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 inPlant physiology (Bethesda) Vol. 152; no. 1; pp. 309 - 319
Main Authors Carey, Anne-Marie, Scheckel, Kirk G, Lombi, Enzo, Newville, Matt, Choi, Yongseong, Norton, Gareth J, Charnock, John M, Feldmann, Joerg, Price, Adam H, Meharg, Andrew A
Format Journal Article
LanguageEnglish
Published Rockville, MD American Society of Plant Biologists 01.01.2010
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Online AccessGet full text
ISSN0032-0889
1532-2548
1532-2548
DOI10.1104/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.
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
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Issue 1
Keywords Monocotyledones
Oryza
Arsenic
Grains
Plant physiology
Gramineae
Angiospermae
Unloading
Herbaceous plant
Spermatophyta
Language English
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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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Snippet 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...
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...
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SubjectTerms 60 APPLIED LIFE SCIENCES
analysis
Arsenates
Arsenic
Arsenic - analysis
Arsenic - metabolism
ARSENIC COMPOUNDS
Arsenites
Biological and medical sciences
Biological Transport
cacodylic acid
Cacodylic Acid - metabolism
carcinogens
CHEMICAL ANALYSIS
chemistry
endosperm
filling period
fluorescence
Fundamental and applied biological sciences. Psychology
Grains
hulls
inflorescences
leaves
mass spectrometry
metabolism
Oryza
Oryza - metabolism
Oryza sativa
Panicles
Phloem
Plant physiology and development
Plants
RICE
Seeds
Seeds - chemistry
Seeds - metabolism
Speciation
staple foods
UPTAKE
WHOLE PLANT AND ECOPHYSIOLOGY
Xylem
Title Grain Unloading of Arsenic Species in Rice
URI https://www.jstor.org/stable/25680649
https://www.ncbi.nlm.nih.gov/pubmed/19880610
https://www.proquest.com/docview/46462996
https://www.proquest.com/docview/733610527
https://www.osti.gov/biblio/1002242
https://pubmed.ncbi.nlm.nih.gov/PMC2799365
Volume 152
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