Complexation of arsenite with phytochelatins reduces arsenite efflux and translocation from roots to shoots in Arabidopsis

Wen-Ju Liu, Barry Alan Wood, Andrea Raab, Steve P. McGrath, Fang-Jie Zhao, Jorg Feldmann

Research output: Contribution to journalArticle

130 Citations (Scopus)

Abstract

Complexation of arsenite [As(III)] with phytochelatins (PCs) is an important mechanism employed by plants to detoxify As; how this complexation affects As mobility was little known. We used high-resolution inductively coupled plasma-mass spectrometry and accurate mass electrospray ionization-mass spectrometry coupled to HPLC to identify and quantify As(III)thiol complexes and free thiol compounds in Arabidopsis (Arabidopsis thaliana) exposed to arsenate [As(V)]. As(V) was efficiently reduced to As(III) in roots. In wild-type roots, 69% of As was complexed as As(III)-PC4, As(III)-PC3, and As(III)-(PC2)(2). Both the glutathione (GSH)-deficient mutant cad2-1 and the PC-deficient mutant cad1-3 were approximately 20 times more sensitive to As(V) than the wild type. In cad1-3 roots, only 8% of As was complexed with GSH as As(III)-(GS)(3) and no As(III)-PCs were detected, while in cad2-1 roots, As(III)-PCs accounted for only 25% of the total As. The two mutants had a greater As mobility, with a significantly higher accumulation of As(III) in shoots and 4.5 to 12 times higher shoot-to-root As concentration ratio than the wild type. Roots also effluxed a substantial proportion of the As(V) taken up as As(III) to the external medium, and this efflux was larger in the two mutants. Furthermore, when wild-type plants were exposed to L-buthionine sulfoximine or deprived of sulfur, both As(III) efflux and root-to-shoot translocation were enhanced. The results indicate that complexation of As(III) with PCs in Arabidopsis roots decreases its mobility for both efflux to the external medium and for root-to-shoot translocation. Enhancing PC synthesis in roots may be an effective strategy to reduce As translocation to the edible organs of food crops.

Original languageEnglish
Pages (from-to)2211-2221
Number of pages11
JournalPlant Physiology
Volume152
Issue number4
Early online date1 Feb 2010
DOIs
Publication statusPublished - Apr 2010

Keywords

  • gamma-glutamyYlcysteine synthetase
  • hyperaccumulator pteris-vittata
  • tolerant holcus-lanatus
  • long-distance transport
  • arsenate reductase
  • glutathione-deficient
  • silene-vulgaris
  • thiol-peptides
  • Indian mustard
  • plants

Cite this

Complexation of arsenite with phytochelatins reduces arsenite efflux and translocation from roots to shoots in Arabidopsis. / Liu, Wen-Ju; Wood, Barry Alan; Raab, Andrea; McGrath, Steve P.; Zhao, Fang-Jie; Feldmann, Jorg.

In: Plant Physiology, Vol. 152, No. 4, 04.2010, p. 2211-2221.

Research output: Contribution to journalArticle

Liu, Wen-Ju ; Wood, Barry Alan ; Raab, Andrea ; McGrath, Steve P. ; Zhao, Fang-Jie ; Feldmann, Jorg. / Complexation of arsenite with phytochelatins reduces arsenite efflux and translocation from roots to shoots in Arabidopsis. In: Plant Physiology. 2010 ; Vol. 152, No. 4. pp. 2211-2221.
@article{4939ec38245c4ced9fd703b93521df1e,
title = "Complexation of arsenite with phytochelatins reduces arsenite efflux and translocation from roots to shoots in Arabidopsis",
abstract = "Complexation of arsenite [As(III)] with phytochelatins (PCs) is an important mechanism employed by plants to detoxify As; how this complexation affects As mobility was little known. We used high-resolution inductively coupled plasma-mass spectrometry and accurate mass electrospray ionization-mass spectrometry coupled to HPLC to identify and quantify As(III)thiol complexes and free thiol compounds in Arabidopsis (Arabidopsis thaliana) exposed to arsenate [As(V)]. As(V) was efficiently reduced to As(III) in roots. In wild-type roots, 69{\%} of As was complexed as As(III)-PC4, As(III)-PC3, and As(III)-(PC2)(2). Both the glutathione (GSH)-deficient mutant cad2-1 and the PC-deficient mutant cad1-3 were approximately 20 times more sensitive to As(V) than the wild type. In cad1-3 roots, only 8{\%} of As was complexed with GSH as As(III)-(GS)(3) and no As(III)-PCs were detected, while in cad2-1 roots, As(III)-PCs accounted for only 25{\%} of the total As. The two mutants had a greater As mobility, with a significantly higher accumulation of As(III) in shoots and 4.5 to 12 times higher shoot-to-root As concentration ratio than the wild type. Roots also effluxed a substantial proportion of the As(V) taken up as As(III) to the external medium, and this efflux was larger in the two mutants. Furthermore, when wild-type plants were exposed to L-buthionine sulfoximine or deprived of sulfur, both As(III) efflux and root-to-shoot translocation were enhanced. The results indicate that complexation of As(III) with PCs in Arabidopsis roots decreases its mobility for both efflux to the external medium and for root-to-shoot translocation. Enhancing PC synthesis in roots may be an effective strategy to reduce As translocation to the edible organs of food crops.",
keywords = "gamma-glutamyYlcysteine synthetase, hyperaccumulator pteris-vittata, tolerant holcus-lanatus, long-distance transport, arsenate reductase, glutathione-deficient, silene-vulgaris, thiol-peptides, Indian mustard, plants",
author = "Wen-Ju Liu and Wood, {Barry Alan} and Andrea Raab and McGrath, {Steve P.} and Fang-Jie Zhao and Jorg Feldmann",
year = "2010",
month = "4",
doi = "10.1104/pp.109.150862",
language = "English",
volume = "152",
pages = "2211--2221",
journal = "Plant Physiology",
issn = "0032-0889",
publisher = "American Society of Plant Biologists",
number = "4",

