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MTP1-dependent Zn sequestration into shoot vacuoles suggests dual roles in Zn tolerance and accumulation in Zn-hyperaccumulating plants
Open accessAbstract
The integral membrane protein Thlaspi goesingense metal tolerance protein 1 (TgMTP1) has been suggested to play an important role in Zn hyperaccumulation in T. goesingense. Here, we show that the TgMTP1 protein is accumulated to high levels at the vacuolar membrane in shoot tissue of T. goesingense. TgMTP1 is likely to act in the transport of Zn into the vacuole, enhancing both Zn accumulation and tolerance. By specifically expressing TgMTP1 in Arabidopsis thaliana shoots, we show that TgMTP1, localized at the vacuolar membrane, can drive the enhanced shoot accumulation of Zn by initiating a systemic Zn deficiency response. The systematic response includes increased expression of Zn transporters (ZIP3, ZIP4, ZIP5 and ZIP9) in both shoot and root tissue. Furthermore, shoot-specific accumulation of TgMTP1 at the vacuolar membrane also leads to increased resistance to Zn in A. thaliana, probably through enhanced Zn compartmentalization in the vacuole. Such evidence leads to the conclusion that the high levels of TgMTP1 at the vacuolar membrane in shoot tissue of the Zn hyperaccumulator T. goesingense play a role in both Zn tolerance and enhanced Zn uptake and accumulation, via the activation of a systemic Zn deficiency response.
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“Moreover, MTP1 was overexpressed in A. halleri and N. caerulescens to transport Zn and Cd (Dräger et al., 2004; Gustin et al., 2009).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as Gustin et al., 2009
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“The transformation of TgMTP1 in A. thaliana resulted in enhanced accumulation of Zn into vacuoles, attributing to Zn tolerance (Gustin et al., 2009).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as Gustin et al., 2009
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Responses of Phytochelatins and Metallothioneins in Alleviation of Heavy Metal Stress in Plants
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Arruda, M. A. Z., & Azevedo, R. A. (2009) · Annals of Applied Biology · doi:10.1111/j.1744-7348.2009.00371.x · Cited by 64
Comparative understanding of metal hyperaccumulation in plants: a mini-review
Peng, J.-S., Guan, Y.-H., Lin, X.-J., Xu, X.-J., Xiao, L., Wang, H.-H., & Meng, S. (2021) · Environmental Geochemistry and Health · doi:10.1007/s10653-020-00533-2 · Cited by 63
“…thaliana microarray system revealed that genes that control many key steps of metal transport and chelation exhibit increased expression (Becher et al. 2004; Weber et al. 2004, 2005; Chiang et al. 2006; Filatov et al. 2006; Hammond et al. 2006; Talke et al. 2006; van de Mortel et al. 2006).”
BackgroundHow metal hyperaccumulating plants can advance Zn biofortification
Clemens, S. (2016) · Plant and Soil · doi:10.1007/s11104-016-2920-3 · Cited by 63
“Such secondary activation of Zn acquisition pathways can also be seen when in the non- hyperaccumulator A. thaliana vacuolar Zn storage is enhanced through the overexpression of an MTP1 gene (Gustin et al. 2009).”
BackgroundPhytoremediation of Soils Contaminated with Heavy Metals: Techniques and Strategies
Pinto, A. P., de Varennes, A., Fonseca, R., & Teixeira, D. M. (2014) · Springer eBooks · doi:10.1007/978-3-319-10395-2_10 · Cited by 63
Sharma, A. K., Sharma, M., Sharma, S., Malik, D. S., Sharma, M., Sharma, M., & Sharma, A. K. (2024) · Journal of Geochemical Exploration · doi:10.1016/j.gexplo.2024.107472 · Cited by 71
Song, W., Hörtensteiner, S., Tomioka, R., Lee, Y., & Martinoia, E. (2011) · Molecules and Cells · doi:10.1007/s10059-011-0024-8 · Cited by 60
Biomolecular approaches to understanding metal tolerance and hyperaccumulation in plants
Corso, M., & García de la Torre, V. S. (2020) · Metallomics · doi:10.1039/d0mt00043d · Cited by 60
Control of Zn uptake in Arabidopsis halleri: a balance between Zn and Fe
Varanavasiappan, S., Lo, J., & Yeh, K. (2013) · Frontiers in Plant Science · doi:10.3389/fpls.2013.00281 · Cited by 60
“…Zn transporter, is highly expressed in both roots and shoots of A. halleri and also linked to a major quantitative trait locus (QTL) responsible for Zn tolerance (Drager et al., 2004; Kobae et al., 2004; Gustin et al., 2009; Kawachi et al., 2009; Shahzad et al., 2010; Willems et al., 2010).”
