In Planta Arsenic Thiolation in Rice and Arabidopsis thaliana.

Inorganic and methylated thioarsenates have recently been reported to form in paddy soil pore waters and accumulate in rice grains. Among them, dimethylmonothioarsenate (DMMTA) is particularly relevant because of its high cytotoxicity and potential misidentification as nonregulated dimethylarsenate (DMA). Studying DMMTA uptake and flag leaf, grain, and husk accumulation in rice plants during grain filling, substantial dethiolation to DMA was observed with only 8.0 ± 0.1, 9.1 ± 0.6, and 1.4 ± 0.2% DMMTA remaining, respectively. More surprisingly, similar shares of DMMTA were observed in control experiments with DMA, indicating in planta DMA thiolation. Exposure of different rice seedling varieties to not only DMA but also to arsenite and monomethylarsenate (MMA) revealed in planta thiolation as a common process in rice. Up to 35 ± 7% DMA thiolation was further observed in the shoots and roots of the model plant Arabidopsis thaliana. Parameters determining the ratio and kinetics of thiolation versus dethiolation are unknown, yet, but less DMA thiolation in glutathione-deficient mutants compared to wild-type plants suggested glutathione concentration as one potential parameter. Our results demonstrate that pore water is not the only source for thioarsenates in rice grains and that especially the currently nonregulated DMA needs to be monitored as a potential precursor of DMMTA formation inside rice plants.

Dimethylmonothioarsenate Is Highly Toxic for Plants and Readily Translocated to Shoots.

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.