Skip to main content
SpringerLink
Log in

Identification of NPR1-Dependent and Independent Genes Early Induced by Salicylic Acid Treatment in Arabidopsis

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Salicylic acid (SA) plays a crucial role in stress resistance in plants by modifying the expression of a battery of genes. In this paper, we report the identification of a group of early SA-regulated genes of Arabidopsis (activated between 0.5–2.5 h), using the cDNA-amplified fragment length polymorphism technique (cDNA-AFLP). Using 128 different primer combinations, we identified several genes based on their differential expression during SA treatment. Among these, we identified 12 genes up-regulated by SA whose patterns of induction were confirmed by Northern analysis. The identified genes can be grouped into two functional groups: Group 1: genes involved in cell protection (i.e. glycosyltransferases, glutathion S-transferases), and Group 2: genes involved in signal transduction (protein kinases and transcription factors). We also evaluated NPR1 requirement for the induction of the 12 up-regulated genes, and found that only those belonging to Group 2 require this co-activator for their expression. In silico analysis of the promoter sequences of the up-regulated genes, allowed us to identify putative cis-elements over-represented in these genes. Interestingly, as-1-like elements, previously characterized as SA-responsive elements, were specifically over-represented in Group 1 genes. The identification of early SA-regulated genes is an important step towards understanding the complex role of this hormone in plant stress resistance.

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

Access this article

Log in via an institution

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

Abbreviations

AFLP-TP:

amplified fragment length polymorphism-based transcript profiling

as-1 :

activation sequence-1

GST:

glutathione S-transferase

GT:

glycosyltransferase

HR:

hypersensitive response

IEGT :

immediate early glycosyltransferase gene

JA:

jasmonic acid

NPR1:

nonexpressor of PR genes 1

PR:

pathogenesis-related proteins

ROS:

reactive oxygen species

SA:

salicylic acid

SAR:

systemic acquired resistance

TDF:

transcript derived fragments

TGAs:

family of bZip transcription factors recognizing TGACG motif

WT:

wild type

References

  • M.E. Alvarez R.I. Pennell P.J. Meijer A. Ishikawa R.A. Dixon C. Lamb (1998) ArticleTitleReactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity Cell 92 773–784 Occurrence Handle10.1016/S0092-8674(00)81405-1 Occurrence Handle9529253 Occurrence Handle1:CAS:528:DyaK1cXit1KlsLg%3D

    Article  PubMed  CAS  Google Scholar 

  • C.W.B. Bachem R.S. Hoeven Particlevan der S.M. Bruijn Particlede D. Vreugdenhil M. Zabeau R.G.F. Visser (1996) ArticleTitleVisualization of differential gene expression using a novel method of RNA fingerprint based on AFLP: Analysis of gene expression during potato tuber development Plant J. 9 745–753 Occurrence Handle10.1046/j.1365-313X.1996.9050745.x Occurrence Handle8653120 Occurrence Handle1:CAS:528:DyaK28XjvVSlsro%3D

    Article  PubMed  CAS  Google Scholar 

  • P.N. Benfey L. Ren N.H. Chua (1990) ArticleTitleTissue-specific expression from CaMV 35S enhancer subdomains in early stages of plant development Embo. J. 9 1677–1684 Occurrence Handle2347301 Occurrence Handle1:CAS:528:DyaK3cXltFSnsrw%3D

    PubMed  CAS  Google Scholar 

  • O. Borsani V. Valpuesta M.A. Botella (2001) ArticleTitleEvidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings Plant Physiol. 126 1024–1030 Occurrence Handle10.1104/pp.126.3.1024 Occurrence Handle11457953 Occurrence Handle1:CAS:528:DC%2BD3MXlsVartbY%3D

    Article  PubMed  CAS  Google Scholar 

  • P. Breyne R. Dreesen K. Vandepoele L. Veylder ParticleDe F. Breusegem ParticleVan L. Callewaert S. Rombauts J. Raes B. Cannoot G. Engler D. Inze M. Zabeau (2002) ArticleTitleTranscriptome analysis during cell division in plants PNAS 99 14825–14830 Occurrence Handle10.1073/pnas.222561199 Occurrence Handle12393816 Occurrence Handle1:CAS:528:DC%2BD38Xpt1yrtrY%3D

