The hyperaccumulator Alyssum murale uses complexation with nitrogen and oxygen donor ligands for Ni transport and storage

David H. McNear; Rufus L. Chaney; Donald L. Sparks

doi:10.1016/j.phytochem.2009.10.023

The hyperaccumulator Alyssum murale uses complexation with nitrogen and oxygen donor ligands for Ni transport and storage

David H. McNear, Rufus L. Chaney, Donald L. Sparks

Plant and Soil Sciences

Research output: Contribution to journal › Article › peer-review

55 Scopus citations

Abstract

The Kotodesh genotype of the nickel (Ni) hyperaccumulator Alyssum murale was examined to determine the compartmentalization and internal speciation of Ni, and other elements, in an effort to ascertain the mechanism used by this plant to tolerate extremely high shoot (stem and leaf) Ni concentrations. Plants were grown either hydroponically or in Ni enriched soils from an area surrounding an historic Ni refinery in Port Colborne, Ontario, Canada. Electron probe micro-analysis (EPMA) and synchrotron based micro X-ray fluorescence (μ-SXRF) spectroscopy were used to determine the metal distribution and co-localization and synchrotron X-ray and attenuated total reflectance-Fourier transform infrared (ATR-FTIR) spectroscopies were used to determine the Ni speciation in plant parts and extracted sap. Nickel is concentrated in the dermal leaf and stem tissues of A. murale bound primarily to malate along with other low molecular weight organic ligands and possibly counter anions (e.g., sulfate). Ni is present in the plant sap and vasculature bound to histidine, malate and other low molecular weight compounds. The data presented herein supports a model in which Ni is transported from the roots to the shoots complexed with histidine and stored within the plant leaf dermal tissues complexed with malate, and other low molecular weight organic acids or counter-ions.

Original language	English
Pages (from-to)	188-200
Number of pages	13
Journal	Phytochemistry
Volume	71
Issue number	2-3
DOIs	https://doi.org/10.1016/j.phytochem.2009.10.023
State	Published - Feb 2010

Bibliographical note

Funding Information:
The authors would like to thank Dr. Ken Livi of the Department of Earth and Planetary Sciences at Johns Hopkins University for help with EMPA data collection, analysis and interpretation. We thank Dr. Kirk Czymeck of the Delaware Biotechnology Institute for help collecting the confocal and SEM image of leaf cross-sections. We thank Dr. Ryan Tappero for assistance/instruction with plant propagation and Dr. Mike Borda for help with collecting ATR-FTIR spectra. We thank Dr. Timothy Strathman for providing EXAFS spectra for selected Ni-organic acid standards. We thank Matthew Marcus for assistance with μ-EXAFS data collection at the Advanced Light Source (ALS) beamline 10.3.2 and the staff of beamline X11A at the National Synchrotron Light Source (NSLS) for their assistance in the collection of EXAFS standards spectra. The Advanced Light Source is supported by the Office of Science, Basic Energy Sciences, Division of Materials Science of the US Department of Energy under Contract No. DE-AC02-05CH11231. Use of the National Synchrotron Light Source, Brookhaven National Laboratory, was supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences, under Contract No. DE-AC02-98CH10886.

Keywords

Alyssum murale
Extended X-ray absorption fine structure (EXAFS) spectroscopy
Histidine
Hyperaccumulation
Malate
Nickel (Ni)
Synchrotron X-ray fluorescence (SXRF) spectroscopy
Tolerance

ASJC Scopus subject areas

Biochemistry
Molecular Biology
Plant Science
Horticulture

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10.1016/j.phytochem.2009.10.023

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@article{4e0d8ed8faf44f6aac0dffdfb1e93ccd,

title = "The hyperaccumulator Alyssum murale uses complexation with nitrogen and oxygen donor ligands for Ni transport and storage",

abstract = "The Kotodesh genotype of the nickel (Ni) hyperaccumulator Alyssum murale was examined to determine the compartmentalization and internal speciation of Ni, and other elements, in an effort to ascertain the mechanism used by this plant to tolerate extremely high shoot (stem and leaf) Ni concentrations. Plants were grown either hydroponically or in Ni enriched soils from an area surrounding an historic Ni refinery in Port Colborne, Ontario, Canada. Electron probe micro-analysis (EPMA) and synchrotron based micro X-ray fluorescence (μ-SXRF) spectroscopy were used to determine the metal distribution and co-localization and synchrotron X-ray and attenuated total reflectance-Fourier transform infrared (ATR-FTIR) spectroscopies were used to determine the Ni speciation in plant parts and extracted sap. Nickel is concentrated in the dermal leaf and stem tissues of A. murale bound primarily to malate along with other low molecular weight organic ligands and possibly counter anions (e.g., sulfate). Ni is present in the plant sap and vasculature bound to histidine, malate and other low molecular weight compounds. The data presented herein supports a model in which Ni is transported from the roots to the shoots complexed with histidine and stored within the plant leaf dermal tissues complexed with malate, and other low molecular weight organic acids or counter-ions.",

keywords = "Alyssum murale, Extended X-ray absorption fine structure (EXAFS) spectroscopy, Histidine, Hyperaccumulation, Malate, Nickel (Ni), Synchrotron X-ray fluorescence (SXRF) spectroscopy, Tolerance",

