Identification of Thlaspi caerulescens Genes That May Be Involved in Heavy Metal Hyperaccumulation and Tolerance. Characterization of a Novel Heavy Metal Transporting ATPase

Papoyan, Ashot; Kochian, Leon V.

doi:10.1104/pp.104.044503

Cited by 324Heavy metals in environmentHeavy Metals in PlantsHeavy Metal Pollution Remediation

Identification of Thlaspi caerulescens Genes That May Be Involved in Heavy Metal Hyperaccumulation and Tolerance. Characterization of a Novel Heavy Metal Transporting ATPase

Open access

Papoyan, Ashot, Kochian, Leon V.·2004·Plant Physiology

DOI 10.1104/pp.104.044503PMC PMC527178

Open this paper in CoChat — free account Open PDF

Abstract

Thlaspi caerulescens is a heavy metal hyperaccumulator plant species that is able to accumulate extremely high levels of zinc (Zn) and cadmium (Cd) in its shoots (30,000 μg g−1 Zn and 10,000 μg g−1 Cd), and has been the subject of intense research as a model plant to gain a better understanding of the mechanisms of heavy metal hyperaccumulation and tolerance and as a source of genes for developing plant species better suited for the phytoremediation of metal-contaminated soils. In this study, we report on the results of a yeast (Saccharomyces cerevisae) complementation screen aimed at identifying candidate heavy metal tolerance genes in T. caerulescens. A number of Thlaspi genes that conferred Cd tolerance to yeast were identified, including possible metal-binding ligands from the metallothionein gene family, and a P-type ATPase that is a member of the P1B subfamily of purported heavy metal-translocating ATPases. A detailed characterization of the Thlaspi heavy metal ATPase, TcHMA4, demonstrated that it mediates yeast metal tolerance via active efflux of a number of different heavy metals (Cd, Zn, lead [Pb], and copper [Cu]) out of the cell. However, in T. caerulescens, based on differences in tissue-specific and metal-responsive expression of this transporter compared with its homolog in Arabidopsis (Arabidopsis thaliana), we suggest that it may not be involved in metal tolerance. Instead, we hypothesize that it may play a role in xylem loading of metals and thus could be a key player in the hyperaccumulation phenotype expressed in T. caerulescens. Additionally, evidence is presented showing that the C terminus of the TcHMA4 protein, which contains numerous possible heavy metal-binding His and Cys repeats residues, participates in heavy metal binding. When partial peptides from this C-terminal domain were expressed in yeast, they conferred an extremely high level of Cd tolerance and Cd hyperaccumulation. The possibilities for enhancing the metal tolerance and phytoremediation potential of higher plants via expression of these metal-binding peptides are also discussed.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1104/pp.104.044503

Cites

22 of 22 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

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?

RNA interference technique showed that higher expression of AhHMA4 was responsible for hypertolerance to Cd and Zn metal ions in Arabidopsis halleri.
“Further, the RNA interference technique showed that higher expression of AhHMA4 was responsible for hypertolerance to Cd and Zn metal ions in Arabidopsis halleri (Papoyan and Kochian, 2004).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as Papoyan and Kochian, 2004
The Tissue-Specific Expression section reports northern analysis of TcHMA4 in Thlaspi caerulescens, and the metal-tolerance section reports TcHMA4 expression in yeast. Neither passage addresses RNA interference, AhHMA4, or Cd and Zn hypertolerance in Arabidopsis halleri; searches for those terms found no matching result in our copy. No page numbers were available. (LLM, conf=0.76)
Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

