Methylated and inorganic thioarsenates have recently been reported from paddy fields besides the better-known oxyarsenates. Methylated thioarsenates are highly toxic for humans, yet their uptake, transformation, and translocation in rice plants is unknown. Here, hydroponic experiments with 20 day old rice plants showed that monomethylmonothioarsenate (MMMTA), dimethylmonothioarsenate (DMMTA), and monothioarsenate (MTA) were taken up by rice roots and could be detected in the xylem. Total arsenic (As) translocation from roots to shoots was higher for plants exposed to DMMTA, MTA, and dimethylarsenate (DMAV) compared to MMMTA and monomethylarsenate (MMAV). All thioarsenates were partially transformed in the presence of rice roots, but processes and extents differed. MMMTA was subject to abiotic oxidation and largely dethiolated to MMAV already outside the plant, probably due to root oxygen loss. DMMTA and MTA were not oxidized abiotically. Crude protein extracts showed rapid enzymatic reduction for MTA but not for DMMTA. Our study implies that DMMTA has the highest potential to contribute to total As accumulation in grains either as DMAV or partially as DMMTA. DMMTA has once been detected in rice grains using enzymatic extraction. By routine acid extraction, DMMTA is determined as DMAV and thus escapes regulation despite its toxicity.

Inorganic and methylated thioarsenates have recently been reported to contribute substantially to arsenic (As) speciation in paddy-soil pore waters. Here, we show that thioarsenates can also accumulate in rice grains and rice products. For their detection, a method was developed using a pepsin–pancreatin enzymatic extraction followed by chromatographic separation at pH 13. From 54 analyzed commercial samples, including white, parboiled and husked rice, puffed rice cakes, and rice flakes, 50 contained dimethylmonothioarsenate (DMMTA) (maximum 25.6 μg kg–1), 18 monothioarsenate (MTA) (maximum 5.6 μg kg–1), 14 dimethyldithioarsenate (DMDTA) (maximum 2.8 μg kg–1), and 5 dithioarsenate (DTA) (maximum 2.3 μg kg–1). Additionally, we show that the commonly used nitric acid extraction transforms MTA to arsenite and DMMTA and DMDTA to dimethylarsenate (DMA). Current food guidelines do not require an analysis of thioarsenates in rice and only limit the contents of inorganic oxyarsenic species (including acid-extraction-transformed MTA), but not DMA (including acid-extraction-transformed DMMTA and DMDTA).

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.

Arsenic (As) occurrence in rice is a serious human health threat. Worldwide, regulations typically limit only carcinogenic inorganic As, but not possibly carcinogenic dimethylated oxyarsenate (DMA). However, there is emerging evidence that “DMA”, determined by routine acid-based extraction and analysis, hides a substantial share of dimethylated thioarsenates that have similar or higher cytotoxicities than arsenite. Risk assessments characterizing the in vivo toxicity of rice-derived dimethylated thioarsenates are urgently needed. In the meantime, either more sophisticated methods based on enzymatic extraction and separation of dimethylated oxy- and thioarsenates have to become mandatory or total As should be regulated.

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