author = "McNear, {David H.} and Chaney, {Rufus L.} and Sparks, {Donald L.}",

note = "Funding Information: The authors would like to thank Dr. Ken Livi of the Department of Earth and Planetary Sciences at Johns Hopkins University for help with EMPA data collection, analysis and interpretation. We thank Dr. Kirk Czymeck of the Delaware Biotechnology Institute for help collecting the confocal and SEM image of leaf cross-sections. We thank Dr. Ryan Tappero for assistance/instruction with plant propagation and Dr. Mike Borda for help with collecting ATR-FTIR spectra. We thank Dr. Timothy Strathman for providing EXAFS spectra for selected Ni-organic acid standards. We thank Matthew Marcus for assistance with μ-EXAFS data collection at the Advanced Light Source (ALS) beamline 10.3.2 and the staff of beamline X11A at the National Synchrotron Light Source (NSLS) for their assistance in the collection of EXAFS standards spectra. The Advanced Light Source is supported by the Office of Science, Basic Energy Sciences, Division of Materials Science of the US Department of Energy under Contract No. DE-AC02-05CH11231. Use of the National Synchrotron Light Source, Brookhaven National Laboratory, was supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences, under Contract No. DE-AC02-98CH10886. ",

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AU - McNear, David H.

AU - Chaney, Rufus L.

AU - Sparks, Donald L.

N1 - Funding Information: The authors would like to thank Dr. Ken Livi of the Department of Earth and Planetary Sciences at Johns Hopkins University for help with EMPA data collection, analysis and interpretation. We thank Dr. Kirk Czymeck of the Delaware Biotechnology Institute for help collecting the confocal and SEM image of leaf cross-sections. We thank Dr. Ryan Tappero for assistance/instruction with plant propagation and Dr. Mike Borda for help with collecting ATR-FTIR spectra. We thank Dr. Timothy Strathman for providing EXAFS spectra for selected Ni-organic acid standards. We thank Matthew Marcus for assistance with μ-EXAFS data collection at the Advanced Light Source (ALS) beamline 10.3.2 and the staff of beamline X11A at the National Synchrotron Light Source (NSLS) for their assistance in the collection of EXAFS standards spectra. The Advanced Light Source is supported by the Office of Science, Basic Energy Sciences, Division of Materials Science of the US Department of Energy under Contract No. DE-AC02-05CH11231. Use of the National Synchrotron Light Source, Brookhaven National Laboratory, was supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences, under Contract No. DE-AC02-98CH10886.

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N2 - The Kotodesh genotype of the nickel (Ni) hyperaccumulator Alyssum murale was examined to determine the compartmentalization and internal speciation of Ni, and other elements, in an effort to ascertain the mechanism used by this plant to tolerate extremely high shoot (stem and leaf) Ni concentrations. Plants were grown either hydroponically or in Ni enriched soils from an area surrounding an historic Ni refinery in Port Colborne, Ontario, Canada. Electron probe micro-analysis (EPMA) and synchrotron based micro X-ray fluorescence (μ-SXRF) spectroscopy were used to determine the metal distribution and co-localization and synchrotron X-ray and attenuated total reflectance-Fourier transform infrared (ATR-FTIR) spectroscopies were used to determine the Ni speciation in plant parts and extracted sap. Nickel is concentrated in the dermal leaf and stem tissues of A. murale bound primarily to malate along with other low molecular weight organic ligands and possibly counter anions (e.g., sulfate). Ni is present in the plant sap and vasculature bound to histidine, malate and other low molecular weight compounds. The data presented herein supports a model in which Ni is transported from the roots to the shoots complexed with histidine and stored within the plant leaf dermal tissues complexed with malate, and other low molecular weight organic acids or counter-ions.

AB - The Kotodesh genotype of the nickel (Ni) hyperaccumulator Alyssum murale was examined to determine the compartmentalization and internal speciation of Ni, and other elements, in an effort to ascertain the mechanism used by this plant to tolerate extremely high shoot (stem and leaf) Ni concentrations. Plants were grown either hydroponically or in Ni enriched soils from an area surrounding an historic Ni refinery in Port Colborne, Ontario, Canada. Electron probe micro-analysis (EPMA) and synchrotron based micro X-ray fluorescence (μ-SXRF) spectroscopy were used to determine the metal distribution and co-localization and synchrotron X-ray and attenuated total reflectance-Fourier transform infrared (ATR-FTIR) spectroscopies were used to determine the Ni speciation in plant parts and extracted sap. Nickel is concentrated in the dermal leaf and stem tissues of A. murale bound primarily to malate along with other low molecular weight organic ligands and possibly counter anions (e.g., sulfate). Ni is present in the plant sap and vasculature bound to histidine, malate and other low molecular weight compounds. The data presented herein supports a model in which Ni is transported from the roots to the shoots complexed with histidine and stored within the plant leaf dermal tissues complexed with malate, and other low molecular weight organic acids or counter-ions.

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KW - Synchrotron X-ray fluorescence (SXRF) spectroscopy

KW - Tolerance

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ER -

The hyperaccumulator Alyssum murale uses complexation with nitrogen and oxygen donor ligands for Ni transport and storage

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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