    Article  PubMed  CAS  Google Scholar 

  • J. Callis R.D. Vierstra (2000) ArticleTitleProtein degradation in signaling Curr. Opin. Plant Biol. 3 381–386 Occurrence Handle10.1016/S1369-5266(00)00100-X Occurrence Handle11019805 Occurrence Handle1:CAS:528:DC%2BD3cXntVyqu7s%3D

    Article  PubMed  CAS  Google Scholar 

  • H. Cao S.A. Bowling A.S. Gordon X. Dong (1994) ArticleTitleCharacterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance Plant Cell 6 1583–1592 Occurrence Handle10.1105/tpc.6.11.1583 Occurrence Handle12244227 Occurrence Handle1:CAS:528:DyaK2MXitl2lsb8%3D

    Article  PubMed  CAS  Google Scholar 

  • H. Cao J. Glazebrook J.D. Clarke S. Volko X. Dong (1997) ArticleTitleThe Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats Cell 88 57–63 Occurrence Handle10.1016/S0092-8674(00)81858-9 Occurrence Handle9019406 Occurrence Handle1:CAS:528:DyaK2sXltFyruw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • W. Chen G. Chao K.B. Singh (1996) ArticleTitleThe promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1- binding sites Plant␣J. 10 955–966 Occurrence Handle9011080 Occurrence Handle1:CAS:528:DyaK2sXnsV2ltA%3D%3D

    PubMed  CAS  Google Scholar 

  • W. Chen K.B. Singh (1999) ArticleTitleThe auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element Plant J. 19 667–677 Occurrence Handle10.1046/j.1365-313x.1999.00560.x Occurrence Handle10571852 Occurrence Handle1:CAS:528:DyaK1MXntFOnsb8%3D

    Article  PubMed  CAS  Google Scholar 

  • I.P. Leon Particlede A. Sanz M. Hamberg C. Castresana (2002) ArticleTitleInvolvement of the Arabidopsis alpha-DOX1 fatty acid dioxygenase in protection against oxidative stress and cell death Plant J. 29 61–72 Occurrence Handle12060227

    PubMed  Google Scholar 

  • A. Paepe ParticleDe M. Vuylsteke P. Hummelen ParticleVan M. Zabeau D. Straeten ParticleVan Der (2004) ArticleTitleTranscriptional profiling by cDNA-AFLP and microarray analysis reveals novel insights into the early response to ethylene in Arabidopsis Plant J. 39 537–559 Occurrence Handle15272873

    PubMed  Google Scholar 

  • T.P. Delaney L. Friedrich J.A. Ryals (1995) ArticleTitleArabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance Proc. Natl. Acad. Sci. USA 92 6602–6606 Occurrence Handle11607555 Occurrence Handle1:CAS:528:DyaK2MXmslOjs7c%3D

    PubMed  CAS  Google Scholar 

  • C. Delessert I. Wilson D. Straeten ParticleVan Der E. Dennis R. Dolferus (2004) ArticleTitleSpatial and temporal analysis of the local response to wounding in Arabidopsis leaves Plant Mol. Biol. 55 165–181 Occurrence Handle10.1007/s11103-004-0112-7 Occurrence Handle15604673 Occurrence Handle1:CAS:528:DC%2BD2MXhsFajtA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • C. Despres C. DeLong S. Glaze E. Liu P.R. Fobert (2000) ArticleTitleThe Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors Plant Cell 12 279–290 Occurrence Handle10.1105/tpc.12.2.279 Occurrence Handle10662863 Occurrence Handle1:CAS:528:DC%2BD3cXktFagtb8%3D