P <scp>HYTOCHELATINS AND</scp> M <scp>ETALLOTHIONEINS</scp> : Roles in Heavy Metal Detoxification and Homeostasis
Cobbett, C., & Goldsbrough, P. (2002) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.53.100301.135154 · Cited by 2,518 · see citing works
Methods in Yeast Genetics: A Laboratory Course Manual
Rose, M. D., Winston, F., & Hieter, P. (1990) · Medical Entomology and Zoology · Cited by 1,894 · 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
Evolution of Substrate Specificities in the P-Type ATPase Superfamily
Axelsen, K. B., & Palmgren, M. B. (1998) · Journal of Molecular Evolution · doi:10.1007/pl00006286 · Cited by 910 · 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
The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens
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
Self-citation
P-Type ATPase Heavy Metal Transporters with Roles in Essential Zinc Homeostasis in Arabidopsis
Hussain, D., Haydon, M. J., Wang, Y., Wong, E., Sherson, S. M., Young, J. C., Camakaris, J., Harper, J. F., & Cobbett, C. S. (2004) · The Plant Cell · doi:10.1105/tpc.020487 · Cited by 739 · see citing works
Emerging mechanisms for heavy metal transport in plants
Williams, L. E., Pittman, J. K., & Hall, J. L. (2000) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(00)00133-4 · Cited by 631 · see citing works
Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs
Minét, M., Dufour, M., & Lacroute, F. (1992) · The Plant Journal · doi:10.1111/j.1365-313x.1992.00417.x · Cited by 518 · see citing works
Phytoremediation of metals, metalloids, and radionuclides
McGrath, S. P., Zhao, J., & Lombi, E. (2002) · Advances in Agronomy · doi:10.1016/s0065-2113(02)75002-5 · Cited by 506 · see citing works
CPx-type ATPases: a class of P-type ATPases that pump heavy metals
Solioz, M., & Vulpe, C. D. (1996) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(96)20016-7 · Cited by 478 · see citing works
Inventory of the Superfamily of P-Type Ion Pumps in Arabidopsis
Axelsen, K. B., & Palmgren, M. B. (2001) · PLANT PHYSIOLOGY · doi:10.1104/pp.126.2.696 · Cited by 458 · see citing works
Cellular 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
The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase
Rensing, C., Mitra, B., & Rosen, B. P. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.26.14326 · Cited by 419 · see citing works
Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense
Lombi, E., Zhao, F. J., Dunham, S. J., & McGrath, S. P. (2000) · New Phytologist · doi:10.1046/j.1469-8137.2000.00560.x · Cited by 384 · see citing works
Physiological Characterization of Root Zn2+ Absorption and Translocation to Shoots in Zn Hyperaccumulator and Nonaccumulator Species of Thlaspi
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
Self-citation
Zinc and Cadmium Uptake by Hyperaccumulator Thlaspi caerulescens Grown in Nutrient Solution
Brown, S. L., Chaney, R. L., Angle, J. S., & Baker, A. J. M. (1995) · Soil Science Society of America Journal · doi:10.2136/sssaj1995.03615995005900010020x · Cited by 380 · see citing works
Altered Zn Compartmentation in the Root Symplasm and Stimulated Zn Absorption into the Leaf as Mechanisms Involved in Zn Hyperaccumulation in Thlaspi caerulescens
Lasat, M. M., Baker, A. J. M., & Kochian, L. V. (1998) · PLANT PHYSIOLOGY · doi:10.1104/pp.118.3.875 · Cited by 306 · see citing works
Self-citation
Functional expression of AtHMA4, a P1B‐type ATPase of the Zn/Co/Cd/Pb subclass
Mills, R. F., Krijger, G. C., Baccarini, P. J., Hall, J. L., & Williams, L. E. (2003) · The Plant Journal · doi:10.1046/j.1365-313x.2003.01790.x · Cited by 241 · see citing works
Functional Expression of a Bacterial Heavy Metal Transporter in Arabidopsis Enhances Resistance to and Decreases Uptake of Heavy Metals
Lee, J., Bae, H., Jeong, J., Lee, J., Yang, Y., Hwang, I., Martinoia, E., & Lee, Y. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp.103.021972 · Cited by 145 · see citing works
TOTAL ORGANIC SULFUR AND HUMUS SULFUR OF MINNESOTA SOILS
EVANS, C. A., & Rost, C. O. (1945) · Soil Science · doi:10.1097/00010694-194502000-00003 · Cited by 51 · see citing works
A Novel Histidine-Rich CPx-ATPase from the Filamentous Cyanobacterium Oscillatoria brevis Related to Multiple-Heavy-Metal Cotolerance
Tong, L., Nakashima, S., Shibasaka, M., Katsuhara, M., & Kasamo, K. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.18.5027-5035.2002 · Cited by 41 · see citing works

Flagged first, then by citations

1 of the 23 references couldn’t be matched to a known paper.

