Grain Unloading of Arsenic Species in Rice1[W]

Rice (Oryza sativa) is the staple food for over half the world's population yet may represent a significant dietary source of inorganic arsenic (As), a nonthreshold, class 1 human carcinogen. Rice grain As is dominated by the inorganic species, and the organic species dimethylarsinic acid (DMA). To investigate how As species are unloaded into grain rice, panicles were excised during grain filling and hydroponically pulsed with arsenite, arsenate, glutathione-complexed As, or DMA. Total As concentrations in flag leaf, grain, and husk, were quantified by inductively coupled plasma mass spectroscopy and As speciation in the fresh grain was determined by x-ray absorption near-edge spectroscopy. The roles of phloem and xylem transport were investigated by applying a ± stem-girdling treatment to a second set of panicles, limiting phloem transport to the grain in panicles pulsed with arsenite or DMA. The results demonstrate that DMA is translocated to the rice grain with over an order magnitude greater efficiency than inorganic species and is more mobile than arsenite in both the phloem and the xylem. Phloem transport accounted for 90% of arsenite, and 55% of DMA, transport to the grain. Synchrotron x-ray fluorescence mapping and fluorescence microtomography revealed marked differences in the pattern of As unloading into the grain between DMA and arsenite-challenged grain. Arsenite was retained in the ovular vascular trace and DMA dispersed throughout the external grain parts and into the endosperm. This study also demonstrates that DMA speciation is altered in planta, potentially through complexation with thiols.

[1]  P. Martín Stem Xylem as a Possible Pathway for Mineral Retranslocation From Senescing Leaves to the Ear in Wheat , 1982 .

[2]  S. McGrath,et al.  Growing rice aerobically markedly decreases arsenic accumulation. , 2008, Environmental science & technology.

[3]  Guo-ping Zhang,et al.  Cadmium translocation and accumulation in developing barley grains , 2007, Planta.

[4]  Enzo Lombi,et al.  Synchrotron-based techniques for plant and soil science: opportunities, challenges and future perspectives , 2009, Plant and Soil.

[5]  I. Koch,et al.  X-ray absorption near-edge structure analysis of arsenic species for application to biological environmental samples. , 2005, Environmental science & technology.

[6]  J. Feldmann,et al.  Uptake, translocation and transformation of arsenate and arsenite in sunflower (Helianthus annuus): formation of arsenic-phytochelatin complexes during exposure to high arsenic concentrations. , 2005, The New phytologist.

[7]  N. Fageria,et al.  Yield Physiology of Rice , 2007 .

[8]  J. Feldmann,et al.  Can arsenic-phytochelatin complex formation be used as an indicator for toxicity in Helianthus annuus? , 2007, Journal of experimental botany.

[9]  Yong-guan Zhu,et al.  Inorganic arsenic in rice bran and its products are an order of magnitude higher than in bulk grain. , 2008, Environmental science & technology.

[10]  M. Islam,et al.  Baseline soil variation is a major factor in arsenic accumulation in Bengal Delta paddy rice. , 2009, Environmental science & technology.

[11]  A. Price,et al.  Identification of low inorganic and total grain arsenic rice cultivars from Bangladesh. , 2009, Environmental science & technology.

[12]  U. Feller,et al.  Transport of Rb and Sr to the ear in mature, excised shoots of wheat: Effects of temperature and stem length on Rb removal from the xylem , 1991, Plant and Soil.

[13]  Yong-guan Zhu,et al.  High percentage inorganic arsenic content of mining impacted and nonimpacted Chinese rice. , 2008, Environmental science & technology.

[14]  K. Scheckel,et al.  Speciation and distribution of arsenic and localization of nutrients in rice grains. , 2009, The New phytologist.

[15]  Yong-guan Zhu,et al.  Geographical variation in total and inorganic arsenic content of polished (white) rice. , 2009, Environmental science & technology.

[16]  T. Fujiwara,et al.  Quantitative estimation of the contribution of the phloem in cadmium transport to grains in rice plants (Oryza sativa L.) , 2007 .

[17]  P. Dayanandan,et al.  Structural and histochemical studies on grain-filling in the caryopsis of rice (Oryza sativa L.) , 2003, Journal of Biosciences.

[18]  H. Hasegawa,et al.  Accumulation of arsenic in tissues of rice plant (Oryza sativa L.) and its distribution in fractions of rice grain. , 2007, Chemosphere.

[19]  Yong-guan Zhu,et al.  Increase in rice grain arsenic for regions of Bangladesh irrigating paddies with elevated arsenic in groundwaters. , 2006, Environmental science & technology.

[20]  Enzo Lombi,et al.  Speciation and localization of arsenic in white and brown rice grains. , 2008, Environmental science & technology.

[21]  Ying-Ru Liu,et al.  Soil As contamination and its risk assessment in areas near the industrial districts of Chenzhou City, Southern China. , 2005, Environment international.

[22]  S. McGrath,et al.  Arsenic uptake and metabolism in plants. , 2009, The New phytologist.

[23]  M. Bliek,et al.  Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcus lanatus. , 2006, The Plant journal : for cell and molecular biology.

[24]  J. Feldmann,et al.  Market basket survey shows elevated levels of As in South Central U.S. processed rice compared to California: consequences for human dietary exposure. , 2007, Environmental science & technology.

[25]  J. Feldmann,et al.  Uptake and translocation of inorganic and methylated arsenic species by plants , 2007 .

[26]  Mark Rivers,et al.  Application of quantitative fluorescence and absorption-edge computed microtomography to image metal compartmentalization in Alyssum murale. , 2005, Environmental science & technology.

[27]  Broome,et al.  Literature cited , 1924, A Guide to the Carnivores of Central America.

[28]  J Feldmann,et al.  Variation in arsenic speciation and concentration in paddy rice related to dietary exposure. , 2005, Environmental science & technology.

[29]  J. Feldmann,et al.  Uptake Kinetics of Arsenic Species in Rice Plants , 2002, Plant Physiology.

[30]  Yong-guan Zhu,et al.  Selenium characterization in the global rice supply chain. , 2009, Environmental science & technology.

[31]  S. McGrath,et al.  Transporters of arsenite in rice and their role in arsenic accumulation in rice grain , 2008, Proceedings of the National Academy of Sciences.

[32]  J. Feldmann,et al.  The Rice Aquaporin Lsi1 Mediates Uptake of Methylated Arsenic Species1[W] , 2009, Plant Physiology.

[33]  A. Meharg,et al.  Arsenic contamination of Bangladesh paddy field soils: implications for rice contribution to arsenic consumption. , 2003, Environmental science & technology.

[34]  M. Beauchemin,et al.  Principal Component Analysis Approach for Modeling Sulfur K-XANES Spectra of Humic Acids , 2002 .

[35]  J. Feldmann,et al.  Arsenic accumulation and metabolism in rice (Oryza sativa L.). , 2002, Environmental science & technology.

[36]  Ren,et al.  Variations in Concentration and Distribution of Health-Related Elements Affected by Environmental and Genotypic Differences in Rice Grains , 2006 .

[37]  A. Meharg,et al.  Arsenate, arsenite and dimethyl arsinic acid (DMA) uptake and tolerance in maize (Zea mays L.) , 2008, Plant and Soil.

[38]  S. Wright,et al.  Pentavalent arsenic can bind to biomolecules. , 2007, Angewandte Chemie.