BackgroundCalcium Deficiency Triggers Phloem Remobilization of Cadmium in a Hyperaccumulating Species
Tian, S., Xie, R., Wang, H., Hu, Y., Ge, J., Liao, X., Gao, X., Brown, P. H., Lin, X., & Lu, L. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.01348 · Cited by 58
“…recent research presented a Ca2+-transporting P-type ATPase, ACA8, as a novel candidate for Cd accumulation in the hyperaccumulatorN. caerulescens (Halimaa et al., 2014), and a gene encoding a Ca2+/H+ antiporter, CAX1, was identified as a candidate gene for Cd tolerance in A. halleri (Baliardini…”
BackgroundNew Insights into the Transport Mechanisms in Plant Vacuoles
Shitan, N., & Yazaki, K. (2013) · International review of cytology · doi:10.1016/b978-0-12-407695-2.00009-3 · Cited by 60
Hafeez, F. Y., Ullah, M. A., & Hassan, M. N. (2013) · Springer eBooks · doi:10.1007/978-3-642-37241-4_9 · Cited by 58
Khalid, N., Aqeel, M. A., & Noman, A. (2019) · Springer eBooks · doi:10.1007/978-3-030-19103-0_6 · Cited by 57
Plants that Hyperaccumulate Heavy Metals
Fasani, E. (2012) · Springer briefs in molecular science · doi:10.1007/978-94-007-4441-7_3 · Cited by 56
Kühnlenz, T., Hofmann, C., Uraguchi, S., Schmidt, H., Schempp, S., Weber, M., Lahner, B., Salt, D. E., & Clemens, S. (2016) · Plant and Cell Physiology · doi:10.1093/pcp/pcw148 · Cited by 55
Self-citationBazihizina, N., Taiti, C., Marti, L., Rodrigo-Moreno, A., Spinelli, F., Giordano, C., Caparrotta, S., Gori, M., Azzarello, E., & Mancuso, S. (2014) · Journal of Experimental Botany · doi:10.1093/jxb/eru251 · Cited by 53
Dang, F., Lin, J., Chen, Y., Li, G., Guan, D., Zheng, S. J., & He, S. (2019) · Journal of Experimental Botany · doi:10.1093/jxb/erz006 · Cited by 55
“Our findings suggest that the enhanced Cd contents might be due to the up-regulation of various Zn transporter genes, such as AtZIP3 , AtZIP4 , and AtZIP9 , by CaWRKY41 (Supplementary Fig.”
InfluentialKawachi, M., Kobae, Y., Kogawa, S., Mimura, T., Krämer, U., & Maeshima, M. (2012) · FEBS Journal · doi:10.1111/j.1742-4658.2012.08613.x · Cited by 54
Sánchez, E., García-Bañuelos, M. L., & Sida-Arreola, J. P. (2014) · Journal of Elementology · doi:10.5601/jelem.2014.19.3.708 · Cited by 54
Phytoremediation of Heavy Metals: An Eco-Friendly and Sustainable Approach
Haq, S., Bhatti, A. A., Dar, Z. A., & Bhat, S. A. (2020) · Springer eBooks · doi:10.1007/978-3-030-35691-0_10 · Cited by 56
Hussain, A., Zahir, Z. A., Asghar, H. N., Ahmad, M., Jamil, M., Naveed, M., & Akhtar, M. F. U. Z. (2018) · Springer eBooks · doi:10.1007/978-981-13-0044-8_7 · Cited by 52
Lang, M., Hao, M., Fan, Q., Wang, W., Mo, S., Zhao, W., & Zhou, J. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/err137 · Cited by 50
“…when expressed in yeast (Delhaize et al., 2003), TgMTP1 from T. goesingense was localized to both the plasma membrane (in yeast cells and protoplasts of A. thaliana shoot tissues) and vacuolar membranes (in A. thaliana and T. goesingense shoot tissues) (Kim et al., 2004; Gustin et al., 2009).”