Research works printed but not linked: 4

Plant Physiology, November 2004, Vol.136, pp.3814-3823, www.plantphysiol.orgÓ 2004 American Society of Plant Biologists
Downloaded from https://academic.oup.com/plphys/article/136/3/3814/6112497 by guest on 16 August 2023
Plant Physiol.Vol.136, 2004 Downloaded from https://academic.oup.com/plphys/article/136/3/3814/6112497 by guest on 16 August 2023
Plant Physiol.Vol.136, 2004

Sorted by citations

Biofortification of crops with seven mineral elements often lacking in human diets – iron, zinc, copper, calcium, magnesium, selenium and iodine
White, P. J., & Broadley, M. R. (2009) · New Phytologist · doi:10.1111/j.1469-8137.2008.02738.x · Cited by 2,178 · see citing works
Zinc in plants
Broadley, M. R., White, P. J., Hammond, J. P., Zelko, I., & Lux, A. (2007) · New Phytologist · doi:10.1111/j.1469-8137.2007.01996.x · Cited by 2,112 · see citing works
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
Heavy Metal Tolerance in Plants: Role of Transcriptomics, Proteomics, Metabolomics, and Ionomics
Singh, S., Parihar, P., Singh, R., Singh, V. P., & Prasad, S. M. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2015.01143 · Cited by 1,322 · 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
Zinc in Soils and Crop Nutrition
Sadeghzadeh, B., & Rengel, Z. (2011) · Wiley eBooks · doi:10.1002/9780470960707.ch16 · Cited by 1,251 · see citing works
Molecular mechanisms of metal hyperaccumulation in plants
Verbruggen, N., Hermans, C., & Schat, H. (2009) · New Phytologist · doi:10.1111/j.1469-8137.2008.02748.x · Cited by 1,071 · see citing works
The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance
Kim, D., Bovet, L., Maeshima, M., Martinoia, E., & Lee, Y. (2007) · The Plant Journal · doi:10.1111/j.1365-313x.2007.03044.x · Cited by 721 · see citing works
Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice
Uraguchi, S., Mori, S., Kuramata, M., Kawasaki, A., Arao, T., & Ishikawa, S. (2009) · Journal of Experimental Botany · doi:10.1093/jxb/erp119 · Cited by 666 · see citing works
Transition metal transport
Krämer, U., Talke, I. N., & Hanikenne, M. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.04.010 · Cited by 583 · see citing works
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, 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. (2006) · Plant Physiology · doi:10.1104/pp.106.082073 · Cited by 547 · see citing works
Zinc biofortification of cereals: problems and solutions
Palmgren, M. B., Clemens, S., Williams, L. E., Krämer, U., Borg, S., Schjoerring, J. K., & Sanders, D. (2008) · Trends in Plant Science · doi:10.1016/j.tplants.2008.06.005 · Cited by 547 · see citing works
Metal tolerance and hyperaccumulation: Costs and trade-offs between traits and environment
Maestri, E., Marmiroli, M., Visioli, G., & Marmiroli, N. (2009) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2009.10.011 · Cited by 539 · see citing works
How Plants Cope with Cadmium: Staking All on Metabolism and Gene Expression
DalCorso, G., Farinati, S., Maistri, S., & Furini, A. (2008) · Journal of Integrative Plant Biology · doi:10.1111/j.1744-7909.2008.00737.x · Cited by 537 · see citing works
Cadmium Toxicity in Plants and Role of Mineral Nutrients in Its Alleviation
Nazar, R., Iqbal, N., Masood, A., Khan, M. I. R., Syeed, S., & Khan, N. A. (2012) · American Journal of Plant Sciences · doi:10.4236/ajps.2012.310178 · Cited by 524 · see citing works
Low-affinity cation transporter ( OsLCT1 ) regulates cadmium transport into rice grains
