Grain Unloading of Arsenic Species in Rice
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)...
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Published in | Plant physiology (Bethesda) Vol. 152; no. 1; pp. 309 - 319 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
Rockville, MD
American Society of Plant Biologists
01.01.2010
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Subjects | |
Online Access | Get full text |
ISSN | 0032-0889 1532-2548 1532-2548 |
DOI | 10.1104/pp.109.146126 |
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Abstract | 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. |
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AbstractList | 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. 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. 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. 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.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. |
Author | Price, Adam H Choi, Yongseong Carey, Anne-Marie Scheckel, Kirk G Lombi, Enzo Newville, Matt Meharg, Andrew A Charnock, John M Feldmann, Joerg Norton, Gareth J |
AuthorAffiliation | Institute of Biology and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, United Kingdom (A.-M.C., G.J.N., A.H.P., A.A.M.); National Risk Management Research Laboratory, United States Environmental Protection Agency, Cincinnati, Ohio 45224 (K.G.S.); Centre for Environmental Risk Assessment and Remediation, University of South Australia, Mawson Lakes, South Australia SA–5095, Australia (E.L.); Cooperative Research Centre for Contamination Assessment and Remediation of the Environment, Salisbury, South Australia 5106, Australia (E.L.); GSECARS Advanced Photon Source, Argonne National Laboratory, Argonne, Illinois 60439 (M.N., Y.C.); Centre for Molecular Environmental Science, University of Manchester, Manchester M13 9PL, United Kingdom (J.M.C.); Council for the Central Laboratory of the Research Councils Daresbury Laboratory, Daresbury, Warrington WA4 4AD, United Kingdom (J.M.C.); and Department of Chemistry, University of Aberdeen, Meston Walk, Aberdeen AB24 3TU, Unite |
AuthorAffiliation_xml | – name: Institute of Biology and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, United Kingdom (A.-M.C., G.J.N., A.H.P., A.A.M.); National Risk Management Research Laboratory, United States Environmental Protection Agency, Cincinnati, Ohio 45224 (K.G.S.); Centre for Environmental Risk Assessment and Remediation, University of South Australia, Mawson Lakes, South Australia SA–5095, Australia (E.L.); Cooperative Research Centre for Contamination Assessment and Remediation of the Environment, Salisbury, South Australia 5106, Australia (E.L.); GSECARS Advanced Photon Source, Argonne National Laboratory, Argonne, Illinois 60439 (M.N., Y.C.); Centre for Molecular Environmental Science, University of Manchester, Manchester M13 9PL, United Kingdom (J.M.C.); Council for the Central Laboratory of the Research Councils Daresbury Laboratory, Daresbury, Warrington WA4 4AD, United Kingdom (J.M.C.); and Department of Chemistry, University of Aberdeen, Meston Walk, Aberdeen AB24 3TU, United Kingdom (J.F.) |
Author_xml | – sequence: 1 fullname: Carey, Anne-Marie – sequence: 2 fullname: Scheckel, Kirk G – sequence: 3 fullname: Lombi, Enzo – sequence: 4 fullname: Newville, Matt – sequence: 5 fullname: Choi, Yongseong – sequence: 6 fullname: Norton, Gareth J – sequence: 7 fullname: Charnock, John M – sequence: 8 fullname: Feldmann, Joerg – sequence: 9 fullname: Price, Adam H – sequence: 10 fullname: Meharg, Andrew A |
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ContentType | Journal Article |
Copyright | 2010 American Society of Plant Biologists 2015 INIST-CNRS Copyright © 2010, American Society of Plant Biologists 2010 |
Copyright_xml | – notice: 2010 American Society of Plant Biologists – notice: 2015 INIST-CNRS – notice: Copyright © 2010, American Society of Plant Biologists 2010 |
CorporateAuthor | Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS) |
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Keywords | Monocotyledones Oryza Arsenic Grains Plant physiology Gramineae Angiospermae Unloading Herbaceous plant Spermatophyta |
Language | English |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 USDOE www.plantphysiol.org/cgi/doi/10.1104/pp.109.146126 The online version of this article contains Web-only data. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Andrew A. Meharg (a.meharg@abdn.ac.uk). This work was supported by a Biotechnology and Biological Sciences Research Council Doctoral Training Grant. Portions of this work were performed at GeoSoilEnviroCARS (sector 13) and PNC/XOR (sector 20), at the Advanced Photon Source, Argonne National Laboratory. GeoSoilEnviro Consortium for Advanced Radiation Sources is supported by the National Science Foundation-Earth Sciences (grant no. EAR–0622171) and Department of Energy-Geosciences (grant no. DE–FG02-94ER14466). Pacific Northwest Consortium Collaborative Access Team Advanced Photon Source, Sector 20 facilities at the Advanced Photon Source, and research at these facilities, are supported by the U.S. Department of Energy-Basic Energy Sciences, a major facilities access grant from the Natural Sciences and Engineering Research Council, the University of Washington, Simon Fraser University, and the Advanced Photon Source. Use of the Advanced Photon Source was supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences (under contract no. DE–AC02–06CH11357). The U.S. Environmental Protection Agency, through its Office of Research and Development, funded and managed a portion of the research; it has not been subject to Agency review and, therefore, does not necessarily reflect the views of the Agency, no official product endorsement should be inferred. |
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Title | Grain Unloading of Arsenic Species in Rice |
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