar 

  • Y.K. Sharma K.R. Davis (1997) ArticleTitleThe effects of ozone on antioxidant responses in plants Free Radic. Biol. Med. 23 480–488 Occurrence Handle10.1016/S0891-5849(97)00108-1 Occurrence Handle1:CAS:528:DyaK2sXksVahur4%3D Occurrence Handle9214586

    Article  CAS  PubMed  Google Scholar 

  • Y.K. Sharma J. Leon I. Raskin K.R. Davis (1996) ArticleTitleOzone-induced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defense-related transcripts and induced resistance Proc. Natl. Acad. Sci. USA 93 5099–5104 Occurrence Handle10.1073/pnas.93.10.5099 Occurrence Handle1:CAS:528:DyaK28XjtVKlur0%3D Occurrence Handle8643534

    Article  CAS  PubMed  Google Scholar 

  • I. Sherameti S.K. Sopory A. Trebicka T. Pfannschmidt R. Oelmuller (2002) ArticleTitlePhotosynthetic electron transport determines nitrate reductase gene expression and activity in higher plants J. Biol. Chem. 277 46594–46600 Occurrence Handle10.1074/jbc.M202924200 Occurrence Handle1:CAS:528:DC%2BD38XovFKgs78%3D Occurrence Handle12244040

    Article  CAS  PubMed  Google Scholar 

  • K. Shirasu R.A. Dixon C. Lamb (1996) ArticleTitleSignal transduction in plant immunity Curr. Opin. Immunol. 8 3–7 Occurrence Handle10.1016/S0952-7915(96)80097-5 Occurrence Handle1:CAS:528:DyaK28XitVansLw%3D Occurrence Handle8729439

    Article  CAS  PubMed  Google Scholar 

  • G.W. Stuart P.F. Searle R.D. Palmiter (1985) ArticleTitleIdentification of multiple metal regulatory elements in mouse metallothionein-i promoter by assaying synthetic sequences Nature 317 828–831 Occurrence Handle10.1038/317828a0 Occurrence Handle1:CAS:528:DyaL28Xhs1Wg Occurrence Handle4058587

    Article  CAS  PubMed  Google Scholar 

  • J.A. Sullivan J.C. Gray (2002) ArticleTitleMultiple plastid signals regulate the expression of the pea plastocyanin gene in pea and transgenic tobacco plants Plant J. 32 763–774 Occurrence Handle10.1046/j.1365-313X.2002.01464.x Occurrence Handle1:CAS:528:DC%2BD3sXjtFWktA%3D%3D Occurrence Handle12472691

    Article  CAS  PubMed  Google Scholar 

  • M. Tamaoki N. Nakajima A. Kubo M. Aono T. Matsuyama H. Saji (2003) ArticleTitleTranscriptome analysis of O3-exposed Arabidopsis reveals that multiple signal pathways act mutually antagonistically to induce gene expression Plant Mol. Biol. 53 443–456 Occurrence Handle10.1023/B:PLAN.0000019064.55734.52 Occurrence Handle1:CAS:528:DC%2BD2cXhvFCgt7o%3D Occurrence Handle15010611

    Article  CAS  PubMed  Google Scholar 

  • J.J. Tilly D.W. Allen T. Jack (1998) ArticleTitleThe CArG boxes in the promoter of the Arabidopsis floral organ identity gene APETALA3 mediate diverse regulatory effects Development 125 1647–1657 Occurrence Handle1:CAS:528:DyaK1cXjslemur0%3D Occurrence Handle9521903

    CAS  PubMed  Google Scholar 

  • H. Tuominen K. Overmyer M. Keinanen H. Kollist J. Kangasjarvi (2004) ArticleTitleMutual antagonism of ethylene and jasmonic acid regulates ozone-induced spreading cell death in Arabidopsis Plant J 39 59–69 Occurrence Handle10.1111/j.1365-313X.2004.02107.x Occurrence Handle1:CAS:528:DC%2BD2cXms1ykurw%3D Occurrence Handle15200642

    Article  CAS  PubMed  Google Scholar 

  • T. Ulmasov G. Hagen T. Guilfoyle (1994) ArticleTitleThe ocs element in the soybean GH2/4 promoter is activated by both active and inactive auxin and salicylic acid analogues Plant Mol. Biol. 26 1055–1064 Occurrence Handle10.1007/BF00040688 Occurrence Handle1:CAS:528:DyaK2MXjtVWrsbk%3D Occurrence Handle7811965

