Large Expression Differences in Genes for Iron and Zinc Homeostasis, Stress Response, and Lignin Biosynthesis Distinguish Roots of Arabidopsis thaliana and the Related Metal Hyperaccumulator Thlaspi caerulescens

van de Mortel, Judith E.; Almar Villanueva, Laia; Schat, Henk; Kwekkeboom, Jeroen; Coughlan, Sean; Moerland, Perry D.; Ver Loren van Themaat, Emiel; Koornneef, Maarten; Aarts, Mark G.M.

doi:10.1104/pp.106.082073

Cited by 547Plant Micronutrient Interactions and EffectsTrace Elements in HealthPlant Molecular Biology Research

Large Expression Differences in Genes for Iron and Zinc Homeostasis, Stress Response, and Lignin Biosynthesis Distinguish Roots of Arabidopsis thaliana and the Related Metal Hyperaccumulator Thlaspi caerulescens

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van de Mortel, Judith E., Almar Villanueva, Laia, Schat, Henk, Kwekkeboom, Jeroen, Coughlan, Sean, Moerland, Perry D., Ver Loren van Themaat, Emiel, Koornneef, Maarten +1 more·2006·Plant Physiology

DOI 10.1104/pp.106.082073PMC PMC1630723

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Abstract

The micronutrient zinc has an essential role in physiological and metabolic processes in plants as a cofactor or structural element in 300 catalytic and noncatalytic proteins, but it is very toxic when available in elevated amounts. Plants tightly regulate their internal zinc concentrations in a process called zinc homeostasis. The exceptional zinc hyperaccumulator species Thlaspi caerulescens can accumulate up to 3% of zinc, but also high amounts of nickel and cadmium, without any sign of toxicity. This should have drastic effects on the zinc homeostasis mechanism. We examined in detail the transcription profiles of roots of Arabidopsis thaliana and T. caerulescens plants grown under deficient, sufficient, and excess supply of zinc. A total of 608 zinc-responsive genes with at least a 3-fold difference in expression level were detected in A. thaliana and 352 in T. caerulescens in response to changes in zinc supply. Only 14% of these genes were also zinc responsive in A. thaliana. When comparing A. thaliana with T. caerulescens at each zinc exposure, more than 2,200 genes were significantly differentially expressed (≥5-fold and false discovery rate < 0.05). While a large fraction of these genes are of yet unknown function, many genes with a different expression between A. thaliana and T. caerulescens appear to function in metal homeostasis, in abiotic stress response, and in lignin biosynthesis. The high expression of lignin biosynthesis genes corresponds to the deposition of lignin in the endodermis, of which there are two layers in T. caerulescens roots and only one in A. thaliana.

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HMA4 encoding Cd and Zn metal ion transporter is overexpressed in the roots and shoots of both A. halleri and T. caerulescens metal ion hyperaccumulators.
“Moreover, it is reported that HMA4 encoding Cd and Zn metal ion transporter is overexpressed in the roots and shoots of both A. halleri and T. caerulescens metal ion hyperaccumulators (Bernard et al., 2004; van de Mortel et al., 2006; Courbot 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 van de Mortel et al., 2006
The Discussion (page not provided) reports higher HMA4 expression in T. caerulescens roots and cites higher expression in A. halleri without specifying tissue. The Semiquantitative Reverse Transcription-PCR section (page not provided) also reports TcHMA4 expression in leaves. Our copy does not establish higher HMA4 expression in both roots and shoots of A. halleri, or identify HMA4 as a cadmium transporter; it identifies HMA4 as a zinc transporter. (LLM, conf=0.86)
Experimental — accuracy not yet measured
FDR3 is another transporter belonging to the MATE (Multidrug and Toxin Efflux) gene family of transporters overexpressed in the root pericycle of A. halleri and T. caerulescens to hyperaccumulate Fe.
“FDR3 is another transporter belonging to the MATE (Multidrug and Toxin Efflux) gene family of transporters overexpressed in the root pericycle of A. halleri and T. caerulescens to hyperaccumulate Fe (Talke et al., 2006; van de Mortel et al., 2006).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as van de Mortel et al., 2006
Table IV identifies FRD3 as a MATE efflux family protein, and the Discussion reports higher expression of its ortholog in T. caerulescens than in A. thaliana. The Discussion also reports higher expression in A. halleri, citing Talke et al. (2006), and links FRD3 to iron homeostasis. It does not establish expression specifically in the root pericycle or that FRD3 causes iron hyperaccumulation in either species; the cited finding concerns zinc-hyperaccumulating plants. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Overexpression of ZNT1 was further confirmed by microarray analysis.
“The overexpression of ZNT1 was further confirmed by microarray analysis (Hammond et al., 2006; van de Mortel et al., 2006).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as van de Mortel et al., 2006

