Location via proxy:   [ UP ]  
[Report a bug]   [Manage cookies]                
Skip to main content
Springer Nature Link
Log in

Light conditions influence specific defence responses in incompatible plant–pathogen interactions: uncoupling systemic resistance from salicylic acid and PR-1 accumulation

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

In incompatible plant–pathogen interactions, disease resistance is generated by rapid activation of a multitude of plant defence reactions. Little is known about the dependency of these resistance responses on external factors. The plasticity of plant defence mechanisms in terms of light conditions is studied here. Interaction of Arabidopsis thaliana (L.) Heynh. with an avirulent strain of Pseudomonas syringae pv. maculicola in the dark resulted in increased apoplastic bacterial growth and therefore reduced local resistance as compared to an infection process in the presence of light. Several characteristic defence reactions, including activation of phenylalanine ammonia-lyase, accumulation of salicylic acid (SA), expression of the pathogenesis-related protein PR-1 and the development of a microscopically defined hypersensitive response, proved to be light dependent. In contrast, the extent of the oxidative burst, as estimated by induction of the protectant gene glutathione-S-transferase, was not weakened by the absence of light. Moreover, pathogen-induced accumulation of jasmonic acid, production of the phytoalexin camalexin and transcriptional induction of a pathogen-inducible myrosinase were even more pronounced in the dark. Apart from affecting local defence responses, light also influenced the establishment of systemic acquired resistance (SAR). SAR development in response to infection by avirulent bacteria was completely lost when the primary infection process occurred in the absence of light. SAR developed both under medium (70 μmol photons m−2 s−1) and strong (500 μmol photons m−2 s−1) light conditions but was in the latter case not associated with an accumulation of SA and PR-1 in systemic leaves, demonstrating that SAR can be executed independently from these molecular SAR markers. Our results are consistent with the notion that SA accumulation in infected primary leaves is necessary for induction of systemic resistance and indicate that defence mechanisms different from SA signalling and PR-protein action exist in systemic tissue to confer resistance during SAR.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4a, b
Fig. 5a, b
Fig. 6
Fig. 7a–c

Similar content being viewed by others

Abbreviations

HR :

Hypersensitive response

JA :

Jasmonic acid

PAL :

Phenylalanine ammonia-lyase

PFD :

Photon flux density

pi :

Post infection

PR :

Pathogenesis-related

Psm :

Pseudomonas syringae pv. maculicola

ROI :

Reactive oxygen intermediate

SA :

Salicylic acid

SAG :

Salicylic acid glucoside

SAR :

Systemic acquired resistance

References

  • Alexander D, Goodman RM, Gut-Rella M, Glascock C, Weymann K, Friedrich L, Maddox D, Ahl-Goy P, Luntz T, Ward E, Ryals J (1993) Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein-1a. Proc Natl Acad Sci USA 90:7327–7331

    CAS  PubMed  Google Scholar 

  • Alvarez ME, Pennell RI, Meijer, P-J, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784

    CAS  PubMed  Google Scholar 

  • Asai T, Stone JM, Heard JE, Kovtun Y, Yorgey P, Sheen J, Ausubel FM (2000) Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell 12:1823–1836

    Google Scholar 

  • Bau S (2001) Untersuchungen zur Jasmonat-Signaltransduktion in Arabidopsis thaliana anhand des Jasmonat-regulierten Gens Atjrg21. Dissertation, Halle-Wittenberg

  • Bisgrove SR, Simonich MT, Smith NM, Sattler A, Innes RW (1994) A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6:927–933

    Article  CAS  PubMed  Google Scholar 

  • Brader G, Tas E, Palva ET (2001) Jasmonate-dependent induction of glucosinolates in Arabidopsis by culture filtrates of the non-specific pathogen Erwinia carotovora. Plant Physiol 126:849–860

    Article  CAS  PubMed  Google Scholar 

  • Brodersen P, Petersen M, Pike HN, Olszak B, Skov-Petersen S, Oedum N, Joergensen LB, Brown RE, Mundy J (2002) Knockout of Arabidopsis ACCELERATED-CELL-DEATH11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev 16:490–502

    Article  CAS  PubMed  Google Scholar 

  • Clarke JD, Liu Y, Klessig DF, Dong X (1998) Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell 10:557–569

    Article  CAS  PubMed  Google Scholar 

  • Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gutrella M, Kessmann H, Ward E, Ryals J (1994) A central role of salicylic acid in plant disease resistance. Science 266:1247–1250