InfluentialCurrent understanding of plant zinc homeostasis regulation mechanisms
Zlobin, I. E. (2021) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2021.03.003 · Cited by 48
Lu, L., Liao, X., Labavitch, J. M., Yang, X., Nelson, E., Du, Y., Brown, P. H., & Tian, S. (2014) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2014.10.004 · Cited by 45
“MTP1 is a Zn transporter in the vacuolar membrane that mediates Zn detoxification and drives leaf Zn accumulation in Zn hyperaccumulator plants Arabidopsis thaliana and Thlaspi goesingense (Desbrosses-Fonrouge et al., 2005; Gustin et al., 2009; Kobae et al., 2004).”
BackgroundZhang, M., Senoura, T., Yang, X., & Nishizawa, N. K. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.07.013 · Cited by 45
“The localization of SaMTP1 was the same with the localization of AtMTP1, AhMTP1 and TgMTP1 [12,16,17].”
BackgroundPhysiology and Molecular Biology of Trace Element Hyperaccumulation
Merlot, S., de la Torre, V. S. G., & Hanikenne, M. (2017) · Mineral resource reviews · doi:10.1007/978-3-319-61899-9_6 · Cited by 44
Migocka, M., Papierniak, A., Kosatka, E., & Kłobus, G. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/err180 · Cited by 39
“TcMTP1, the CDF transporter in heavy metal hyperaccumulator Thlaspi goesingense, is accumulated to high levels at the tonoplast of shoot cells, participating in the enhanced tolerance of the plant to Zn and Cd (Persans et al., 2001; Gustin et al., 2009).”
BackgroundRetractedLi, X., Wu, Y., Li, B., He, W., Yang, Y., & Yang, Y. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00103 · Cited by 39
Machado-Estrada, B., Calderón, J., Moreno‐Sánchez, R., & Rodríguez‐Zavala, J. S. (2012) · Environmental Science and Pollution Research · doi:10.1007/s11356-012-1344-8 · Cited by 36
“In this regard, free histidine has been proposed to play a key role in metal translocation through the xylem along with the participation of Zn transporters to take up the metal into the cytosol and vacuole (Mills et al. 2005; Gustin et al. 2009; Maestri et al. 2010).”
BackgroundZinc-Solubilizing Bacteria: An Option to Increase Zinc Uptake by Plants
Haroon, M., Khan, S. T., & Malik, A. R. A. (2021) · Springer eBooks · doi:10.1007/978-3-030-76609-2_11 · Cited by 35
Metadata
- Authors
- Gustin, J. L., Loureiro, M. E., Kim, D., Na, G., Tikhonova, M., & Salt, D. E.
- Affiliations
- Purdue University West Lafayette (US)
- Universidade Federal de Viçosa (BR)
- Gyeongsang National University (KR)
- Corresponding author
- Salt, David E.
- ORCID
- Gustin, Jeffery L.
- Venue
- The Plant Journal
- Publisher
- Wiley
- Published
- 2009-03
- Volume
- 57
- Issue
- 6
- Pages
- 1116-1127
- ISSN
- 0960-7412 (ISSN-L)
- 1365-313X
- OpenAlex
- W2119893617
- Cited by
- 203
- References
- 46
- Citations by year
- 2026: 7 · 2025: 7 · 2024: 7 · 2023: 8 · 2022: 4 · 2021: 24 · 2020: 18 · 2019: 15 · 2018: 8 · 2017: 10 · 2016: 12 · 2015: 8 · 2014: 13 · 2013: 14 · 2012: 11
- FWCI
- 14.92
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Plant Journal (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- Purdue University
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Micronutrient Interactions and Effects
- Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
- Physical Sciences › Chemistry › Analytical Chemistry › Heavy Metals in Plants
- Keywords
- metal tolerance proteins, zinc hyperaccumulation, tonoplast, zinc tolerance, ZIP transporters, zinc uptake, Arabidopsis thaliana transformation, metal hyperaccumulator plants
- MeSH terms
- Amino Acid Sequence, Molecular Sequence Data, Plant Proteins, Vacuoles, Zinc, Sequence Alignment, Arabidopsis, Gene Expression Regulation, Plant, Plant Shoots, Cation Transport Proteins, Thlaspi
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