Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators

John L. Freeman, M W Persans, K Nieman, C Albrecht, Wendy Ann Peer, Ingrid J. Pickering, David Edward Salt

Research output: Contribution to journalArticle

307 Citations (Scopus)

Abstract

Worldwide more than 400 plant species are now known that hyperaccumulate various trace metals (Cd, Co, Cu, Mn, Ni, and Zn), metalloids (As) and nonmetals [Se) in their shoots. Of these, almost one-quarter are Brassicaceae family members, including numerous Thlaspi species that hyperaccumulate Ni up to 3% of there shoot dry weight. We observed that concentrations of glutathione, Cys, and O-acetyl-L-serine (OAS), in shoot tissue, are strongly correlated with the ability to hyperaccumulate Ni in various Thlaspi hyperaccumulators collected from serpentine soils, including Thlaspi goesingense, T. oxyceras, and T. rosulare, and nonaccumulator relatives, including T. perfoliatum, T. arvense, and Arabidopsis thaliana. Further analysis of the Austrian Ni hyperaccumulator T. goesingense revealed that the high concentrations of OAS, Cys, and GSH observed in this hyperaccumulator coincide with constitutively high activity of both serine acetyltransferase (SAT) and glutathione reductase. SAT catalyzes the acetylation Of L-Ser to produce OAS, which acts as both a key positive regulator of sulfur assimilation and forms the carbon skeleton for Cys biosynthesis. These changes in Cys and GSH metabolism also coincide with the ability of T. goesingense to both hyperaccumulate Ni and resist its damaging oxidative effects. Overproduction of T. goesingense SAT in the nonaccumulator Brassicaceae family member Arabidopsis was found to cause accumulation of OAS, Cys, and glutathione, mimicking the biochemical changes observed in the Ni hyperaccumulators. In these transgenic Arabidopsis, glutathione concentrations strongly correlate with increased resistance to both the growth inhibitory and oxidative stress induced effects of Ni. Taken together, such evidence supports our conclusion that elevated GSH concentrations, driven by constitutively elevated SAT activity, are involved in conferring tolerance to Ni-induced oxidative stress in Thlaspi Ni hyperaccumulators.

Original languageEnglish
Pages (from-to)2176-2191
Number of pages16
JournalThe Plant Cell
Volume16
Issue number8
DOIs
Publication statusPublished - Aug 2004

Keywords

  • bacterial serine acetyltransferase
  • restriction-site variation
  • ray-absorption spectroscopy
  • heavy-metal detoxification
  • induced oxidative stress
  • Vulgaris moench garcke
  • Arabidopsis thaliana
  • Silene vulgaris
  • zinc tolerance
  • phylogenetic-relationships

Cite this

Freeman, J. L., Persans, M. W., Nieman, K., Albrecht, C., Peer, W. A., Pickering, I. J., & Salt, D. E. (2004). Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. The Plant Cell, 16(8), 2176-2191. https://doi.org/10.1105/tpc.104.023036

Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. / Freeman, John L.; Persans, M W ; Nieman, K ; Albrecht, C ; Peer, Wendy Ann; Pickering, Ingrid J.; Salt, David Edward.

In: The Plant Cell, Vol. 16, No. 8, 08.2004, p. 2176-2191.

Research output: Contribution to journalArticle

Freeman, JL, Persans, MW, Nieman, K, Albrecht, C, Peer, WA, Pickering, IJ & Salt, DE 2004, 'Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators', The Plant Cell, vol. 16, no. 8, pp. 2176-2191. https://doi.org/10.1105/tpc.104.023036
Freeman JL, Persans MW, Nieman K, Albrecht C, Peer WA, Pickering IJ et al. Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. The Plant Cell. 2004 Aug;16(8):2176-2191. https://doi.org/10.1105/tpc.104.023036
Freeman, John L. ; Persans, M W ; Nieman, K ; Albrecht, C ; Peer, Wendy Ann ; Pickering, Ingrid J. ; Salt, David Edward. / Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. In: The Plant Cell. 2004 ; Vol. 16, No. 8. pp. 2176-2191.
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AU - Pickering, Ingrid J.

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AB - Worldwide more than 400 plant species are now known that hyperaccumulate various trace metals (Cd, Co, Cu, Mn, Ni, and Zn), metalloids (As) and nonmetals [Se) in their shoots. Of these, almost one-quarter are Brassicaceae family members, including numerous Thlaspi species that hyperaccumulate Ni up to 3% of there shoot dry weight. We observed that concentrations of glutathione, Cys, and O-acetyl-L-serine (OAS), in shoot tissue, are strongly correlated with the ability to hyperaccumulate Ni in various Thlaspi hyperaccumulators collected from serpentine soils, including Thlaspi goesingense, T. oxyceras, and T. rosulare, and nonaccumulator relatives, including T. perfoliatum, T. arvense, and Arabidopsis thaliana. Further analysis of the Austrian Ni hyperaccumulator T. goesingense revealed that the high concentrations of OAS, Cys, and GSH observed in this hyperaccumulator coincide with constitutively high activity of both serine acetyltransferase (SAT) and glutathione reductase. SAT catalyzes the acetylation Of L-Ser to produce OAS, which acts as both a key positive regulator of sulfur assimilation and forms the carbon skeleton for Cys biosynthesis. These changes in Cys and GSH metabolism also coincide with the ability of T. goesingense to both hyperaccumulate Ni and resist its damaging oxidative effects. Overproduction of T. goesingense SAT in the nonaccumulator Brassicaceae family member Arabidopsis was found to cause accumulation of OAS, Cys, and glutathione, mimicking the biochemical changes observed in the Ni hyperaccumulators. In these transgenic Arabidopsis, glutathione concentrations strongly correlate with increased resistance to both the growth inhibitory and oxidative stress induced effects of Ni. Taken together, such evidence supports our conclusion that elevated GSH concentrations, driven by constitutively elevated SAT activity, are involved in conferring tolerance to Ni-induced oxidative stress in Thlaspi Ni hyperaccumulators.

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KW - restriction-site variation

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KW - heavy-metal detoxification

KW - induced oxidative stress

KW - Vulgaris moench garcke

KW - Arabidopsis thaliana

KW - Silene vulgaris

KW - zinc tolerance

KW - phylogenetic-relationships

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JO - The Plant Cell

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SN - 1040-4651

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