    CAS  Google Scholar 

  • Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive response. Proc Natl Acad Sci USA 98:13454–13459

    CAS  PubMed  Google Scholar 

  • Dewdney J, Reuber TL, Wildermuth MC, Devoto A, Cui J, Stutius LM, Drummond EP, Ausubel FM (2000) Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J 24:205–218

    Article  CAS  PubMed  Google Scholar 

  • Epple P, Apel K, Bohlmann H (1995) An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol 109:813–820

    CAS  PubMed  Google Scholar 

  • Felton GW, Korth KL, Bi JL, Wesley SV, Huhman DV, Mathews MC, Murphy JB, Lamb C, Dixon RA (1999) Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Curr Biol 9:317–320

    CAS  PubMed  Google Scholar 

  • Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756

    CAS  Google Scholar 

  • Genoud T, Buchala AJ, Chua NH, Metraux JP (2002) Phytochrome signalling modulates the SA-perceptive pathway in Arabidopsis. Plant J 31:87–95

    Article  CAS  PubMed  Google Scholar 

  • Glazebrook J Ausubel FM (1994) Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci USA 91:8955–8959

    CAS  Google Scholar 

  • Glazebrook J, Chen W, Estes B, Chang H-S, Nawrath C, Métraux J-P, Zhu T, Katagiri F (2003). Topology of the network integrating salicylic acid and jasmonate signal transduction derived from global expression phenotyping. Plant J 34:217–228

    CAS  PubMed  Google Scholar 

  • Graham TL, Graham MY (1996) Signaling in soybean phenylpropanoid responses (dissection of primary, secondary, and conditioning effects of light, wounding, and elicitor treatments). Plant Physiol 110:1123–1133

    CAS  PubMed  Google Scholar 

  • Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657

    Article  CAS  PubMed  Google Scholar 

  • Kenton P, Mur LAJ, Atzorn R, Wasternack C, Draper J (1999) (−)-Jasmonic acid accumulation in tobacco hypersensitive response lesions. Mol Plant Microbe Interact 12:74–78

    CAS  Google Scholar 

  • Kim HS, Delaney TP (2002) Arabidopsis SON1 regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance. Plant Cell 14:1469–1482

    Google Scholar 

  • Kinkema M, Fan W, Dong X (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12:2339–2350

    Google Scholar 

  • Kloek AP, Verbsky ML, Sharma SB, Schoelz JE, Vogel J, Klessig DF, Kunkel BN (2001) Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J 26:509–522

    Article  CAS  PubMed  Google Scholar 

  • Koch E, Slusarenko AJ (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2:437–445

    Article  CAS  PubMed  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275

    CAS  Google Scholar 

  • Levine A, Tenhaken R, Dixon RA, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive response. Cell 79:583–593

    CAS  PubMed  Google Scholar 

  • Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid. A likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002–1004

    CAS  Google Scholar 

  • Mauch-Mani B, Slusarenko AJ (1996) Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8:203–212

    Article  CAS  PubMed  Google Scholar 

  • Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944

    CAS  PubMed  Google Scholar 

  • Mueller MJ, Brodschelm W (1994) Quantification of jasmonic acid by capillary gas chromatography–negative chemical ionization–mass spectrometry. Anal Biochem 218:425–435

    Article  CAS  PubMed  Google Scholar 

  • Nawrath C, Métraux JP (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11:1393–1404

    CAS  PubMed  Google Scholar 

  • Nawrath C, Heck S, Parinthawong N, Métraux JP (2002) EDS5, 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

    CAS  PubMed  Google Scholar 

  • Pieterse CM, van Wees SC, Hoffland E, van Pelt JA, van Loon LC (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8:1225–1237

    CAS  PubMed  Google Scholar 

  • Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1:404–411

    CAS  PubMed  Google Scholar 

  • Rogers EE, Ausubel FM (1997) Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. Plant Cell 9:305–316

    Article  CAS  PubMed  Google Scholar 

  • Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819

    CAS  Google Scholar 

  • Shulaev V, Leon J, Raskin I (1995) Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? Plant Cell 7:1691–1701

    Google Scholar 

  • Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala, AJ, Métraux J-P, Brown R, Kazan K, Van Loon LC, Dong X, Pieterse CMJ (2003) NPR1 modulates cross talk between salicylic acid- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770

    Google Scholar 

  • Sticher L, Mauch-Mani B, Metraux JP (1997) Systemic acquired resistance. Annu Rev Phytopathol 35:235–270