}

TY - JOUR

T1 - Complexation of arsenite with phytochelatins reduces arsenite efflux and translocation from roots to shoots in Arabidopsis

AU - Liu, Wen-Ju

AU - Wood, Barry Alan

AU - Raab, Andrea

AU - McGrath, Steve P.

AU - Zhao, Fang-Jie

AU - Feldmann, Jorg

PY - 2010/4

Y1 - 2010/4

N2 - Complexation of arsenite [As(III)] with phytochelatins (PCs) is an important mechanism employed by plants to detoxify As; how this complexation affects As mobility was little known. We used high-resolution inductively coupled plasma-mass spectrometry and accurate mass electrospray ionization-mass spectrometry coupled to HPLC to identify and quantify As(III)thiol complexes and free thiol compounds in Arabidopsis (Arabidopsis thaliana) exposed to arsenate [As(V)]. As(V) was efficiently reduced to As(III) in roots. In wild-type roots, 69% of As was complexed as As(III)-PC4, As(III)-PC3, and As(III)-(PC2)(2). Both the glutathione (GSH)-deficient mutant cad2-1 and the PC-deficient mutant cad1-3 were approximately 20 times more sensitive to As(V) than the wild type. In cad1-3 roots, only 8% of As was complexed with GSH as As(III)-(GS)(3) and no As(III)-PCs were detected, while in cad2-1 roots, As(III)-PCs accounted for only 25% of the total As. The two mutants had a greater As mobility, with a significantly higher accumulation of As(III) in shoots and 4.5 to 12 times higher shoot-to-root As concentration ratio than the wild type. Roots also effluxed a substantial proportion of the As(V) taken up as As(III) to the external medium, and this efflux was larger in the two mutants. Furthermore, when wild-type plants were exposed to L-buthionine sulfoximine or deprived of sulfur, both As(III) efflux and root-to-shoot translocation were enhanced. The results indicate that complexation of As(III) with PCs in Arabidopsis roots decreases its mobility for both efflux to the external medium and for root-to-shoot translocation. Enhancing PC synthesis in roots may be an effective strategy to reduce As translocation to the edible organs of food crops.

AB - Complexation of arsenite [As(III)] with phytochelatins (PCs) is an important mechanism employed by plants to detoxify As; how this complexation affects As mobility was little known. We used high-resolution inductively coupled plasma-mass spectrometry and accurate mass electrospray ionization-mass spectrometry coupled to HPLC to identify and quantify As(III)thiol complexes and free thiol compounds in Arabidopsis (Arabidopsis thaliana) exposed to arsenate [As(V)]. As(V) was efficiently reduced to As(III) in roots. In wild-type roots, 69% of As was complexed as As(III)-PC4, As(III)-PC3, and As(III)-(PC2)(2). Both the glutathione (GSH)-deficient mutant cad2-1 and the PC-deficient mutant cad1-3 were approximately 20 times more sensitive to As(V) than the wild type. In cad1-3 roots, only 8% of As was complexed with GSH as As(III)-(GS)(3) and no As(III)-PCs were detected, while in cad2-1 roots, As(III)-PCs accounted for only 25% of the total As. The two mutants had a greater As mobility, with a significantly higher accumulation of As(III) in shoots and 4.5 to 12 times higher shoot-to-root As concentration ratio than the wild type. Roots also effluxed a substantial proportion of the As(V) taken up as As(III) to the external medium, and this efflux was larger in the two mutants. Furthermore, when wild-type plants were exposed to L-buthionine sulfoximine or deprived of sulfur, both As(III) efflux and root-to-shoot translocation were enhanced. The results indicate that complexation of As(III) with PCs in Arabidopsis roots decreases its mobility for both efflux to the external medium and for root-to-shoot translocation. Enhancing PC synthesis in roots may be an effective strategy to reduce As translocation to the edible organs of food crops.

KW - gamma-glutamyYlcysteine synthetase

KW - hyperaccumulator pteris-vittata

KW - tolerant holcus-lanatus

KW - long-distance transport

KW - arsenate reductase

KW - glutathione-deficient

KW - silene-vulgaris

KW - thiol-peptides

KW - Indian mustard

KW - plants

U2 - 10.1104/pp.109.150862

DO - 10.1104/pp.109.150862

M3 - Article

VL - 152

SP - 2211

EP - 2221

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 4

ER -