Skip to main content
SpringerLink
Log in

Endogenous jasmonic and salicylic acids levels in the Cd-hyperaccumulator Noccaea (Thlaspi) praecox exposed to fungal infection and/or mechanical stress

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Sensitivity to Erysiphe in Noccaea praecox with low metal supply is related to the failure in enhancing SA. Cadmium protects against fungal-infection by direct toxicity and/or enhanced fungal-induced JA signaling.

Abstract

Metal-based defense against biotic stress is an attractive hypothesis on evolutionary advantages of plant metal hyperaccumulation. Metals may compensate for a defect in biotic stress signaling in hyperaccumulators (metal-therapy) by either or both direct toxicity to pathogens and by metal-induced alternative signaling pathways. Jasmonic acid (JA) and salicylic acid (SA) are well-established components of stress signaling pathways. However, few studies evaluate the influence of metals on endogenous concentrations of these defense-related hormones. Even less data are available for metal hyperaccumulators. To further test the metal-therapy hypothesis we analyzed endogenous SA and JA concentrations in Noccaea praecox, a cadmium (Cd) hyperaccumulator. Plants treated or not with Cd, were exposed to mechanical wounding, expected to enhance JA signaling, and/or to infection by biotrophic fungus Erysiphe cruciferarum for triggering SA. JA and SA were analyzed in leaf extracts using LC–ESI(−)–MS/MS. Plants without Cd were more susceptible to fungal attack than plants receiving Cd. Cadmium alone tended to increase leaf SA but not JA. Either or both fungal attack and mechanical wounding decreased SA levels and enhanced JA in the Cd-rich leaves of plants exposed to Cd. High leaf Cd in N. praecox seems to hamper biotic-stress-induced SA, while triggering JA signaling in response to fungal attack and wounding. To the best of our knowledge, this is the first report on the endogenous JA and SA levels in a Cd-hyperaccumulator exposed to different biotic and abiotic stresses. Our results support the view of a defect in SA stress signaling in Cd hyperaccumulating N. praecox.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

    CAS  Google Scholar 

  • Behmer ST, Lloyd CM, Raubenheimer D, Stewart-Clark J, Kneight J, Leighton RS, Harper FA, Smith JAC (2005) Metal hyperaccumulation in plants: mechanisms of defence against insect herbivores. Funct Ecol 19:55–66

    Article  Google Scholar 

  • Boyd RS (2004) Ecology of metal hyperaccumulation. New Phytol 162:563–567

    Article  Google Scholar 

  • Boyd RS (2012) Plant defense using toxic inorganic ions: conceptual models of the defensive enhancement and joint effects hypotheses. Plant Sci 195:88–95

    Article  PubMed  CAS  Google Scholar 

  • Boyd RS, Jhee EM (2005) A test of elemental defence against slugs by Ni in hyperaccumulator and non-hyperaccumulator Streptanthus species. Chemoecology 15:179–185

    Article  CAS  Google Scholar 

  • Cabot C, Gallego B, Martos S, Barcelo J, Poschenrieder C (2013) Signal cross talk in Arabidopsis exposed to cadmium, silicon, and Botrytis cinerea. Planta 237:337–349

    Article  PubMed  CAS  Google Scholar 

  • Cui W, Li L, Gao ZZ, Wu HH et al (2012) Haem oxygenase-1 is involved in salicylic acid-induced alleviation of oxidative stress due to cadmium stress in Medicago sativa. J Exp Bot 63:5521–5534

    Article  PubMed  CAS  Google Scholar 

  • DalCorso G, Farinati S, Furini A (2010) Regulatory networks of cadmium stress in plants. Plant Signal Behav 5(6):663–667

    Article  PubMed  CAS  Google Scholar 

  • Epstein E (1972) Mineral nutrition of plants: principles and perspectives. Wiley, New York

    Google Scholar 

  • Fones H, Davis CAR, Rico A et al (2010) Metal hyperaccumulation armors plants against disease. PLoS Pathog 6:e1001093

    Article  PubMed  Google Scholar 

  • Freeman JL, Garcia D, Kim D, Hopf A, Salt DE (2005) Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiol 137:1082–1091

    Article  PubMed  CAS  Google Scholar 

  • Galeas ML, Klamper EM, Bennett LE, Freeman JL, Kondratieff BC, Quinn CF, Pilon-Smits EAH (2008) Selenium hyperaccumulation reduces plant arthropod loads in the field. New Phytol 177:715–724

