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Dimethylmonothioarsenate Is Highly Toxic for Plants and Readily Translocated to Shoots

  • Erik Pischke
    Erik Pischke
    Plant Physiology, Bayreuth Center for Ecology and Environmental Research (BayCEER), University of Bayreuth, D-95440 Bayreuth, Germany
    More by Erik Pischke
  • Fabrizio Barozzi
    Fabrizio Barozzi
    Plant Physiology, Bayreuth Center for Ecology and Environmental Research (BayCEER), University of Bayreuth, D-95440 Bayreuth, Germany
  • Andrea E. Colina Blanco
    Andrea E. Colina Blanco
    Environmental Geochemistry, Bayreuth Center for Ecology and Environmental Research (BayCEER), University of Bayreuth, D-95440 Bayreuth, Germany
  • Carolin F. Kerl
    Carolin F. Kerl
    Environmental Geochemistry, Bayreuth Center for Ecology and Environmental Research (BayCEER), University of Bayreuth, D-95440 Bayreuth, Germany
  • Britta Planer-Friedrich
    Britta Planer-Friedrich
    Environmental Geochemistry, Bayreuth Center for Ecology and Environmental Research (BayCEER), University of Bayreuth, D-95440 Bayreuth, Germany
  • , and 
  • Stephan Clemens*
    Stephan Clemens
    Plant Physiology, Bayreuth Center for Ecology and Environmental Research (BayCEER), University of Bayreuth, D-95440 Bayreuth, Germany
    *Email: [email protected]. Phone: +49 921 55 2630.
Cite this: Environ. Sci. Technol. 2022, 56, 14, 10072–10083
Publication Date (Web):June 27, 2022
https://doi.org/10.1021/acs.est.2c01206
Copyright © 2022 American Chemical Society

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    Abstract

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    Arsenic is one of the most relevant environmental pollutants and human health threats. Several arsenic species occur in soil pore waters. Recently, it was discovered that these include inorganic and organic thioarsenates. Among the latter, dimethylmonothioarsenate (DMMTA) is of particular concern because in mammalian cells, its toxicity was found to exceed even that of arsenite. We investigated DMMTA toxicity for plants in experiments with Arabidopsis thaliana and indeed observed stronger growth inhibition than with arsenite. DMMTA caused a specific, localized deformation of root epidermal cells. Toxicity mechanisms apparently differ from those of arsenite since no accumulation of reactive oxygen species was observed in DMMTA-exposed root tips. Also, there was no contribution of the phytochelatin pathway to the DMMTA detoxification as indicated by exposure experiments with respective mutants and thiol profiling. RNA-seq analysis found strong transcriptome changes dominated by stress-responsive genes. DMMTA was taken up more efficiently than the methylated oxyarsenate dimethylarsenate and highly mobile within plants as revealed by speciation analysis. Shoots showed clear indications of DMMTA toxicity such as anthocyanin accumulation and a decrease in chlorophyll and carotenoid levels. The toxicity and efficient translocation of DMMTA within plants raise important food safety issues.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.2c01206.

    • DMMTA stability in medium samples; inhibition of root growth by different arsenic species for A. thaliana wild-type and mutant seedlings; effects of arsenite, DMMTA, and DMA on seed germination; quantification of ROS accumulation in Col-0 root tips after 24 h of exposure to 10 and 25 μM DMMTA, arsenite, or DMA; propidium iodide staining of roots exposed to 10 and 25 μM DMMTA, arsenite, or DMA; visualization of the tonoplast in root cells exposed to DMMTA; relative transcript levels of the As-responsive genes DRG1-3 and RBL14 in A. thaliana Col-0 after exposure to different As species; confirmation of RNA-seq results by qRT-PCR for selected genes; GO term enrichment among DEGs in DMMTA-exposed A. thaliana seedlings; the arsenic core response and genes specifically induced by DMMTA; cellular localization of DMMTA responses in A. thaliana roots; the aquaglyceroporin NIP1;1 not contributing to DMMTA uptake in A. thaliana seedlings; arsenic accumulation in A. thaliana Col-0 exposed to different As species; DMMTA exposure inhibiting leaf growth; DMMTA exposure activating stress marker gene expression in leaves; effect of DMMTA exposure during flowering; quality of DMMTA synthesis; primers used for qRT-PCR analysis; and total arsenic contents and translocation factors (PDF)

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    Cited By

    This article is cited by 2 publications.

    1. Andrea E. Colina Blanco, Erik Pischke, Alejandra Higa Mori, Carolin F. Kerl, Stephan Clemens, Britta Planer-Friedrich. In Planta Arsenic Thiolation in Rice and Arabidopsis thaliana. Environmental Science & Technology 2023, 57 (51) , 21846-21854. https://doi.org/10.1021/acs.est.3c06603
    2. Cristina Navarro, Micaela A. Navarro, Antonio Leyva. Arsenic perception and signaling: The yet unexplored world. Frontiers in Plant Science 2022, 13 https://doi.org/10.3389/fpls.2022.993484

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