    Article  PubMed  CAS  Google Scholar 

  • X. Dong (2004) ArticleTitleNPR1, all things considered Curr. Opin. Plant. Biol. 7 547–552 Occurrence Handle10.1016/j.pbi.2004.07.005 Occurrence Handle15337097 Occurrence Handle1:CAS:528:DC%2BD2cXntV2msLs%3D

    Article  PubMed  CAS  Google Scholar 

  • J. Draper (1997) ArticleTitleSalicylate, superoxide synthesis and cell suicide in plant defence Trends Plant Sci. 2 162–165 Occurrence Handle10.1016/S1360-1385(97)01030-3

    Article  Google Scholar 

  • F. Droog A. Spek A. Kooy Particlevan der A. Ruyter Particlede H. Hoge K. Libbenga P. Hooykaas B. Zaal Particlevan der (1995) ArticleTitlePromoter analysis of the auxin-regulated tobacco glutathione S-transferase genes Nt103-1 and Nt103-35 Plant Mol. Biol. 29 413–429 Occurrence Handle10.1007/BF00020974 Occurrence Handle8534842 Occurrence Handle1:CAS:528:DyaK28Xit1aqsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • W.E. Durrant X. Dong (2004) ArticleTitleSystemic acquired resistance Annu. Rev. Phytopathol. 42 185–209 Occurrence Handle10.1146/annurev.phyto.42.040803.140421 Occurrence Handle15283665 Occurrence Handle1:CAS:528:DC%2BD2cXotFyrtbs%3D

    Article  PubMed  CAS  Google Scholar 

  • R. Edwards D.P. Dixon V. Walbot (2000) ArticleTitlePlant glutathione S-transferases: enzymes with multiple functions in sickness and in health Trends Plant Sci. 5 193–198 Occurrence Handle10.1016/S1360-1385(00)01601-0 Occurrence Handle10785664 Occurrence Handle1:STN:280:DC%2BD3c3kvFalsg%3D%3D

    Article  PubMed  CAS  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 1377–1389 Occurrence Handle10.1105/tpc.001628 Occurrence Handle12084833 Occurrence Handle1:CAS:528:DC%2BD38Xlt1alsLk%3D

    Article  PubMed  CAS  Google Scholar 

  • B.J. Feys L.J. Moisan M.A. Newman J.E. Parker (2001) ArticleTitleDirect interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4 Embo J. 20 5400–5411 Occurrence Handle10.1093/emboj/20.19.5400 Occurrence Handle11574472 Occurrence Handle1:CAS:528:DC%2BD38XjtVSqtA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • T. Gaffney L. Friedrich B. Vernooij D. Negrotto G. Nye S. Uknes E. Ward H. Kessmann J. Ryals (1993) ArticleTitleRequierement of salicylic acid for the induction of systemic acquired resistance Science 250 754–756

    Google Scholar 

  • V. Garreton J. Carpinelli X. Jordana L. Holuigue (2002) ArticleTitleThe as-1 promoter element is an oxidative stress-responsive element and salicylic acid activates it via oxidative species Plant Physiol. 130 1516–1526 Occurrence Handle10.1104/pp.009886 Occurrence Handle12428016 Occurrence Handle1:CAS:528:DC%2BD38XovVOmsbo%3D

    Article  PubMed  CAS  Google Scholar 

  • J. Glazebrook E.E. Rogers F.M. Ausubel (1996) ArticleTitleIsolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening Genetics 143 973–982 Occurrence Handle8725243 Occurrence Handle1:CAS:528:DyaK28XjvV2htLk%3D

    PubMed  CAS  Google Scholar 

  • Y. He H. Fukushige D.F. Hildebrand S. Gan (2002) ArticleTitleEvidence supporting a role of jasmonic acid in Arabidopsis leaf senescence Plant Physiol. 128 876–884 Occurrence Handle10.1104/pp.010843 Occurrence Handle11891244 Occurrence Handle1:CAS:528:DC%2BD38Xit1Gqtrc%3D

