Phytotoxicity and detoxification mechanism differ among inorganic and methylated arsenic species in Arabidopsis thaliana

Zhong Tang, Yuanyuan Kang, Peitong Wang, Fang Jie Zhao

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

Background and aims: Plants are able to take up inorganic arsenic (As) and methylated As, but whether the mode of phytotoxicity and the detoxification mechanism differ between different As species remains unclear. This study aimed to investigate the differences in phytotoxicity and detoxification mechanism between arsenate [As(V)], monomethylarsonic acid [MMA(V)] and dimethylarsinic acid [DMA(V)]. Methods: Arabidopsis thaliana was grown in agar-solidified medium, hydroponic or soil pot experiments. Root and shoot growth, seed production, As accumulation and oxidative stress indicators of wild-type plants exposed to As(V), MMA(V) and DMA(V) were compared. The role of thiols in As detoxification was investigated using a specific inhibitor of glutathione (GSH) biosynthesis and the mutants defective in GSH synthesis (cad2-1), phytochelatin (PC) synthesis (cad1-3) or tonoplast transporters for As(III)-PCs (abcc1-2). Results: Methylated As species, especially DMA(V), were more toxic than As(V) for growth and seed production in A. thaliana. Methylated As species were more efficiently translocated from roots to shoots and from shoots to seeds than As(V). DMA(V) exposure resulted in a greater oxidative stress than other As species. As(V) and MMA(V) induced the production of non-protein thiols (NPT), but DMA(V) did not. The GSH inhibitor BSO greatly enhanced the sensitivity to As(V) and MMA(V), but decreased the sensitivity to DMA(V). The mutants cad1-3, cad2-1 and abcc1-2 were similarly hypersensitive to As(V) and MMA(V), but not to DMA(V). As(V) and MMA(V) enhanced the expression of the sulphur assimilation genes encoding ATP Sulphurylase (ATPS) and adenosine-5′-phosphosulphate reductase (APR1) more than DMA(V). Conclusions: DMA(V) is more toxic to A. thaliana than As(V) or MMA(V). The detoxification mechanism for MMA(V) is similar to that for As(V), involving thiol production, complexation with PCs and vacuolar sequestration. This mechanism is ineffective for the detoxification of DMA(V).

Original languageEnglish
Pages (from-to)243-257
Number of pages15
JournalPlant and Soil
Volume401
Issue number1-2
DOIs
Publication statusPublished - Apr 1 2016
Externally publishedYes

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phytotoxicity
detoxification
arsenic
Arabidopsis thaliana
thiol
thiols
seed productivity
seed production
shoots
inhibitor
oxidative stress
adenylyl-sulfate reductase
shoot
cacodylic acid
phytochelatins
mutants
arsenates
synthesis
hydroponics
acid

Keywords

  • Arabidopsis thaliana
  • Arsenic
  • Detoxification
  • Methylated arsenic
  • Phytochelatins

ASJC Scopus subject areas

  • Soil Science
  • Plant Science

Cite this

Phytotoxicity and detoxification mechanism differ among inorganic and methylated arsenic species in Arabidopsis thaliana. / Tang, Zhong; Kang, Yuanyuan; Wang, Peitong; Zhao, Fang Jie.

In: Plant and Soil, Vol. 401, No. 1-2, 01.04.2016, p. 243-257.

Research output: Contribution to journalArticle

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title = "Phytotoxicity and detoxification mechanism differ among inorganic and methylated arsenic species in Arabidopsis thaliana",
abstract = "Background and aims: Plants are able to take up inorganic arsenic (As) and methylated As, but whether the mode of phytotoxicity and the detoxification mechanism differ between different As species remains unclear. This study aimed to investigate the differences in phytotoxicity and detoxification mechanism between arsenate [As(V)], monomethylarsonic acid [MMA(V)] and dimethylarsinic acid [DMA(V)]. Methods: Arabidopsis thaliana was grown in agar-solidified medium, hydroponic or soil pot experiments. Root and shoot growth, seed production, As accumulation and oxidative stress indicators of wild-type plants exposed to As(V), MMA(V) and DMA(V) were compared. The role of thiols in As detoxification was investigated using a specific inhibitor of glutathione (GSH) biosynthesis and the mutants defective in GSH synthesis (cad2-1), phytochelatin (PC) synthesis (cad1-3) or tonoplast transporters for As(III)-PCs (abcc1-2). Results: Methylated As species, especially DMA(V), were more toxic than As(V) for growth and seed production in A. thaliana. Methylated As species were more efficiently translocated from roots to shoots and from shoots to seeds than As(V). DMA(V) exposure resulted in a greater oxidative stress than other As species. As(V) and MMA(V) induced the production of non-protein thiols (NPT), but DMA(V) did not. The GSH inhibitor BSO greatly enhanced the sensitivity to As(V) and MMA(V), but decreased the sensitivity to DMA(V). The mutants cad1-3, cad2-1 and abcc1-2 were similarly hypersensitive to As(V) and MMA(V), but not to DMA(V). As(V) and MMA(V) enhanced the expression of the sulphur assimilation genes encoding ATP Sulphurylase (ATPS) and adenosine-5′-phosphosulphate reductase (APR1) more than DMA(V). Conclusions: DMA(V) is more toxic to A. thaliana than As(V) or MMA(V). The detoxification mechanism for MMA(V) is similar to that for As(V), involving thiol production, complexation with PCs and vacuolar sequestration. This mechanism is ineffective for the detoxification of DMA(V).",
keywords = "Arabidopsis thaliana, Arsenic, Detoxification, Methylated arsenic, Phytochelatins",
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T1 - Phytotoxicity and detoxification mechanism differ among inorganic and methylated arsenic species in Arabidopsis thaliana