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Authors: van de Mortel, J. E., Almar Villanueva, L., Schat, H., Kwekkeboom, J., Coughlan, S., Moerland, P. D., Ver Loren van Themaat, E., Koornneef, M., & Aarts, M. G. M.
Affiliations: Laboratory of Genetics, Wageningen University, 6703 BD Wageningen, The Netherlands (J.E.v.d.M., L.A.V., M.K., M.G.M.A.); Institute of Ecological Sciences, Faculty of Earth and Life Sciences, Vrije Universiteit, 1081 HV Amsterdam, The Netherlands (H.S.); ServiceXS BV, 2333 AL Leiden, The Netherlands (J.K.); Agilent Technologies, Little Falls Site, Wilmington, Delaware 19808–1644 (S.C.); and Bioinf
Amsterdam UMC Location University of Amsterdam (NL)
ORCID: Moerland, Perry D.
Koornneef, Maarten
Aarts, Mark G.M.
Venue: Plant Physiology
Publisher: Oxford University Press (OUP)
Published: 2006-09-22
Volume: 142
Issue: 3
Pages: 1127-1147
ISSN: 0032-0889 (ISSN-L)
1532-2548
DOI: 10.1104/pp.106.082073
PMC: PMC1630723
OpenAlex: W2162834837
Semantic Scholar: 4645c206f855941c2af395c0cadc4052a5bafafe
Cited by: 547
References: 85
Citations by year: 2026: 11 · 2025: 31 · 2024: 20 · 2023: 23 · 2022: 31 · 2021: 50 · 2020: 33 · 2019: 30 · 2018: 26 · 2017: 24 · 2016: 28 · 2015: 21 · 2014: 38 · 2013: 33 · 2012: 33
FWCI: 24.29
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Locations: PLANT PHYSIOLOGY (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Pure Amsterdam UMC (publishedVersion)
Socio-Environmental Systems Modeling (acceptedVersion)
VU Research Portal (submittedVersion, other-oa)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Data Archiving and Networked Services (DANS) (submittedVersion)
Funders: European Commission
Nederlandse Organisatie voor Wetenschappelijk Onderzoek
Arizona Biomedical Research Commission
Topics: Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Micronutrient Interactions and Effects
Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
Keywords: zinc homeostasis, Thlaspi caerulescens, Arabidopsis thaliana, metal hyperaccumulation, differential gene expression, root transcriptome, abiotic stress response, lignin biosynthesis, endodermis, micronutrient toxicity
MeSH terms: Biodegradation, Environmental, Homeostasis, Iron, Lignin, Plant Proteins, Species Specificity, Zinc, Arabidopsis, Gene Expression Regulation, Plant, Plant Roots, Gene Expression Profiling, Thlaspi

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Large Expression Differences in Genes for Iron and Zinc Homeostasis, Stress Response, and Lignin Biosynthesis Distinguish Roots of Arabidopsis thaliana and the Related Metal Hyperaccumulator Thlaspi caerulescens

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