    Article  PubMed  CAS  Google Scholar 

  • Y. He S. Gan (2001) ArticleTitleIdentical promoter elements are involved in regulation of the OPR1 gene by senescence and jasmonic acid in Arabidopsis Plant Mol Biol. 47 595–605 Occurrence Handle10.1023/A:1012211011538 Occurrence Handle11725945 Occurrence Handle1:CAS:528:DC%2BD3MXovVylu78%3D

    Article  PubMed  CAS  Google Scholar 

  • Z.-H. He D. He B.D. Kohorn (1998) ArticleTitleRequirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response Plant J. 14 55–63 Occurrence Handle10.1046/j.1365-313X.1998.00092.x Occurrence Handle9681026 Occurrence Handle1:CAS:528:DyaK1cXjtV2is7k%3D

    Article  PubMed  CAS  Google Scholar 

  • K. Higo Y. Ugawa M. Iwamoto T. Korenaga (1999) ArticleTitlePlant cis-acting regulatory DNA elements (PLACE) database: 1999 Nucleic Acids Res. 27 297–300 Occurrence Handle10.1093/nar/27.1.297 Occurrence Handle9847208 Occurrence Handle1:CAS:528:DyaK1MXpsVKgug%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • D.M. Horvath N.H. Chua (1996) ArticleTitleIdentification of an immediate-early salicylic acid-inducible tobacco gene and characterization of induction by other compounds Plant Mol. Biol. 31 1061–1072 Occurrence Handle10.1007/BF00040724 Occurrence Handle8843948 Occurrence Handle1:CAS:528:DyaK28XmtFGisrY%3D

    Article  PubMed  CAS  Google Scholar 

  • D.M. Horvath D.J. Huang N.H. Chua (1998) ArticleTitleFour classes of salicylate-induced tobacco genes Mol. Plant Microbe Interact. 11 895–905 Occurrence Handle9725022 Occurrence Handle1:CAS:528:DyaK1cXls1Sjsb8%3D

    PubMed  CAS  Google Scholar 

  • C. Johnson E. Boden J. Arias (2003) ArticleTitleSalicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis Plant Cell 15 1846–1858 Occurrence Handle10.1105/tpc.012211 Occurrence Handle12897257 Occurrence Handle1:CAS:528:DC%2BD3sXms1Wlsb0%3D

    Article  PubMed  CAS  Google Scholar 

  • C. Johnson E. Boden M. Desai P. Pascuzzi J. Arias (2001) ArticleTitleIn vivo target promoter-binding activities of a xenobiotic stress-activated TGA factor Plant J. 28 237–243 Occurrence Handle10.1046/j.1365-313X.2001.01147.x Occurrence Handle11722767 Occurrence Handle1:CAS:528:DC%2BD3MXovV2ksb8%3D

    Article  PubMed  CAS  Google Scholar 

  • M. Kinkema W. Fan X. Dong (2000) ArticleTitleNuclear localization of NPR1 is required for activation of PR gene expression Plant Cell 12 2339–2350 Occurrence Handle10.1105/tpc.12.12.2339 Occurrence Handle11148282 Occurrence Handle1:CAS:528:DC%2BD3MXns1Shtg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • S. Krawczyk C. Thurow R. Niggeweg C. Gatz (2002) ArticleTitleAnalysis of the spacing between the two palindromes of activation sequence-1 with respect to binding to different TGA factors and transcriptional activation potential Nucleic Acids Res. 30 775–781 Occurrence Handle10.1093/nar/30.3.775 Occurrence Handle11809891 Occurrence Handle1:CAS:528:DC%2BD38XhsVyhtLg%3D

    Article  PubMed  CAS  Google Scholar 

  • E. Lam P.N. Benfey P.M. Gilmartin R.X. Fang N.H. Chua (1989) ArticleTitleSite-specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants Proc. Natl. Acad. Sci. USA 86 7890–7894 Occurrence Handle2813365 Occurrence Handle1:CAS:528:DyaL1MXmt1Knsrk%3D

