TcYSL3, a member of the YSL gene family from the hyper‐accumulator Thlaspi caerulescens, encodes a nicotianamine‐Ni/Fe transporter
Abstract
The two main features of plant hyper-accumulator species are the massive translocation of heavy metal ions to the aerial parts and their tolerance to such high metal concentrations. Recently, several lines of evidence have indicated a role for nicotianamine (NA) in metal homeostasis, through the chelation and transport of NA-metal complexes. The function of transport of NA-metal chelates, required for the loading and unloading of vessels, has been assigned to the Yellow Stripe 1 (YSL)-Like family of proteins. We have characterized three YSL genes in Thlaspi caerulescens in the context of hyper-accumulation. The three YSL genes are expressed at high rates compared with their Arabidopsis thaliana homologs but with distinct patterns. While TcYSL7 was highly expressed in the flowers, TcYSL5 was more highly expressed in the shoots, and the expression of TcYSL3 was equivalent in all the organs tested. In situ hybridizations have shown that TcYSL7 and TcYSL5 are expressed around the vasculature of the shoots and in the central cylinder in the roots. The exposure to heavy metals (Zn, Cd, Ni) does not affect the high and constitutive expression of the TcYSL genes. Finally, we have demonstrated by mutant yeast complementation and uptake measurements that TcYSL3 is an Fe/Ni-NA influx transporter. This work provides therefore molecular, histological and biochemical evidence supporting a role for YSL transporters in the overall scheme of NA and NA-metal, particularly NA-Ni, circulation in a metal hyper-accumulator plant.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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 Gendre et al., 2007
In T. caerulescens three genes viz. TcYSL3, TcYSL5, and YSL7 are over-expressed to mediate vascular loading and transport of Ni and Fe in the form of Nicotinamide-Ni complex and Nicotinamide-Fe complex.
“In T. caerulescens three genes viz. TcYSL3, TcYSL5, and YSL7 are over-expressed to mediate vascular loading and transport of Ni and Fe in the form of Nicotinamide-Ni complex and Nicotainmide-Fe complex (Gendre 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 Gendre et al., 2007
Cites
Baker, A. J. M., & Brooks, R. R. (1989) · Cited by 2,213 · see citing works
Molecular mechanisms of plant metal tolerance and homeostasis
Clemens, S. (2001) · Planta · doi:10.1007/s004250000458 · Cited by 1,417 · see citing works
A long way ahead: understanding and engineering plant metal accumulation
Clemens, S., Palmgren, M. G., & Krämer, U. (2002) · Trends in Plant Science · doi:10.1016/s1360-1385(02)02295-1 · Cited by 1,265 · see citing works
Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake
Curie, C., Panaviene, Z., Loulergue, C., Dellaporta, S. L., Briat, J., & Walker, E. L. (2001) · Nature · doi:10.1038/35053080 · Cited by 1,033 · see citing works
Self-citationFree histidine as a metal chelator in plants that accumulate nickel
Krämer, U., Cotter-Howells, J. D., Charnock, J., Baker, A. J. M., & Smith, J. A. C. (1996) · Nature · doi:10.1038/379635a0 · Cited by 963 · see citing works
Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants
Brooks, R. R., Lee, J., Reeves, R. D., & Jaffré, T. (1977) · Journal of Geochemical Exploration · doi:10.1016/0375-6742(77)90074-7 · Cited by 896 · see citing works
Pence, N. S., Larsen, P. B., Ebbs, S. D., Letham, D. L. D., Lasat, M. M., Garvin, D. F., Eide, D., & Kochian, L. V. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4956 · Cited by 748 · see citing works
Becher, M., Talke, I. N., Krall, L., & Krämer, U. (2004) · The Plant Journal · doi:10.1046/j.1365-313x.2003.01959.x · Cited by 568 · see citing works
Koike, S., Inoue, H., Mizuno, D., Takahashi, M., Nakanishi, H., Mori, S., & Nishizawa, N. K. (2004) · The Plant Journal · doi:10.1111/j.1365-313x.2004.02146.x · Cited by 559 · see citing works
