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Methylated thioarsenates and monothioarsenate differ in uptake, transformation, and contribution to total arsenic translocation in rice plants Carolin F. Kerl, Ruth Alina Schindele, Lena Brüggenwirth, Andrea E. Colina Blanco, Colleen Rafferty, Stephan Clemens, and Britta Planer-Friedrich Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.9b00592 • Publication Date (Web): 29 Apr 2019 Downloaded from http://pubs.acs.org on April 29, 2019
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Environmental Science & Technology
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Methylated thioarsenates and monothioarsenate differ in uptake, transformation, and contribution to total arsenic translocation in rice plants
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Authors: Carolin F. Kerl†, Ruth Alina Schindele†, Lena Brüggenwirth†, Andrea E. Colina Blanco†, Colleen Rafferty‡, Stephan Clemens‡, Britta Planer-Friedrich†*
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†Environmental
Geochemistry, Bayreuth Center for Ecology and Environmental Research (BayCEER), University of Bayreuth, D-95440 Bayreuth, Germany
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Plant Physiology, Bayreuth Center for Ecology and Environmental Research (BayCEER), University of Bayreuth, D-95440 Bayreuth, Germany
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* Corresponding author phone: +49 921 55 3999, E-mail:
[email protected] 1
‡
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Abstract
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Methylated and inorganic thioarsenates have recently been reported from paddy fields besides the
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better-known oxyarsenates. Methylated thioarsenates are highly toxic for humans, yet their uptake,
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transformation and translocation in rice plants is unknown. Here, hydroponic experiments with 20-
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day-old
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dimethylmonothioarsenate (DMMTA), and monothioarsenate (MTA) were taken up by rice roots and
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could be detected in the xylem. Total arsenic (As) translocation from roots to shoots was higher for
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plants exposed to DMMTA, MTA, and dimethylarsenate (DMAV) compared to MMMTA and
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monomethylarsenate (MMAV). All thioarsenates were partially transformed in the presence of rice
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roots, but processes and extents differed. MMMTA was subject to abiotic oxidation and largely
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dethiolated to MMAV already outside the plant, probably due to root oxygen loss. DMMTA and MTA
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were not oxidized abiotically. Crude protein extracts showed rapid enzymatic reduction for MTA but
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not for DMMTA. Our study implies that DMMTA has the highest potential to contribute to total As
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accumulation in grains either as DMAV or partially as DMMTA. DMMTA has once been detected in rice
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grains using enzymatic extraction. By routine acid extraction, DMMTA is determined as DMAV and thus
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escapes regulation despite its toxicity.
rice
plants
showed
that
monomethylmonothioarsenate
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TOC
29 1 ACS Paragon Plus Environment
(MMMTA),
Environmental Science & Technology
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Introduction
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Rice, being a staple food for half of the world’s population,1,2 takes up approximately 10 times more
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arsenic (As) than other cereals3,4 and contributes to human As exposure.5 Arsenic is ubiquitously
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present in soils and mobilized during rice cultivation on flooded paddy soils by reductive dissolution of
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iron (Fe) minerals.6,7 While arsenite is the most abundant As species under reducing conditions, minor
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amounts of arsenate, monomethylarsenate (MMAV), and dimethylarsenate (DMAV) were reported in
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pore-water of paddy soils.
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that are able to biomethylate inorganic As by the enzyme As(III) S-adenosylmethionine (SAM)
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methyltransferase prior to uptake by plants.9,10 Uptake of inorganic arsenite (by nodulin 26-like
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intrinsic protein (NIP) aquaglyceroporins such as Lsi1 (OsNIP2;1)11-13) and arsenate (by phosphate
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transporters such as OsPht1;1,14 OsPht1;4,15,16 or OsPht1;817) is well studied. Less is known about
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methylated As which is microbially produced in the rhizosphere.10 Similar to arsenite, non-dissociated
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MMAV ((CH3)AsO(OH)2, pKa1 4.2) and DMAV ((CH3)2AsO(OH), pKa1 6.1) are taken up via OsNIP2;1.18
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However, additional, so far unknown transporters are hypothesized to account for the uptake of
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dissociated MMAV and DMAV.5 Further transport of As to xylem and phloem is limited by As
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sequestration in root cell vacuoles via phytochelatin (PC) complexation. Inorganic As is stored as AsIII-
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PC complexes19-22 and MMAV is stored as MMAIII-PC complexes after reduction of MMAV to MMAIII.23,24
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No DMAIII-PC complexes have been found in rice roots so far.23 Lack of DMAIII-complexation explains
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the
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arsenite