    PubMed  CAS  Google Scholar 

  • E. Lebel P. Heifetz L. Thorne S. Uknes J. Ryals E. Ward (1998) ArticleTitleFunctional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis Plant J. 16 223–233 Occurrence Handle10.1046/j.1365-313x.1998.00288.x Occurrence Handle9839467 Occurrence Handle1:CAS:528:DyaK1cXnvFKqsbg%3D

    Article  PubMed  CAS  Google Scholar 

  • Y. Li S. Baldauf E.K. Lim D.J. Bowles (2001) ArticleTitlePhylogenetic analysis of the UDP-glycosyltransferase multigene family of Arabidopsis thaliana J. Biol. Chem. 276 4338–4343 Occurrence Handle11042215 Occurrence Handle1:CAS:528:DC%2BD3MXht1GnsLk%3D

    PubMed  CAS  Google Scholar 

  • E.K. Lim C.J. Doucet Y. Li L. Elias D. Worrall S.P. Spencer J. Ross D.J. Bowles (2002) ArticleTitleThe activity of␣Arabidopsis glycosyltransferases toward salicylic acid, 4-hydroxybenzoic acid, and other benzoates J. Biol. Chem. 277 586–592 Occurrence Handle11641410 Occurrence Handle1:CAS:528:DC%2BD38XjslGntQ%3D%3D

    PubMed  CAS  Google Scholar 

  • X. Liu E. Lam (1994) ArticleTitleTwo binding sited for the plant transcription factor ASF-1 can respond to auxin treatments in transgenic tobacco J. Biol. Chem. 269 668–675 Occurrence Handle8276868 Occurrence Handle1:CAS:528:DyaK2cXntVOhsA%3D%3D

    PubMed  CAS  Google Scholar 

  • R. Mahalingam A. Gomez-Buitrago N. Eckardt N. Shah A. Guevara-Garcia P. Day R. Raina N. Fedoroff (2003) ArticleTitleCharacterizing the stress/defense transcriptome of Arabidopsis Genome Biol. 4 R20.1–R20.13 Occurrence Handle10.1186/gb-2003-4-3-r20

    Article  Google Scholar 

  • K. Maleck A. Levine T. Eulgem A. Morgan J. Schmid K.A. Lawton J.L. Dangl R.A. Dietrich (2000) ArticleTitleThe transcriptome of Arabidopsis thaliana during systemic acquired resistance Nat. Genet. 26 403–410 Occurrence Handle11101835 Occurrence Handle1:CAS:528:DC%2BD3cXptVWgsbk%3D

    PubMed  CAS  Google Scholar 

  • K.A. Marrs (1996) ArticleTitleThe functions and regulation of glutathione S-transferases in plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 47 127–158 Occurrence Handle10.1146/annurev.arplant.47.1.127 Occurrence Handle15012285 Occurrence Handle1:CAS:528:DyaK28XjtlWgsbo%3D

    Article  PubMed  CAS  Google Scholar 

  • H. Matsumura S. Reich A. Ito H. Saitoh S. Kamoun P. Winter G. Kahl M. Reuter D.H. Kruger R. Terauchi (2003) ArticleTitleGene expression analysis of plant host–pathogen interactions by SuperSAGE PNAS 100 15718–15723 Occurrence Handle10.1073/pnas.2536670100 Occurrence Handle14676315 Occurrence Handle1:CAS:528:DC%2BD2cXhtVCnsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • Z. Mou W. Fan X. Dong (2003) ArticleTitleInducers of plant systemic acquired resistance regulate NPR1 function through redox changes Cell 113 935–944 Occurrence Handle10.1016/S0092-8674(03)00429-X Occurrence Handle12837250 Occurrence Handle1:CAS:528:DC%2BD3sXlsVSjur8%3D