    Article  PubMed  CAS  Google Scholar 

  • Ghaderian YSM, Lyon AJE, Baker AJM (2000) Seedling mortality of metal hyperaccumulator plants resulting from damping off by Pythium spp. New Phytol 146:219–224

    Article  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  PubMed  CAS  Google Scholar 

  • Guo Y, Gan S-S (2012) Convergence and divergence in gene expression profiles induced by a leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments. Plant Cell Environ 35:644–655

    Article  PubMed  CAS  Google Scholar 

  • Maksyiemic W, Krupa Z (2006) The effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ Exp Bot 57:187–194

    Article  Google Scholar 

  • Maksymiec W, Wianowska D, Dawidowicz AL, Radkiewicz S, Mardarowicz M, Krupa Z (2005) The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. J Plant Physiol 162:1338–1346

    Article  PubMed  CAS  Google Scholar 

  • McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282

    Article  PubMed  CAS  Google Scholar 

  • Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281

    Article  PubMed  CAS  Google Scholar 

  • Noret N, Meerts P, Tolra R, Poschenrieder C, Barcelo J, Escarre J (2005) Palatability of Thlaspi caerulescens for snails: influence of zinc and glucosinolates. New Phytol 165:763–772

    Article  PubMed  CAS  Google Scholar 

  • Poschenrieder C, Tolrà R, Barceló J (2006) Can metals defend plants against biotic stress? Trends Plant Sci 11:288–295

    Article  PubMed  CAS  Google Scholar 

  • Poschenrieder C, Cabot C, Tolra R, Llugany M, Martos S, Gallego B, Barcelo J (2011) Metal defense against biotic stress; is it real? Agrochimica 55:29–44

    CAS  Google Scholar 

  • Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Serrano M, Romero-Puertas MC, Pazmino DM, Testillano PS, Risueño MC, del Rio LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229–243

    Article  PubMed  CAS  Google Scholar 

  • Schat H, Vooijs R, Kuiper E (1996) Identical major gene loci for heavy metal tolerances have independently evolved in different local populations and subspecies of Silene vulgaris. Evolution 50:1888–1895

    Article  CAS  Google Scholar 

  • Segarra G, Jauregui O, Casanova E, Trillas I (2006) Simultaneous quantitative LC-ESI–MS/MS analyses of salicylic acid and jasmonic acid in crude extracts of Cucumis sativus under biotic stress. Phytochemistry 67:395–401

    Article  PubMed  CAS  Google Scholar 

  • Shirasu K, Nakajima H, Rajasekhar VK, Dixon RA, Lamb C (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9:261–270

    PubMed  CAS  Google Scholar 

  • Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270

    Article  PubMed  CAS  Google Scholar 

  • Tolrà R, Pongrac P, Poschenrieder C, Vogel-Mikus K, Regvar M, Barcelo J (2006) Distinctive effects of cadmium on glucosinolate profiles in Cd hyperaccumulator Thlaspi praecox and non-hyperaccumulator Thlaspi arvense. Plant Soil 288:333–341

    Article  Google Scholar 

  • Vogel-Mikuš K, Drobne D, Regvar M (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ Pollut 133:233–242

    Article  PubMed  Google Scholar 

  • Zhang F, Zhang H, Xia Y, Wang G, Xu L, Shen Z (2011) Exogenous application of salicylic acid alleviates cadmium toxicity and reduces hydrogen peroxide accumulation in root apoplasts of Phaseolus aureus and Vicia sativa. Plant Cell Rep 30:1475–1483

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work has been supported by the Spanish Ministry of Science and Innovation projects BFU2010-14873/BFI and Catalonian Generalitat 2009 SGR 953.

Author information

Authors and Affiliations

  1. Plant Physiology Laboratory, Bioscience Faculty, Universitat Autònoma de Barcelona, 08193, Bellaterra, Spain

    M. Llugany, S. R. Martin, J. Barceló & C. Poschenrieder

Authors
  1. M. Llugany
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. R. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Barceló
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Poschenrieder
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. Poschenrieder.

Additional information

Communicated by P. Kumar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Llugany, M., Martin, S.R., Barceló, J. et al. Endogenous jasmonic and salicylic acids levels in the Cd-hyperaccumulator Noccaea (Thlaspi) praecox exposed to fungal infection and/or mechanical stress. Plant Cell Rep 32, 1243–1249 (2013). https://doi.org/10.1007/s00299-013-1427-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-013-1427-0

Keywords

Search

Navigation