Uraguchi, S., Kamiya, T., Sakamoto, T., Kasai, K., Sato, Y., Nagamura, Y., Yoshida, A., Kyozuka, J., Ishikawa, S., & Fujiwara, T. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1116531109 · Cited by 516 · see citing works
Phytoremediation: novel approaches to cleaning up polluted soils
Krämer, U. (2005) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2005.02.006 · Cited by 501 · see citing works
Zinc-Dependent Global Transcriptional Control, Transcriptional Deregulation, and Higher Gene Copy Number for Genes in Metal Homeostasis of the Hyperaccumulator Arabidopsis halleri
Talke, I. N., Hanikenne, M., & Krämer, U. (2006) · Plant Physiology · doi:10.1104/pp.105.076232 · Cited by 452 · see citing works
A Review of Environmental Contamination and Health Risk Assessment of Wastewater Use for Crop Irrigation with a Focus on Low and High-Income Countries
Khalid, S., Shahid, M. A. R., Natasha, N., Bibi, I., Sarwar, T., Shah, A. H., & Niazi, N. K. (2018) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph15050895 · Cited by 451 · see citing works
Preferential Delivery of Zinc to Developing Tissues in Rice Is Mediated by P-Type Heavy Metal ATPase OsHMA2
Yamaji, N., Xia, J., Mitani‐Ueno, N., Yokosho, K., & Feng, J. X. (2013) · PLANT PHYSIOLOGY · doi:10.1104/pp.113.216564 · Cited by 441 · see citing works
P1B-ATPases – an ancient family of transition metal pumps with diverse functions in plants
Williams, L. E., & Mills, R. F. (2005) · Trends in Plant Science · doi:10.1016/j.tplants.2005.08.008 · Cited by 437 · see citing works
How plants cope with heavy metals
Viehweger, K. (2014) · Botanical studies · doi:10.1186/1999-3110-55-35 · Cited by 434 · see citing works
Trace metal metabolism in plants
Andresen, E., Peiter, E., & Küpper, H. (2018) · Journal of Experimental Botany · doi:10.1093/jxb/erx465 · Cited by 431 · see citing works
Put the metal to the petal: metal uptake and transport throughout plants
Colangelo, E. P., & Guerinot, M. L. (2006) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2006.03.015 · Cited by 429 · see citing works
Implications of metal accumulation mechanisms to phytoremediation
Memon, A. R., & Schröder, P. (2008) · Environmental Science and Pollution Research · doi:10.1007/s11356-008-0079-z · Cited by 399 · see citing works
OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice
Liu, X. S., Feng, S. J., Zhang, B. Q., Wang, M. Q., Cao, H. W., Rono, J. K., Chen, X., & Yang, Z. M. (2019) · BMC Plant Biology · doi:10.1186/s12870-019-1899-3 · Cited by 351 · see citing works
Role of Hyperaccumulators in Phytoextraction of Metals From Contaminated Mining Sites: A Review
Sheoran, V., Sheoran, A. S., & Poonia, P. (2010) · Critical Reviews in Environmental Science and Technology · doi:10.1080/10643380902718418 · Cited by 350 · see citing works
Comparative physiology of elemental distributions in plants
Conn, S., & Gilliham, M. (2010) · Annals of Botany · doi:10.1093/aob/mcq027 · Cited by 344 · see citing works
Mechanisms of Cadmium Accumulation in Plants
Sterckeman, T., & Thomine, S. (2020) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2020.1792179 · Cited by 343 · see citing works
The Arabidopsis heavy metal P‐type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots
Andrés‐Colás, N., Sancenón, V., Rodríguez‐Navarro, S., Mayo, S., Thiele, D. J., Ecker, J. R., Puig, S., & Peñarrubia, L. (2005) · The Plant Journal · doi:10.1111/j.1365-313x.2005.02601.x · Cited by 342 · see citing works
Role of phosphate fertilizers in heavy metal uptake and detoxification of toxic metals
