Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors

Weber, Michael; Harada, Emiko; Vess, Christoph; Roepenack‐Lahaye, Edda v.; Clemens, Stephan

doi:10.1046/j.1365-313x.2003.01960.x

Cited by 440Plant Micronutrient Interactions and EffectsHeavy Metals in PlantsHeavy metals in environment

Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors

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Weber, Michael, Harada, Emiko, Vess, Christoph, Roepenack‐Lahaye, Edda v., Clemens, Stephan·2004·The Plant Journal

DOI 10.1046/j.1365-313x.2003.01960.x

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Abstract

The hyperaccumulation of zinc (Zn) and cadmium (Cd) is a constitutive property of the metallophyte Arabidopsis halleri. We therefore used Arabidopsis GeneChips to identify genes more active in roots of A. halleri as compared to A. thaliana under control conditions. The two genes showing highest expression in A. halleri roots relative to A. thaliana roots out of more than 8000 genes present on the chip encode a nicotianamine (NA) synthase and a putative Zn2+ uptake system. The significantly higher activity of these and other genes involved in metal homeostasis under various growth conditions was confirmed by Northern and RT-PCR analyses. A. halleri roots also show higher NA synthase protein levels. Furthermore, we developed a capillary liquid chromatography electrospray ionization quadrupole time-of-flight mass spectrometry (CapLC-ESI-QTOF-MS)-based NA analysis procedure and consistently found higher NA levels in roots of A. halleri. Expression of a NA synthase in Zn2+-hypersensitive Schizosaccharomyces pombe cells demonstrated that formation of NA can confer Zn2+ tolerance. Taken together, these observations implicate NA in plant Zn homeostasis and NA synthase in the hyperaccumulation of Zn by A. halleri. Furthermore, the results show that comparative microarray analysis of closely related species can be a valuable tool for the elucidation of phenotypic differences between such species.

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Overexpression of several ZIP family member transporters has been reported in A. halleri and T. caerulescens to hyperaccumulate Zn metal ions.
“In addition, overexpression of several ZIP family member transporters has been reported in A. halleri and T. caerulescens to hyperaccumulate Zn metal ions (Becher et al., 2004; Weber et al., 2004; Filatov et al., 2006; Hammond et al., 2006; Talke et al., 2006; Krämer et al., 2007).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as Weber et al., 2004
The results report higher ZIP9 expression in A. halleri roots, and the Discussion links high ZIP expression to greater metal uptake capacity. The Discussion mentions earlier observations of ZNT1 expression in T. caerulescens, but the passages do not establish overexpression of several ZIP transporters in that species. Page numbers are unavailable in our copy. (LLM, conf=0.85)
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In Cd/Zn non-hyperaccumulator plants, the expression of ZIPs was detected only under Zn-deficient conditions, suggesting a Zn-mediated regulation unlike the constitutive expression observed in the hyperaccumulator counterpart.
“While in Cd/Zn non-hyperaccumulator plants, the expression of ZIPs was detected only under Zn-deficient conditions, suggesting a Zn-mediated regulation unlike the constitutive expression observed in the hyperaccumulator counterpart (Weber et al., 2004; Yan et al., 2020).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as Weber et al., 2004
The Results passage on Zn supply reports that ZIP9 expression in non-hyperaccumulating A. thaliana roots was highest under Zn deficiency and appeared downregulated under Zn-replete conditions; it does not say expression was detected only under deficiency. The Discussion says ZIP9 in hyperaccumulating A. halleri remained responsive to Zn levels, while a later Discussion passage reports high ZIP9 expression even under replete conditions. The claim therefore captures the contrast in expression levels but overstates it as deficiency-only versus constitutive expression. (LLM, conf=0.88)
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Authors: Weber, M., Harada, E., Vess, C., Roepenack‐Lahaye, E. V., & Clemens, S.
Affiliations: Leibniz Institute of Plant Biochemistry (DE)
Corresponding author: Clemens, Stephan
ORCID: Weber, Michael
Harada, Emiko
Roepenack‐Lahaye, Edda v.
Clemens, Stephan
Venue: The Plant Journal
Publisher: Wiley
Published: 2003-12-04
Volume: 37
Issue: 2
Pages: 269-281
ISSN: 0960-7412 (ISSN-L)
1365-313X
DOI: 10.1046/j.1365-313x.2003.01960.x
OpenAlex: W1951962559
Cited by: 440
References: 65
Citations by year: 2026: 4 · 2025: 7 · 2024: 11 · 2023: 6 · 2022: 5 · 2021: 20 · 2020: 24 · 2019: 21 · 2018: 17 · 2017: 12 · 2016: 16 · 2015: 18 · 2014: 20 · 2013: 22 · 2012: 24
FWCI: 28.80
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Plant Journal (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Micronutrient Interactions and Effects
Physical Sciences › Chemistry › Analytical Chemistry › Heavy Metals in Plants
Physical Sciences › Environmental Science › Pollution › Heavy metals in environment
Keywords: metal hyperaccumulation, Arabidopsis halleri, Arabidopsis thaliana, nicotianamine synthase, nicotianamine, zinc homeostasis, cadmium, ZIP transporters, metallophytes, root gene expression, zinc tolerance, Schizosaccharomyces pombe
MeSH terms: Kinetics, Metals, Transcription Factors, Gene Expression Regulation, Enzymologic, Arabidopsis, Gene Expression Regulation, Plant, Plant Roots, Alkyl and Aryl Transferases, Oligonucleotide Array Sequence Analysis, Arabidopsis Proteins

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Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors

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