Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators

John L. Freeman, Daniel Garcia, D G Kim, A Hopf, David Edward Salt

Research output: Contribution to journalArticle

152 Citations (Scopus)

Abstract

Progress is being made in understanding the biochemical and molecular basis of nickel (Ni)/zinc (Zn) hyperaccumulation in Thlaspi; however, the molecular signaling pathways that control these mechanisms are not understood. We observed that elevated concentrations of salicylic acid (SA), a molecule known to be involved in signaling induced pathogen defense responses in plants, is a strong predictor of Ni hyperaccumulation in the six diverse Thlaspi species investigated, including the hyperaccumulators Thlaspi goesingense, Thlaspi rosulare, Thlaspi oxyceras, and Tlilaspi caerulescens and the nonaccumulators Thlaspi arvense and Thlaspi perfoliatum. Furthermore, the SA metabolites phenylalanine, cinnamic acid, salicyloyl-glucose, and catechol are also elevated in the hyperaccumulator T. goesingense when compared to the nonaccumulators Arabidopsis (Arabidopsis thaliana) and T arvense. Elevation of free SA levels in Arabidopsis, both genetically and by exogenous feeding, enhances the specific activity of serine acetyltransferase, leading to elevated glutathione and increased Ni resistance. Such SA-mediated Ni resistance in Arabidopsis phenocopies the glutathione-based Ni tolerance previously observed in Thlaspi, suggesting a biochemical linkage between SA and Ni tolerance in this genus. Intriguingly, the hyperaccumulator T. goesingense also shows enhanced sensitivity to the pathogen powdery mildew (Erysiphe cruciferarum) and fails to induce SA biosynthesis after infection. Nickel hyperaccumulation reverses this pathogen hypersensitivity, suggesting that the interaction between pathogen resistance and Ni tolerance and hyperaccumulation may have played a critical role in the evolution of metal hyperaccumulation in the Thlaspi genus.

Original languageEnglish
Pages (from-to)1082-1091
Number of pages10
JournalPlant Physiology
Volume137
Issue number3
DOIs
Publication statusPublished - Mar 2005

Keywords

  • DNA binding activity
  • Arabidopsis thaliana
  • serine acetyltransferase
  • disease resistance
  • metal transport
  • soybean cells
  • plants
  • protein
  • NPR1
  • defense

Cite this

Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. / Freeman, John L.; Garcia, Daniel; Kim, D G ; Hopf, A ; Salt, David Edward.

In: Plant Physiology, Vol. 137, No. 3, 03.2005, p. 1082-1091.

Research output: Contribution to journalArticle

Freeman, John L. ; Garcia, Daniel ; Kim, D G ; Hopf, A ; Salt, David Edward. / Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. In: Plant Physiology. 2005 ; Vol. 137, No. 3. pp. 1082-1091.
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