Arsenic poisoning affects millions of people worldwide. Human arsenic intake from rice consumption can be substantial because rice is particularly efficient in assimilating arsenic from paddy soils, although the mechanism has not been elucidated. Here we report that two different types of transporters mediate transport of arsenite, the predominant form of arsenic in paddy soil, from the external medium to the xylem. Transporters belonging to the NIP subfamily of aquaporins in rice are permeable to arsenite but not to arsenate. Mutation in OsNIP2;1 (Lsi1, a silicon influx transporter) significantly decreases arsenite uptake. Furthermore, in the rice mutants defective in the silicon efflux transporter Lsi2, arsenite transport to the xylem and accumulation in shoots and grain decreased greatly. Mutation in Lsi2 had a much greater impact on arsenic accumulation in shoots and grain in field-grown rice than Lsi1. Arsenite transport in rice roots therefore shares the same highly efficient pathway as silicon, which explains why rice is efficient in arsenic accumulation. Our results provide insight into the uptake mechanism of arsenite in rice and strategies for reducing arsenic accumulation in grain for enhanced food safety.

https://www.pnas.org/content/pnas/105/29/9931.full.pdf

Transporters of arsenite in rice and their role in arsenic accumulation in rice grain

Arsenic (As) is an environmental and food chain contaminant. Excessive accumulation of As, particularly inorganic arsenic (As(i)), in rice (Oryza sativa) poses a potential health risk to populations with high rice consumption. Rice is efficient at As accumulation owing to flooded paddy cultivation that leads to arsenite mobilization, and the inadvertent yet efficient uptake of arsenite through the silicon transport pathway. Iron, phosphorus, sulfur, and silicon interact strongly with As during its route from soil to plants. Plants take up arsenate through the phosphate transporters, and arsenite and undissociated methylated As species through the nodulin 26-like intrinsic (NIP) aquaporin channels. Arsenate is readily reduced to arsenite in planta, which is detoxified by complexation with thiol-rich peptides such as phytochelatins and/or vacuolar sequestration. A range of mitigation methods, from agronomic measures and plant breeding to genetic modification, may be employed to reduce As uptake by food crops.

Arsenic as a Food Chain Contaminant: Mechanisms of Plant Uptake and Metabolism and Mitigation Strategies

Arsenic (As) is an element that is nonessential for and toxic to plants. Arsenic contamination in the environment occurs in many regions, and, depending on environmental factors, its accumulation in food crops may pose a health risk to humans.Recent progress in understanding the mechanisms of As uptake and metabolism in plants is reviewed here. Arsenate is taken up by phosphate transporters. A number of the aquaporin nodulin26-like intrinsic proteins (NIPs) are able to transport arsenite,the predominant form of As in reducing environments. In rice (Oryza sativa), arsenite uptake shares the highly efficient silicon (Si) pathway of entry to root cells and efflux towards the xylem. In root cells arsenate is rapidly reduced to arsenite, which is effluxed to the external medium, complexed by thiol peptides or translocated to shoots. One type of arsenate reductase has been identified, but its in planta functions remain to be investigated. Some fern species in the Pteridaceae family are able to hyperaccumulate As in above-ground tissues. Hyperaccumulation appears to involve enhanced arsenate uptake, decreased arsenite-thiol complexation and arsenite efflux to the external medium, greatly enhanced xylem translocation of arsenite, and vacuolar sequestration of arsenite in fronds. Current knowledge gaps and future research directions are also identified.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1469-8137.2008.02716.x

Arsenic uptake and metabolism in plants.

Arsenic, cadmium, lead, and mercury are toxic elements that are almost ubiquitously present at low levels in the environment because of anthropogenic influences. Dietary intake of plant-derived food represents a major fraction of potentially health-threatening human exposure, especially to arsenic and cadmium. In the interest of better food safety, it is important to reduce toxic element accumulation in crops. A molecular understanding of the pathways responsible for this accumulation can enable the development of crop varieties with strongly reduced concentrations of toxic elements in their edible parts. Such understanding is rapidly progressing for arsenic and cadmium but is in its infancy for lead and mercury. Basic discoveries have been made in Arabidopsis, rice, and other models, and most advances in crops have been made in rice. Proteins mediating the uptake of arsenic and cadmium have been identified, and the speciation and biotransformations of arsenic are now understood. Factors controlling the efficiency of root-to-shoot translocation and the partitioning of toxic elements through the rice node have also been identified.

