Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd‐hyperaccumulating ecotype of Thlaspi caerulescens

Ueno, Daisei; Milner, Matthew J.; Yamaji, Naoki; Yokosho, Kengo; Koyama, Emi; Clemencia Zambrano, M.; Kaskie, Molly; Ebbs, Stephen; Kochian, Leon V.; Ma, Jian Feng

doi:10.1111/j.1365-313x.2011.04548.x

Cited by 243Heavy metals in environmentHeavy Metals in PlantsPlant Stress Responses and Tolerance

Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd‐hyperaccumulating ecotype of Thlaspi caerulescens

Ueno, Daisei, Milner, Matthew J., Yamaji, Naoki, Yokosho, Kengo, Koyama, Emi, Clemencia Zambrano, M., Kaskie, Molly, Ebbs, Stephen +2 more·2011·The Plant Journal

DOI 10.1111/j.1365-313x.2011.04548.x

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Abstract

Cadmium (Cd) is a highly toxic heavy metal for plants, but several unique Cd-hyperaccumulating plant species are able to accumulate this metal to extraordinary concentrations in the aboveground tissues without showing any toxic symptoms. However, the molecular mechanisms underlying this hypertolerance to Cd are poorly understood. Here we have isolated and functionally characterized an allelic gene, TcHMA3 (heavy metal ATPase 3) from two ecotypes (Ganges and Prayon) of Thlaspi caerulescens contrasting in Cd accumulation and tolerance. The TcHMA3 alleles from the higher (Ganges) and lower Cd-accumulating ecotype (Prayon) share 97.8% identity, and encode a P(1B)-type ATPase. There were no differences in the expression pattern, cell-specificity of protein localization and transport substrate-specificity of TcHMA3 between the two ecotypes. Both alleles were characterized by constitutive expression in the shoot and root, a tonoplast localization of the protein in all leaf cells and specific transport activity for Cd. The only difference between the two ecotypes was the expression level of TcHMA3: Ganges showed a sevenfold higher expression than Prayon, partly caused by a higher copy number. Furthermore, the expression level and localization of TcHMA3 were different from AtHMA3 expression in Arabidopsis. Overexpression of TcHMA3 in Arabidopsis significantly enhanced tolerance to Cd and slightly increased tolerance to Zn, but did not change Co or Pb tolerance. These results indicate that TcHMA3 is a tonoplast-localized transporter highly specific for Cd, which is responsible for sequestration of Cd into the leaf vacuoles, and that a higher expression of this gene is required for Cd hypertolerance in the Cd-hyperaccumulating ecotype of T. caerulescens.

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Similar types of enhancement in expression were due to a five times more copy number of TcHMA3 transporter to accumulate Cd in ecotypes of N. caerulescens.
“Similar types of enhancement in expression were due to a five times more copy number of TcHMA3 transporter to accumulate Cd in ecotypes of N. caerulescens (Ueno et al., 2011).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as Ueno et al., 2011
A higher copy number resulted in over-expression of TcHMA3 gene encoding Cd transporters in Saint-Laurent-le-Minier (Ganges) population compared to the Prayon population of N. caerulescens.
“In addition, it was observed that a higher copy number resulted in over-expression of TcHMA3 gene encoding Cd transporters in Saint- Laurent-le-Minier (Ganges) population compared to the Prayon population of N. caerulescens (Ueno et al., 2011).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as Ueno et al., 2011
Several transporters were overexpressed, such as SpHMA1 in S. plumbizincicola, SaZIP4 in Sedum alfredii, and TcYSL3, TcHMA3, TcYSL5, and TcYSL7 in N. caerulescens plants for transport of metal ions.
“Several transporters were overexpressed, such as SpHMA1 in S. plumbizincicola, SaZIP4 in Sedum alfredii, and TcYSL3, TcHMA3, TcYSL5, and TcYSL7 in N. caerulescens plants for transport of metal ions (Gendre et al., 2007; Ueno et al., 2011; Zhao et al., 2019).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as Ueno et al., 2011

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Усманова, О. В., Саидмурадов, Ш. Д., & Якубова, М. М. (2012) · Доклады Академии наук Республики Таджикистан
Transcriptomic and cell wall proteomic datasets of rosettes and floral stems from five Arabidopsis thaliana ecotypes grown at optimal or sub-optimal temperature
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Expression of a High Mobility Group Protein Isolated from Cucumis sativus Affects the Germination of Arabidopsis thaliana under Abiotic Stress Conditions
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Authors: Ueno, D., Milner, M. J., Yamaji, N., Yokosho, K., Koyama, E., Clemencia Zambrano, M., Kaskie, M., Ebbs, S., Kochian, L. V., & Ma, J. F.
Affiliations: Okayama University (JP)
United States Department of Agriculture (US)
Southern Illinois University Carbondale (US)
Corresponding author: Kochian, Leon V.
ORCID: Ueno, Daisei
Milner, Matthew J.
Yamaji, Naoki
Yokosho, Kengo
Ebbs, Stephen
Kochian, Leon V.
Venue: The Plant Journal
Publisher: Wiley
Published: 2011-04-04
Volume: 66
Issue: 5
Pages: 852-862
ISSN: 0960-7412 (ISSN-L)
1365-313X
DOI: 10.1111/j.1365-313x.2011.04548.x
OpenAlex: W1529362576
Cited by: 243
References: 56
Citations by year: 2026: 7 · 2025: 16 · 2024: 15 · 2023: 16 · 2022: 17 · 2021: 12 · 2020: 21 · 2019: 16 · 2018: 21 · 2017: 14 · 2016: 15 · 2015: 14 · 2014: 18 · 2013: 18 · 2012: 18
FWCI: 17.50
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Plant Journal (publishedVersion)
PubMed (publishedVersion)
Funders: Agricultural Research Service
Topics: Physical Sciences › Environmental Science › Pollution › Heavy metals in environment
Physical Sciences › Chemistry › Analytical Chemistry › Heavy Metals in Plants
Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
Keywords: Thlaspi caerulescens, heavy metal ATPase, cadmium hyperaccumulation, cadmium tolerance, vacuolar sequestration, gene expression levels, gene copy number, allelic variation, Arabidopsis overexpression, zinc tolerance
MeSH terms: Adenosine Triphosphatases, Alleles, Cadmium, Cloning, Molecular, Phylogeny, Plant Proteins, Transfection, Yeasts, Arabidopsis, Gene Expression Regulation, Plant, Plant Roots, Plant Shoots, Gene Dosage, Gene Expression Profiling, Membrane Transport Proteins, Plants, Genetically Modified, Thlaspi

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Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd‐hyperaccumulating ecotype of Thlaspi caerulescens

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