AU - Tang, Zhong

AU - Kang, Yuanyuan

AU - Wang, Peitong

AU - Zhao, Fang Jie

PY - 2016/4/1

Y1 - 2016/4/1

N2 - Background and aims: Plants are able to take up inorganic arsenic (As) and methylated As, but whether the mode of phytotoxicity and the detoxification mechanism differ between different As species remains unclear. This study aimed to investigate the differences in phytotoxicity and detoxification mechanism between arsenate [As(V)], monomethylarsonic acid [MMA(V)] and dimethylarsinic acid [DMA(V)]. Methods: Arabidopsis thaliana was grown in agar-solidified medium, hydroponic or soil pot experiments. Root and shoot growth, seed production, As accumulation and oxidative stress indicators of wild-type plants exposed to As(V), MMA(V) and DMA(V) were compared. The role of thiols in As detoxification was investigated using a specific inhibitor of glutathione (GSH) biosynthesis and the mutants defective in GSH synthesis (cad2-1), phytochelatin (PC) synthesis (cad1-3) or tonoplast transporters for As(III)-PCs (abcc1-2). Results: Methylated As species, especially DMA(V), were more toxic than As(V) for growth and seed production in A. thaliana. Methylated As species were more efficiently translocated from roots to shoots and from shoots to seeds than As(V). DMA(V) exposure resulted in a greater oxidative stress than other As species. As(V) and MMA(V) induced the production of non-protein thiols (NPT), but DMA(V) did not. The GSH inhibitor BSO greatly enhanced the sensitivity to As(V) and MMA(V), but decreased the sensitivity to DMA(V). The mutants cad1-3, cad2-1 and abcc1-2 were similarly hypersensitive to As(V) and MMA(V), but not to DMA(V). As(V) and MMA(V) enhanced the expression of the sulphur assimilation genes encoding ATP Sulphurylase (ATPS) and adenosine-5′-phosphosulphate reductase (APR1) more than DMA(V). Conclusions: DMA(V) is more toxic to A. thaliana than As(V) or MMA(V). The detoxification mechanism for MMA(V) is similar to that for As(V), involving thiol production, complexation with PCs and vacuolar sequestration. This mechanism is ineffective for the detoxification of DMA(V).

AB - Background and aims: Plants are able to take up inorganic arsenic (As) and methylated As, but whether the mode of phytotoxicity and the detoxification mechanism differ between different As species remains unclear. This study aimed to investigate the differences in phytotoxicity and detoxification mechanism between arsenate [As(V)], monomethylarsonic acid [MMA(V)] and dimethylarsinic acid [DMA(V)]. Methods: Arabidopsis thaliana was grown in agar-solidified medium, hydroponic or soil pot experiments. Root and shoot growth, seed production, As accumulation and oxidative stress indicators of wild-type plants exposed to As(V), MMA(V) and DMA(V) were compared. The role of thiols in As detoxification was investigated using a specific inhibitor of glutathione (GSH) biosynthesis and the mutants defective in GSH synthesis (cad2-1), phytochelatin (PC) synthesis (cad1-3) or tonoplast transporters for As(III)-PCs (abcc1-2). Results: Methylated As species, especially DMA(V), were more toxic than As(V) for growth and seed production in A. thaliana. Methylated As species were more efficiently translocated from roots to shoots and from shoots to seeds than As(V). DMA(V) exposure resulted in a greater oxidative stress than other As species. As(V) and MMA(V) induced the production of non-protein thiols (NPT), but DMA(V) did not. The GSH inhibitor BSO greatly enhanced the sensitivity to As(V) and MMA(V), but decreased the sensitivity to DMA(V). The mutants cad1-3, cad2-1 and abcc1-2 were similarly hypersensitive to As(V) and MMA(V), but not to DMA(V). As(V) and MMA(V) enhanced the expression of the sulphur assimilation genes encoding ATP Sulphurylase (ATPS) and adenosine-5′-phosphosulphate reductase (APR1) more than DMA(V). Conclusions: DMA(V) is more toxic to A. thaliana than As(V) or MMA(V). The detoxification mechanism for MMA(V) is similar to that for As(V), involving thiol production, complexation with PCs and vacuolar sequestration. This mechanism is ineffective for the detoxification of DMA(V).

KW - Arabidopsis thaliana

KW - Arsenic

KW - Detoxification

KW - Methylated arsenic

KW - Phytochelatins

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JO - Plant and Soil

JF - Plant and Soil

SN - 0032-079X

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