Dimethylmonothioarsenate Is Highly Toxic for Plants and Readily Translocated to Shoots

Abstract

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.

In Planta Arsenic Thiolation in Rice and Arabidopsis thaliana

“…We therefore investigated whether in planta thiolation also occurs in the dicot A. thaliana like in the monocot O. sativa. Like in our previous study, 28 A. thaliana (Col-0) seedlings exposed to DMMTA showed a 10fold higher As accumulation in both roots and shoots compared to DMA-exposed seedlings (Figure S12), which is the same trend as observed in rice seedlings 20 and the rice plants during grain filling (Figure 1). The observation supports similar transport and translocation capacities for DMA and DMMTA in monocots and dicots.…”

“…Considering that DMMTA toxicity in A. thaliana is far greater than that of DMA, the alleviation in the toxic effect could be due to less production of DMMTA in the roots. From a food security perspective, it would be worth addressing similarly the impact of DMMTA on rice plants.…”

“…Interestingly, a study addressing DMA phytotoxicity in A. thaliana determined that inhibition of GSH biosynthesis decreased the plant's sensitivity to DMA. 47 Considering that DMMTA toxicity in A. thaliana is far greater than that of DMA, 28 the alleviation in the toxic effect could be due to less production of DMMTA in the roots. From a food security perspective, it would be worth addressing similarly the impact of DMMTA on rice plants.…”

“…Previous studies have overlooked the presence of DMMTA in grains because routine acid extractions and detection methods transform DMMTA to DMA . Misidentification of DMMTA is problematic because of its high mobility and toxicity in plants and high cytotoxicity in humans. − Despite its ubiquitous presence in rice and food safety concerns associated with DMMTA, its behavior in rice plants and its path to the grains remain unclear.…”

Arsenic perception and signaling: The yet unexplored world

“…As(III) is then rapidly incorporated into the vascular cells through symplastic intracellular transporters and rapidly accumulated in rice kernels. Recently, the study of the accumulation in plants of arsenic methylated forms produced by soil microorganisms (Lomax et al, 2012;Di et al, 2019), particularly the highly toxic dimethyl monothioarsenate (DMMTA), has raised research interest (Colina Blanco et al, 2021;Dai et al, 2021Dai et al, , 2022Zhao et al, 2021;Pischke et al, 2022).…”