    Article  PubMed  CAS  Google Scholar 

  • G. Neuhaus G. Neuhaus-Url F. Katagiri K. Seipel N-H. Chua (1994) ArticleTitleTissue-specific expression of as-1 in transgenic tobacco Plant Cell 6 827–834 Occurrence Handle10.1105/tpc.6.6.827 Occurrence Handle12244260 Occurrence Handle1:CAS:528:DyaK2MXit1SjtQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • R. Niggeweg C. Thurow C. Kegler C. Gatz (2000a) ArticleTitleTobacco transcription factor TGA2.2 is the main component of as-1-binding factor ASF-1 and is involved in salicylic acid- and auxin-inducible expression of as-1-containing target promoters J. Biol. Chem. 275 19897–19905 Occurrence Handle10.1074/jbc.M909267199 Occurrence Handle1:CAS:528:DC%2BD3cXkslahtbg%3D

    Article  CAS  Google Scholar 

  • R. Niggeweg C. Thurow R. Weigel U. Pfitzner C. Gatz (2000b) ArticleTitleTobacco TGA factors differ with respect to interaction with NPR1, activation potential and DNA-binding properties Plant Mol. Biol. 42 775–788 Occurrence Handle10.1023/A:1006319113205 Occurrence Handle1:CAS:528:DC%2BD3cXjt1Grt7o%3D

    Article  CAS  Google Scholar 

  • T. Nurnberger D. Scheel (2001) ArticleTitleSignal transmission in the plant immune response Trends Plant Sci. 6 372–379 Occurrence Handle11495791 Occurrence Handle1:CAS:528:DC%2BD3MXmtFCkur8%3D

    PubMed  CAS  Google Scholar 

  • K. Overmyer M. Brosche J. Kangasjarvi (2003) ArticleTitleReactive oxygen species and hormonal control of cell death Trends Plant Sci. 8 335–342 Occurrence Handle10.1016/S1360-1385(03)00135-3 Occurrence Handle12878018 Occurrence Handle1:CAS:528:DC%2BD3sXls1CjtLg%3D

    Article  PubMed  CAS  Google Scholar 

  • J.H. Park S.A. Oh Y.H. Kim H.R. Woo H.G. Nam (1998) ArticleTitleDifferential expression of senescence-associated mRNAs during leaf senescence induced by different senescence-inducing factors in Arabidopsis Plant Mol. Biol. 37 445–454 Occurrence Handle10.1023/A:1005958300951 Occurrence Handle9617812 Occurrence Handle1:CAS:528:DyaK1cXjtlOjs7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • D. Pontier Z.H. Miao E. Lam (2001) ArticleTitleTrans-dominant suppression of plant TGA factors reveals their negative and positive roles in plant defense responses Plant J. 27 529–538 Occurrence Handle10.1046/j.1365-313X.2001.01086.x Occurrence Handle11576436 Occurrence Handle1:CAS:528:DC%2BD3MXos12ktL4%3D

    Article  PubMed  CAS  Google Scholar 

  • X.F. Qin L. Holuigue D.M. Horvath N.H. Chua (1994) ArticleTitleImmediate early transcription activation by salicylic acid via the cauliflower mosaic virus as-1 element Plant Cell 6 863–874 Occurrence Handle10.1105/tpc.6.6.863 Occurrence Handle8061520 Occurrence Handle1:CAS:528:DyaK2MXit1Sjuw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • J.A. Quiel J. Bender (2003) ArticleTitleGlucose conjugation of anthranilate by the Arabidopsis UGT74F2 glucosyltransferase is required for tryptophan mutant blue fluorescence J. Biol. Chem. 278 6275–6281 Occurrence Handle10.1074/jbc.M211822200 Occurrence Handle12475971 Occurrence Handle1:CAS:528:DC%2BD3sXht1aqu7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • M. Reijans R. Lascaris A.O. Groeneger A. Wittenberg E. Wesselink J. Oeveren Particlevan E. Wit Particlede A. Boorsma B. Voetdijk H. Spek Particlevan der L.A. Grivell G. Simons (2003) ArticleTitleQuantitative comparison of cDNA-AFLP, microarrays, and GeneChip expression data in Saccharomyces cerevisiae Genomics 82 606–618 Occurrence Handle10.1016/S0888-7543(03)00179-4 Occurrence Handle14611802 Occurrence Handle1:CAS:528:DC%2BD3sXoslOgtb0%3D