Nicotianamine Chelates Both FeIII and FeII. Implications for Metal Transport in Plants1
Nicolaus Von Wirén, A., Klair, S. S., Bansal, S., Briat, J., Khodr, H., Shioiri, T., Leigh, R. A., & Hider, R. C. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.119.3.1107 · Cited by 476 · see citing works
Self-citationCellular Compartmentation of Zinc in Leaves of the Hyperaccumulator Thlaspi caerulescens1
Küpper, H., Zhao, F. J., & McGrath, S. P. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.119.1.305 · Cited by 444 · see citing works
Weber, M., Harada, E., Vess, C., Roepenack‐Lahaye, E. V., & Clemens, S. (2004) · The Plant Journal · doi:10.1046/j.1365-313x.2003.01960.x · Cited by 440 · see citing works
Higuchi, K., Suzuki, K. Z., Nakanishi, H., Yamaguchi, H., Nishizawa, N., & Mori, S. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.119.2.471 · Cited by 435 · see citing works
Schaaf, G., Ludewig, U., Erenoglu, B. E., Mori, S., Kitahara, T., & von Wirén, N. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m311799200 · Cited by 422 · see citing works
<i>Sebertia acuminata</i> : A Hyperaccumulator of Nickel from New Caledonia
Jaffré, T., Brooks, R. R., Lee, J., & Reeves, R. D. (1976) · Science · doi:10.1126/science.193.4253.579 · Cited by 410 · see citing works
Assunção, A. G. L., Martins, P. D. C., de Folter, S., Vooijs, R., Schat, H., & Aarts, M. G. M. (2001) · Plant Cell & Environment · doi:10.1046/j.1365-3040.2001.00666.x · Cited by 402 · see citing works
Lasat, M. M., Baker, A. J. M., & Kochian, L. V. (1996) · PLANT PHYSIOLOGY · doi:10.1104/pp.112.4.1715 · Cited by 381 · see citing works
Dohmen, R. J., Strasser, A. W. M., Höner, C. B., et al. (1991) · Yeast · doi:10.1002/yea.320070704 · Cited by 375 · see citing works
DiDonato, R. J., Roberts, L. A., Sanderson, T., Eisley, R. B., & Walker, E. L. (2004) · The Plant Journal · doi:10.1111/j.1365-313x.2004.02128.x · Cited by 369 · see citing works
Küpper, H., Lombi, E., Zhao, F. J., Wieshammer, G., & McGrath, S. P. (2001) · Journal of Experimental Botany · doi:10.1093/jexbot/52.365.2291 · Cited by 359 · see citing works
Assunção, A. G. L., Martins, P. D. C., De Folter, S., Vooijs, R., Schat, H., & Aarts, M. G. M. (2001) · Plant, Cell & Environment · doi:10.1111/j.1365-3040.2001.00666.x · Cited by 350 · see citing works
Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens
Lasat, M. M., Pence, N. S., Garvin, D. F., Ebbs, S. D., & Kochian, L. V. (2000) · Journal of Experimental Botany · doi:10.1093/jexbot/51.342.71 · Cited by 344 · see citing works
Dräger, D. B., Desbrosses‐Fonrouge, A., Krach, C., Chardonnens, A. N., Meyer, R. C., Saumitou‐Laprade, P., & Krämer, U. (2004) · The Plant Journal · doi:10.1111/j.1365-313x.2004.02143.x · Cited by 294 · see citing works
THE MOLECULAR BIOLOGY OF METAL ION TRANSPORT INSACCHAROMYCES CEREVISIAE
Eide, D. J. (1998) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.18.1.441 · Cited by 292 · see citing works
A loss‐of‐function mutation in AtYSL1 reveals its role in iron and nicotianamine seed loading
Jean, M. L., Schikora, A., Mari, S., Briat, J., & Curie, C. (2005) · The Plant Journal · doi:10.1111/j.1365-313x.2005.02569.x · Cited by 261 · see citing works
Self-citationRoots of Iron-Efficient Maize also Absorb Phytosiderophore-Chelated Zinc
von Wirén, N., Marschner, H., & Römheld, V. (1996) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.4.1119 · Cited by 251 · see citing works
Nicolaus Von Wirén, A., Mori, S., Marschner, H., & Römheld, V. (1994) · PLANT PHYSIOLOGY · doi:10.1104/pp.106.1.71 · Cited by 248 · see citing works
Plant responses to metal toxicity
Briat, J., & Lebrun, M. (1999) · Comptes Rendus de l Académie des Sciences - Series III - Sciences de la Vie · doi:10.1016/s0764-4469(99)80016-x · Cited by 237 · see citing works
Self-citationNicotianamine: mediator of transport of iron and heavy metals in the phloem?