Toxic Heavy Metal and Metalloid Accumulation in Crop Plants and Foods

An extensive data set of total arsenic analysis for 901 polished (white) grain samples, originating from 10 countries from 4 continents, was compiled. The samples represented the baseline (i.e., notspecifically collected from arsenic contaminated areas), and all were for market sale in major conurbations. Median total arsenic contents of rice varied 7-fold, with Egypt (0.04 mg/kg) and India (0.07 mg/kg) having the lowest arsenic content while the U.S. (0.25 mg/kg) and France (0.28 mg/kg) had the highest content. Global distribution of total arsenic in rice was modeled by weighting each country's arsenic distribution by that country's contribution to global production. A subset of 63 samples from Bangladesh, China, India, Italy, and the U.S. was analyzed for arsenic species. The relationship between inorganic arsenic contentversus total arsenic contentsignificantly differed among countries, with Bangladesh and India having the steepest slope in linear regression, and the U.S. having the shallowest slope. Using country-specific rice consumption data, daily intake of inorganic arsenic was estimated and the associated internal cancer risk was calculated using the U.S. Environmental Protection Agency (EPA) cancer slope. Median excess internal cancer risks posed by inorganic arsenic ranged 30-fold for the 5 countries examined, being 0.7 per 10,000 for Italians to 22 per 10,000 for Bangladeshis, when a 60 kg person was considered.

/pdf/geographical-variation-in-total-and-inorganic-arsenic-2ctamzxoam.pdf

Geographical Variation in Total and Inorganic Arsenic Content of Polished (White) Rice

Paired grain, shoot, and soil of 173 individual sample sets of commercially farmed temperate rice, wheat, and barley were surveyed to investigate variation in the assimilation and translocation of arsenic (As). Rice samples were obtained from the Carmargue (France), Donana (Spain), Cadiz (Spain), California, and Arkansas. Wheat and barleywere collected from Cornwall and Devon (England) and the east coast of Scotland. Transfer of As from soil to grain was an order of magnitude greater in rice than for wheat and barley, despite lower rates of shoot-to-grain transfer. Rice grain As levels over 0.60 microg g(-1) d. wt were found in rice grown in paddy soil of around only 10 microg g(-1) As, showing that As in paddy soils is problematic with respect to grain As levels. This is due to the high shoot/soil ratio of approximately 0.8 for rice compared to 0.2 and 0.1 for barley and wheat, respectively. The differences in these transfer ratios are probably due to differences in As speciation and dynamics in anaerobic rice soils compared to aerobic soils for barley and wheat. In rice, the export of As from the shoot to the grain appears to be under tight physiological control as the grain/shoot ratio decreases by more than an order of magnitude (from approximately 0.3 to 0.003 mg/kg) and as As levels in the shoots increase from 1 to 20 mg/kg. A down regulation of shoot-to-grain export may occur in wheat and barley, but it was not detected at the shoot As levels found in this survey. Some agricultural soils in southwestern England had levels in excess of 200 microg g(-1) d. wt, although the grain levels for wheat and barley never breached 0.55 microg g(-1) d. wt. These grain levels were achieved in rice in soils with an order of magnitude lower As. Thus the risk posed by As in the human food-chain needs to be considered in the context of anaerobic verses aerobic ecosystems.

Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley

Factors responsible for paddy soil arsenic accumulation in the tubewell irrigated systems of the Bengal Delta were investigated Baseline (ie, nonirrigated) and paddy soils were collected from 30 field systems across Bangladesh For each field, soil sampled at dry season (Boro) harvest ie, the crop cycle irrigated with tubewell water, was collected along a 90 m transect away from the tubewell irrigation source Baseline soil arsenic levels ranged from 08 to 21 mg/kg, with lower values found on the Pliestocene Terrace around Gazipur (average, 16 +/- 02 mg/kg), and higher levels found in Holecene sediment tracts of Jessore and Faridpur (average, 66 +/- 10 mg/kg) Two independent approaches were used to assess the extent of arsenic build-up in irrigated paddy soils First, arsenic build-up in paddy soil at the end of dry season production (irrigated - baseline soil arsenic) was regressed against number of years irrigated and tubewell arsenic concentration Years of irrigation was not significant (P = 0711), indicating no year-on-year arsenic build-up, whereas tubewell As concentration was significant (P = 0008) The second approach was analysis of irrigated soils for 20 fields over 2 successive years For nine of the fields there was a significant (P < 005) decrease in soil arsenic from year 1 to 2, one field had a significant increase, whereas there was no change for the remaining 10 Over the dry season irrigation cycle, soil arsenic built-up in soils at a rate dependent on irrigation tubewell water, 35* (tubewell water concentration in mg/kg, triple bond mg/L) Grain arsenic rises steeply at low soil/shoot arsenic levels, plateauing out at concentratations Baseline soil arsenic at Faridpur sites corresponded to grain arsenic levels at the start of this saturation phase Therefore, variation in baseline levels of soil arsenic leads to a large range in grain arsenic Where sites have high baseline soil arsenic, further additional arsenic from irrigation water only leads to a gradual increase in grain arsenic concentration

Baseline Soil Variation Is a Major Factor in Arsenic Accumulation in Bengal Delta Paddy Rice

This study assessed
the concentrations of arsenic and iron in paddy soil and rice grain samples
collected from the Nobewam and Odumase paddy field sites in the Anum Valley of
Ghana, as a means of determining the impacts of gold mining activities in the area
on rice production. The arsenic content of rice grains from the Anum Valley
paddy fields was compared to that in rice grains of the same variety harvested
from three non-impacted paddy fields (control sites) in other parts of Ghana.
The study findings indicated that soils in the Odumase paddy fields, which are
located closer to the gold mining site, were significantly more impacted by
mining pollution than soils in the Nobewam paddy fields. Arsenic concentration
in the Nobewam paddy soils ranged from 0.6 to 76.1 mg/kg with a mean of 8.3
mg/kg, while that in the Odumase paddy soils ranged from 5.3 to 106.2 mg/kg
with a mean of 41.1 mg/kg. Despite the significant difference in mean soil
arsenic content, there was no significant difference in the arsenic content of
rice grains harvested from the two Anum Valley paddy sites (i.e. Nobewam and Odumase). There was
also no significant difference between the two Anum Valley paddy sites with
respect to soil iron concentration. The regression equation for a graph of
soil arsenic against soil iron (As = 70.0 Fe – 37.7) was, however, highly
significant (P

/pdf/impacts-of-gold-mining-on-rice-production-in-the-anum-valley-u0mxg3nsxg.pdf

Impacts of Gold Mining on Rice Production in the Anum Valley of Ghana

Inorganic arsenic is a chronic exposure carcinogen. Analysis of UK baby rice revealed a median inorganic arsenic content (n ¼ 17) of 0.11 mg/kg. By plotting inorganic arsenic against total arsenic, it was found that inorganic concentrations increased linearly up to 0.25 mg/ kg total arsenic, then plateaued at 0.16 mg/kg at higher total arsenic concentrations. Inorganic arsenic intake by babies (4e12 months) was considered with respect to current dietary ingestion regulations. It was found that 35% of the baby rice samples analysed would be illegal for sale in China which has regulatory limit of 0.15 mg/kg inorganic arsenic. EU and US food regulations on arsenic are non-existent. When baby inorganic arsenic intake from rice was considered, median consumption (expressed as mg/kg/d) was higher than drinking water maximum exposures predicted for adults in these regions when water intake was expressed on a bodyweight basis. 2008 Elsevier Ltd. All rights reserved.

Claire Deacon

Papers

Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley

Baseline Soil Variation Is a Major Factor in Arsenic Accumulation in Bengal Delta Paddy Rice

Impacts of Gold Mining on Rice Production in the Anum Valley of Ghana

Rapid communication Inorganic arsenic levels in baby rice are of concern