    Article  PubMed  CAS  Google Scholar 

  • F. Schaller C. Biesgen C. Mussig T. Altmann E.W. Weiler (2000) ArticleTitle12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis Planta 210 979–984 Occurrence Handle10872231 Occurrence Handle1:CAS:528:DC%2BD3cXjtVWrtLw%3D

    PubMed  CAS  Google Scholar 

  • P.M. Schenk K. Kazan I. Wilson J.P. Anderson T. Richmond S.C. Somerville J.M. Manners (2000) ArticleTitleCoordinated plant defense responses in Arabidopsis revealed by microarray analysis Proc. Natl. Acad. Sci. USA 97 11655–11660 Occurrence Handle10.1073/pnas.97.21.11655 Occurrence Handle11027363 Occurrence Handle1:CAS:528:DC%2BD3cXnsF2qtro%3D

    Article  PubMed  CAS  Google Scholar 

  • J. Shah (2005) ArticleTitleLipids, lipases, and modifying enzymes in plant diseases resistance Annu Rev. Phytopathol. 43 8.1–8.32 Occurrence Handle10.1146/annurev.phyto.43.040204.135951

    Article  Google Scholar 

  • G. Strompen R. Gruner U.M. Pfitzner (1998) ArticleTitleAn as-1-like motif controls the level of expression of the gene for the pathogenesis-related protein 1a from tobacco Plant Mol. Biol. 37 871–883 Occurrence Handle10.1023/A:1006003916284 Occurrence Handle9678582 Occurrence Handle1:CAS:528:DyaK1cXkvVyrtbk%3D

    Article  PubMed  CAS  Google Scholar 

  • G. Thijs M. Lescot K. Marchal S. Rombauts B. Moor ParticleDe P. Rouze Y. Moreau (2001) ArticleTitleA higher-order background model improves the detection of promoter regulatory elements by Gibbs sampling Bioinformatics 17 1113–1122 Occurrence Handle10.1093/bioinformatics/17.12.1113 Occurrence Handle11751219 Occurrence Handle1:CAS:528:DC%2BD38XmtVCmtA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • G. Thijs K. Marchal M. Lescot S. Rombauts B. Moor ParticleDe P. Rouze Y. Moreau (2002) ArticleTitleA Gibbs sampling method to detect overrepresented motifs in the upstream regions of coexpressed genes J. Comput. Biol. 9 447–464 Occurrence Handle10.1089/10665270252935566 Occurrence Handle12015892 Occurrence Handle1:CAS:528:DC%2BD3sXotVSqsbo%3D

    Article  PubMed  CAS  Google Scholar 

  • S. Uknes S. Dincher L. Friedrich D. Negrotto S. Williams H. Thompson-Taylor S. Potter E. Ward J. Ryals (1993) ArticleTitleRegulation of pathogenesis-related protein-1a gene expression in tobacco Plant Cell 5 159–169 Occurrence Handle10.1105/tpc.5.2.159 Occurrence Handle8453300 Occurrence Handle1:CAS:528:DyaK3sXitVKltLw%3D

    Article  PubMed  CAS  Google Scholar 

  • C. Uquillas I. Letelier F. Blanco X. Jordana L. Holuigue (2004) ArticleTitleNPR1-independent activation of immediate early salicylic acid-responsive genes in Arabidopsis Mol. Plant Microbe Interact. 17 34–42 Occurrence Handle14714866 Occurrence Handle1:CAS:528:DC%2BD2cXivVSltrw%3D

    PubMed  CAS  Google Scholar 

  • L. Loon ParticleVan E. Strien ParticleVan (1999) ArticleTitleThe families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins Physiol. Mol. Plant Pathol. 55 85–97

    Google Scholar 

  • S. Vandenabeele S. Vanderauwera M. Vuylsteke S. Rombauts C. Langebartels H.K. Seidlitz M. Zabeau M. Montagu ParticleVan D. Inze F. Breusegem ParticleVan (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 Handle15200641 Occurrence Handle1:CAS:528:DC%2BD2cXms1ykur4%3D