    CAS  Google Scholar 

  • Tenhaken R, Rubel C (1997) Salicylic acid is needed in hypersensitive cell death in soybean but does not act as a catalase inhibitor. Plant Physiol 115:291–298

    CAS  PubMed  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei YD, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley–powdery mildew interaction. Plant J 11:1187–1194

    CAS  Google Scholar 

  • Ton J, De Vos M, Robben C, Buchala AJ, Métraux J-P, Van Loon LC, Pieterse CMJ (2002) Characterization of Arabidopsis enhanced disease susceptibility mutants that are affected in systemically induced resistance. Plant J 29:11–21

    Article  CAS  PubMed  Google Scholar 

  • Tsuji J, Jackson EP, Gage DA, Hammerschmidt R, Somerville SC (1992) Phytoalexin accumulation in Arabidopsis thaliana during the hypersensitive reaction to Pseudomonas syringae pv. syringae. Plant Physiol 98:1304–1309

    CAS  Google Scholar 

  • Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J (1992) Acquired resistance in Arabidopsis. Plant Cell 4:645–656

    CAS  PubMed  Google Scholar 

  • van Wees SC, Glazebrook J (2003) Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. phaseolicola is due to degradation products of salicylic acid. Plant J 33:733–742

    Article  PubMed  Google Scholar 

  • Verberne MC, Verpoorte R, Bol JF, Mercado-Blanco J, Linthorst HJM (2000) Overproduction of salicylic acid in plants by bacterial transgenes results in enhanced resistance to pathogens. Nature Biotechnol 18:779–783

    Article  CAS  Google Scholar 

  • Vernooij B, Friedrich L, Morse A, Reist R, Kolditzjawhar R, Ward E, Uknes S, Kessmann H, Ryals J (1994) Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6:959–965

    Article  CAS  PubMed  Google Scholar 

  • Volko SM, Boller T, Ausubel FM (1998) Isolation of new Arabidopsis mutants with enhanced disease susceptibility to Pseudomonas syringae by direct screening. Genetics 149:537–548

    Google Scholar 

  • Weymann K, Hunt M, Uknes S, Neuenschwander U, Lawton K, Steiner H-Y, Ryals J (1995) Suppression and restoration of lesion formation in Arabidopsis lsd mutants. Plant Cell 7:2013–2022

    CAS  Google Scholar 

  • White RF (1979) Acetylsalicylic acid (Aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99:410–412

    CAS  Google Scholar 

  • Wildermuth MC, Dewdney J, Wu G, Ausubel, FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565

    Article  CAS  PubMed  Google Scholar 

  • Wittstock U, Halkier BA (2002) Glucosinolate research in the Arabidopsis era. Trends Plant Sci 7:263–270

    Article  CAS  PubMed  Google Scholar 

  • Xue JP, Jorgensen M, Pihlgren U, Rask L (1995) The myrosinase gene family in Arabidopsis thaliana—gene organization, expression and evolution. Plant Mol Biol 27:911–922

    CAS  PubMed  Google Scholar 

  • Yang K-Y, Kim E-Y, Kim C-S, Guh J-O, Kim K-C, Cho B-H (1998) Characterization of a glutathione S-transferase gene ATGST1 in Arabidopsis thaliana. Plant Cell Rep 17:700–704

    Article  CAS  Google Scholar 

  • Zhou N, Tootle TL, Tsui F, Klessig DF, Glazebrook J (1998) PAD4 functions upstream from salicylic acid to control defence responses in Arabidopsis. Plant Cell 10:1021–1030

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgement

We thank Dr. Gabriele Gresser (Department of Pharmaceutical Biology, Würzburg) for JA analysis.

Author information

Authors and Affiliations

  1. Julius-von-Sachs-Institute of Biological Science, University of Würzburg, Julius-von-Sachs-Platz 3, 97082, Würzburg, Germany

    Jürgen Zeier, Bianka Pink, Martin J. Mueller & Susanne Berger

Authors
  1. Jürgen Zeier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bianka Pink
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin J. Mueller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Susanne Berger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jürgen Zeier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zeier, J., Pink, B., Mueller, M.J. et al. Light conditions influence specific defence responses in incompatible plant–pathogen interactions: uncoupling systemic resistance from salicylic acid and PR-1 accumulation. Planta 219, 673–683 (2004). https://doi.org/10.1007/s00425-004-1272-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-004-1272-z

Keywords

Search

Navigation