    Article  CAS  PubMed  Google Scholar 

  • T. Ulmasov G. Hagen T.J. Guilfoyle (1997) ArticleTitleARF1, a transcription factor that binds to auxin response elements Science 276 1865–1868 Occurrence Handle10.1126/science.276.5320.1865 Occurrence Handle1:CAS:528:DyaK2sXksVCnu7k%3D Occurrence Handle9188533

    Article  CAS  PubMed  Google Scholar 

  • T. Ulmasov Z.B. Liu G. Hagen T.J. Guilfoyle (1995) ArticleTitleComposite structure of auxin response elements Plant Cell 7 1611–1623 Occurrence Handle10.1105/tpc.7.10.1611 Occurrence Handle1:CAS:528:DyaK2MXovFCqurw%3D Occurrence Handle7580254

    Article  CAS  PubMed  Google Scholar 

  • S. Vandenabeele K. Kelen ParticleVan Der J. Dat I. Gadjev T. Boonefaes S. Morsa P. Rottiers L. Slooten M. Van Montagu M. Zabeau D. Inze F. Van Breusegem (2003) ArticleTitleA comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco Proceedings of the National Academy of Sciences of the United States of America 100 16113–16118 Occurrence Handle10.1073/pnas.2136610100 Occurrence Handle1:CAS:528:DC%2BD2cXhtVGisg%3D%3D Occurrence Handle14671332

    Article  CAS  PubMed  Google Scholar 

  • S. Vandenabeele S. Vanderauwera M. Vuylsteke S. Rombauts C. Langebartels H.K. Seidlitz M. Zabeau M. Van Montagu D. Inze F. Van Breusegem (2004) ArticleTitleCatalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana Plant J. 39 45–58 Occurrence Handle10.1111/j.1365-313X.2004.02105.x Occurrence Handle1:CAS:528:DC%2BD2cXms1ykur4%3D Occurrence Handle15200641

    Article  CAS  PubMed  Google Scholar 

  • A.V. Vener I. Ohad B. Andersson (1998) ArticleTitleProtein phosphorylation and redox sensing in chloroplast thylakoids Curr. Opin. Plant Biol. 1 217–223 Occurrence Handle10.1016/S1369-5266(98)80107-6 Occurrence Handle1:CAS:528:DyaK1cXktFaku78%3D Occurrence Handle10066592

    Article  CAS  PubMed  Google Scholar 

  • A.V. Vener P.J. Van Kan P.R. Rich I.I. Ohad B. Andersson (1997) ArticleTitlePlastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash Proc. Natl. Acad. Sci. USA 94 1585–1590 Occurrence Handle10.1073/pnas.94.4.1585 Occurrence Handle1:CAS:528:DyaK2sXhtl2mt7g%3D Occurrence Handle11038603

    Article  CAS  PubMed  Google Scholar 

  • W. Xu M.M. Purugganan D.H. Polisensky D.M. Antosiewicz S.C. Fry J. Braam (1995) ArticleTitleArabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase Plant Cell 7 1555–1567 Occurrence Handle10.1105/tpc.7.10.1555 Occurrence Handle1:CAS:528:DyaK2MXovFCqtbY%3D Occurrence Handle7580251

    Article  CAS  PubMed  Google Scholar 

  • H. Zer I. Ohad (2003) ArticleTitleLight, redox state, thylakoid-protein phosphorylation and signaling gene expression Trends Biochem. Sci. 28 467–470 Occurrence Handle10.1016/S0968-0004(03)00173-7 Occurrence Handle1:CAS:528:DC%2BD3sXnt1yls7o%3D Occurrence Handle13678955

    Article  CAS  PubMed  Google Scholar 

  • J.M. Zhou Y. Trifa H. Silva D. Pontier E. Lam J. Shah D.F. Klessig (2000) ArticleTitleNPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid Mol Plant Microbe Int. 13 191–202 Occurrence Handle1:CAS:528:DC%2BD3cXntFGqsw%3D%3D

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ramamurthy Mahalingam.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mahalingam, R., Shah, N., Scrymgeour, A. et al. Temporal evolution of the Arabidopsis oxidative stress response. Plant Mol Biol 57, 709–730 (2005). https://doi.org/10.1007/s11103-005-2860-4

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-005-2860-4

Keywords

Navigation