    Article  PubMed  CAS  Google Scholar 

  • T. Vogt P. Jones (2000) ArticleTitleGlycosyltransferases in plant natural product synthesis: characterization of a supergene family Trends Plant Sci. 5 380–386 Occurrence Handle10.1016/S1360-1385(00)01720-9 Occurrence Handle10973093 Occurrence Handle1:STN:280:DC%2BD3M%2FjslKhsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • U. Wagner R. Edwards D.P. Dixon F. Mauch (2002) ArticleTitleProbing the diversity of the Arabidopsis glutathione S-transferase gene family Plant Mol. Biol. 49 515–532 Occurrence Handle10.1023/A:1015557300450 Occurrence Handle12090627 Occurrence Handle1:CAS:528:DC%2BD38XkvVWrurY%3D

    Article  PubMed  CAS  Google Scholar 

  • E. Wingender P. Dietze H. Karas R. Knuppel (1996) ArticleTitleTRANSFAC: a database on transcription factors and their DNA binding sites Nucleic Acids Res. 24 238–241 Occurrence Handle10.1093/nar/24.1.238 Occurrence Handle8594589 Occurrence Handle1:CAS:528:DyaK28XnsFSiug%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • C. Xiang Z.H. Miao E. Lam (1996) ArticleTitleCoordinated activation of as-1-type elements and a tobacco glutathione S-transferase gene by auxins, salicylic acid, methyl-jasmonate and hydrogen peroxide Plant Mol. Biol. 32 415–426 Occurrence Handle10.1007/BF00019093 Occurrence Handle8980490 Occurrence Handle1:CAS:528:DyaK2sXitVersg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • N Yalpani L.J A.J. Enyedi I Raskin (1994) ArticleTitleUltraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis related proteins and virus resistance in tobacco Planta 193 372–376 Occurrence Handle10.1007/BF00201815 Occurrence Handle1:CAS:528:DyaK2cXitl2iurc%3D

    Article  CAS  Google Scholar 

  • Y. Zhang W. Fan M. Kinkema X. Li X. Dong (1999) ArticleTitleInteraction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene Proc. Natl. Acad. Sci. USA 96 6523–6528 Occurrence Handle10339621 Occurrence Handle1:CAS:528:DyaK1MXksFKktbY%3D

    PubMed  CAS  Google Scholar 

  • Y. Zhang M.J. Tessaro M. Lassner X. Li (2003) ArticleTitleKnockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance Plant Cell 15 2647–2653 Occurrence Handle14576289 Occurrence Handle1:CAS:528:DC%2BD3sXpt1Orur8%3D

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, P.O. Box 114-D, Santiago, Chile

    Francisca Blanco, Virginia Garretón, Nicolas Frey, Xavier Jordana & Loreto Holuigue

  2. Centro de Genómica y Bioinformática, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, P.O. Box 114-D, Santiago, Chile

    Calixto Dominguez & Tomás Pérez-Acle

  3. Department of Molecular Genetics, Unit Plant Hormone Signaling and Bio-imaging, Ghent University, Ledeganckstraat 35, B-9000, Gent, Belgium

    Francisca Blanco & Dominique Van der Straeten

  4. AustralBiotech SA., San Sebastian 2952, piso 5. Las Condes., Santiago, Chile

    Virginia Garretón

Authors
  1. Francisca Blanco
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Virginia Garretón
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicolas Frey
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Calixto Dominguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tomás Pérez-Acle
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dominique Van der Straeten
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xavier Jordana
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Loreto Holuigue
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Loreto Holuigue.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blanco, F., Garretón, V., Frey, N. et al. Identification of NPR1-Dependent and Independent Genes Early Induced by Salicylic Acid Treatment in Arabidopsis. Plant Mol Biol 59, 927–944 (2005). https://doi.org/10.1007/s11103-005-2227-x

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-005-2227-x

Keywords

Search

Navigation