Stephan, U. W., & Scholz, G. (1993) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1993.tb01367.x · Cited by 213 · see citing works
European species of Thlaspi L.(Cruciferae) as indicators of nickel and zinc
Reeves, R. D., & Brooks, R. R. (1983) · Journal of Geochemical Exploration · doi:10.1016/0375-6742(83)90073-0 · Cited by 207 · see citing works
Nicotianamine: mediator of transport of iron and heavy metals in the phloem?
Stephan, U. W., & Scholz, G. (1993) · Physiologia Plantarum · doi:10.1034/j.1399-3054.1993.880318.x · Cited by 202 · see citing works
Hoof, N. A. L. M. V., Hassinen, V. H., Hakvoort, H. W. J., Ballintijn, K. F., Schat, H., Verkleij, J. A. C., Ernst, W. H. O., Kärenlampi, S. O., & Tervahauta, A. I. (2001) · PLANT PHYSIOLOGY · doi:10.1104/pp.126.4.1519 · Cited by 201 · see citing works
Yellow Stripe1. Expanded Roles for the Maize Iron-Phytosiderophore Transporter
Roberts, L. A., Pierson, A. J., Panaviene, Z., & Walker, E. L. (2004) · PLANT PHYSIOLOGY · doi:10.1104/pp.103.037572 · Cited by 200 · see citing works
Schaaf, G., Schikora, A., Häberle, J., Vert, G., Ludewig, U., Briat, J., Curie, C., & von Wirén, N. (2005) · Plant and Cell Physiology · doi:10.1093/pcp/pci081 · Cited by 195 · see citing works
Self-citationKim, S., Takahashi, M., Higuchi, K., Tsunoda, K., Nakanishi, H., Yoshimura, E., Mori, S., & Nishizawa, N. K. (2005) · Plant and Cell Physiology · doi:10.1093/pcp/pci196 · Cited by 185 · see citing works
Roosens, N. H. C., Bernard, C., Leplae, R., & Verbruggen, N. (2004) · FEBS Letters · doi:10.1016/j.febslet.2004.08.084 · Cited by 162 · see citing works
Vacchina, V., Mari, S., Czernic, P., Marqués, L. P., Pianelli, K., Schaumlöffel, D., Lebrun, M., & Łobiński, R. (2003) · Analytical Chemistry · doi:10.1021/ac020704m · Cited by 150 · see citing works
Self-citationPersans, M. W., Yan, X., Patnoe, J.-M. M. L., Krämer, U., & Salt, D. E. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.121.4.1117 · Cited by 146 · see citing works
Metal complex formation by nicotianamine, a possible phytosiderophore
Beneš, I., Schreiber, K., Ripperger, H., & Kircheiss, A. (1983) · Cellular and Molecular Life Sciences · doi:10.1007/bf01955293 · Cited by 144 · see citing works
The nicotianamine molecule is made-to-measure for complexation of metal micronutrients in plants
Stephan, U. W., Schmidke, I., Stephan, V., & Scholz, G. (1996) · BioMetals · doi:10.1007/bf00188095 · Cited by 136 · see citing works
Felsenstein, J. (1992) · Genetics Research · doi:10.1017/s0016672300030962 · Cited by 135 · see citing works
Douchkov, D., Gryczka, C., Stephan, U. W., Hell, R., & Bäumlein, H. (2004) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2005.01273.x · Cited by 133 · see citing works
Nicotianamine Over-accumulation Confers Resistance to Nickel in Arabidopsis thaliana
Pianelli, K., Mari, S., Marqués, L. P., Lebrun, M., & Czernic, P. (2005) · Transgenic Research · doi:10.1007/s11248-005-7159-3 · Cited by 122 · see citing works
Self-citationNicotianamine ‐ a common constituent of strategies I and II of iron acquisition by plants: A review
Scholz, G., Becker, R., Pich, A., et al. (1992) · Journal of Plant Nutrition · doi:10.1080/01904169209364428 · Cited by 112 · see citing works
Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens
Lasat, M. M., Pence, N. S., Garvin, D. F., et al. (2000) · Journal of Experimental Botany · doi:10.1093/jxb/51.342.71 · Cited by 96 · see citing works
Marqués, L. P., Cossegal, M., Bodin, S., Czernic, P., & Lebrun, M. (2004) · New Phytologist · doi:10.1111/j.1469-8137.2004.01178.x · Cited by 49 · see citing works
Self-citationMetal immobilization: where and how
Mari, S., & Lebrun, M. (2005) · Topics in Current Genetics · doi:10.1007/4735_103 · Cited by 15 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting
Rascio, N., & Navari-Izzo, F. (2011) · Plant Science · doi:10.1016/j.plantsci.2010.08.016 · Cited by 2,012 · see citing works
Metal hyperaccumulation in plants
Krämer, U. (2010) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042809-112156 · Cited by 1,284 · see citing works
Krämer, U., Talke, I. N., & Hanikenne, M. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.04.010 · Cited by 583 · see citing works
Oomen, R. J. F. J., Wu, J., Lelièvre, F., Blanchet, S., Richaud, P., Barbier‐Brygoo, H., Aarts, M. G. M., & Thomine, S. (2009) · New Phytologist · doi:10.1111/j.1469-8137.2008.02694.x · Cited by 270 · see citing works
Physiological and molecular mechanisms of metal accumulation in hyperaccumulator plants
Sytar, O., Ghosh, S., Malinska, H., Zivcak, M., & Brestic, M. (2020) · Physiologia Plantarum · doi:10.1111/ppl.13285 · Cited by 192 · see citing works
Jaffré, T., Pillon, Y., Thomine, S., & Merlot, S. (2013) · Frontiers in Plant Science · doi:10.3389/fpls.2013.00279 · Cited by 146 · see citing works
Recent advances in physiological and molecular mechanisms of heavy metal accumulation in plants
Feki, K., Tounsi, S., Mrabet, M., Mhadhbi, H., & Brini, F. (2021) · Environmental Science and Pollution Research · doi:10.1007/s11356-021-16805-y · Cited by 83 · see citing works
Low-molecular-weight ligands in plants: role in metal homeostasis and hyperaccumulation
Seregin, I. V., & Kozhevnikova, A. D. (2021) · Photosynthesis Research · doi:10.1007/s11120-020-00768-1 · Cited by 73 · see citing works
Schneider, T., Persson, D. P., Husted, S., Schellenberg, M., Gehrig, P., Lee, Y., Martinoia, E., Schjoerring, J. K., & Meyer, S. (2013) · The Plant Journal · doi:10.1111/tpj.12022 · Cited by 71 · see citing works
Bhat, B. A., Rather, M. A., Bilal, T., Nazir, R., Qadir, R. U., & Mir, R. A. (2025) · Frontiers in Plant Science · doi:10.3389/fpls.2025.1631378 · Cited by 68 · see citing works
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 · see citing works
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 · see citing works
Root and shoot response to nickel in hyperaccumulator and non-hyperaccumulator species
Rosatto, S., Mariotti, M., Romeo, S., & Roccotiello, E. (2021) · Plants · doi:10.3390/plants10030508 · Cited by 28 · see citing works
Heavy metal hyperaccumulation and hypertolerance in Brassicaceae
Dar, M. I., Naikoo, M. I., Green, I. D., Sayeed, N., Ali, B., & Khan, F. A. (2018) · Plants Under Metal and Metalloid Stress · doi:10.1007/978-981-13-2242-6_10 · Cited by 17 · see citing works
- Authors
- Gendre, D., Czernic, P., Conéjéro, G., Pianelli, K., Briat, J., Lebrun, M., & Mari, S.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Institut des Sciences des Plantes de Montpellier (FR)
- Corresponding author
- Mari, Stéphane
- ORCID
- Venue
- The Plant Journal
- Publisher
- Wiley
- Published
- 2006-11-28
- Volume
- 49
- Issue
- 1
- Pages
- 1-15
- ISSN
- 0960-7412 (ISSN-L)
- 1365-313X
- OpenAlex
- W2130251381
- Cited by
- 221
- References
- 47
- Citations by year
- 2026: 4 · 2025: 10 · 2024: 12 · 2023: 12 · 2022: 12 · 2021: 14 · 2020: 12 · 2019: 11 · 2018: 11 · 2017: 8 · 2016: 11 · 2015: 6 · 2014: 10 · 2013: 14 · 2012: 15
- FWCI
- 14.32
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Plant Journal (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Micronutrient Interactions and Effects
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Keywords
- Thlaspi caerulescens, hyperaccumulator plants, nicotianamine, metal homeostasis, heavy metal translocation, iron transport, nickel transport, xylem loading, gene expression patterns, yeast complementation
- MeSH terms
- Amino Acid Sequence, Azetidinecarboxylic Acid, Cloning, Molecular, Multigene Family, Iron, Molecular Sequence Data, Nickel, Phylogeny, Plant Proteins, Gene Expression Regulation, Plant, Plant Roots, Plant Stems, Membrane Transport Proteins, Thlaspi
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review