Gupta, D. K., Chatterjee, S., Datta, S., Veer, V., & Walther, C. (2014) · Chemosphere · doi:10.1016/j.chemosphere.2014.01.030 · Cited by 339 · see citing works
Investigating Heavy-metal Hyperaccumulation using Thlaspi caerulescens as a Model System
Milner, M. J., & Kochian, L. V. (2008) · Annals of Botany · doi:10.1093/aob/mcn063 · Cited by 328 · see citing works
Self-citation
Cadmium‐induced inhibition of photosynthesis and long‐term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens
Küpper, H., Aravind, P., Leitenmaier, B., Trtílek, M., & Šetlík, I. (2007) · New Phytologist · doi:10.1111/j.1469-8137.2007.02139.x · Cited by 321 · see citing works
Phytoremediation of Heavy Metals: Physiological and Molecular Mechanisms
Jabeen, R., Ahmad, A., & Iqbal, M. M. (2009) · The Botanical Review · doi:10.1007/s12229-009-9036-x · Cited by 305 · see citing works
A Major Quantitative Trait Locus for Cadmium Tolerance in Arabidopsis halleri Colocalizes with HMA4, a Gene Encoding a Heavy Metal ATPase
Courbot, M., Willems, G., Motte, P., Arvidsson, S., Roosens, N., Saumitou-Laprade, P., & Verbruggen, N. (2007) · Plant Physiology · doi:10.1104/pp.106.095133 · Cited by 303 · see citing works
Moving micronutrients from the soil to the seeds: Genes and physiological processes from a biofortification perspective
Waters, B. M., & Sankaran, R. P. (2010) · Plant Science · doi:10.1016/j.plantsci.2010.12.003 · Cited by 301 · see citing works
Cadmium minimization in rice. A review
Sebastian, A., & Prasad, M. N. V. (2013) · Agronomy for Sustainable Development · doi:10.1007/s13593-013-0152-y · Cited by 279 · see citing works
Compartmentation and complexation of metals in hyperaccumulator plants
Leitenmaier, B., & Küpper, H. (2013) · Frontiers in Plant Science · doi:10.3389/fpls.2013.00374 · Cited by 275 · see citing works
Phytoremediation: role of terrestrial plants and aquatic macrophytes in the remediation of radionuclides and heavy metal contaminated soil and water
Sharma, S., Singh, B., & Manchanda, V. K. (2014) · Environmental Science and Pollution Research · doi:10.1007/s11356-014-3635-8 · Cited by 274 · see citing works
Genetically modified plants in phytoremediation of heavy metal and metalloid soil and sediment pollution
Kotrba, P., Najmanová, J., Macek, T., Ruml, T., & Macková, M. (2009) · Biotechnology Advances · doi:10.1016/j.biotechadv.2009.06.003 · Cited by 273 · see citing works
Can metals defend plants against biotic stress?
Poschenrieder, C., Tolrà, R. P., & Barceló, J. A. (2006) · Trends in Plant Science · doi:10.1016/j.tplants.2006.04.007 · Cited by 265 · see citing works
Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd‐hyperaccumulating ecotype of Thlaspi caerulescens
Ueno, D., Milner, M. J., Yamaji, N., Yokosho, K., Koyama, E., Clemencia Zambrano, M., Kaskie, M., Ebbs, S., Kochian, L. V., & Ma, J. F. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04548.x · Cited by 243 · see citing works
Self-citation
Phytoremediation: green technology for the clean up of toxic metals in the environment
Gratão, P. L., Prasad, M. N. V., Cardoso, P. F., Lea, P. J., & Azevedo, R. A. (2005) · Brazilian Journal of Plant Physiology · doi:10.1590/s1677-04202005000100005 · Cited by 242 · see citing works
A Novel Major Facilitator Superfamily Protein at the Tonoplast Influences Zinc Tolerance and Accumulation in Arabidopsis
Haydon, M. J., & Cobbett, C. S. (2007) · PLANT PHYSIOLOGY · doi:10.1104/pp.106.092015 · Cited by 242 · see citing works
Copper accumulation in vineyard soils: Rhizosphere processes and agronomic practices to limit its toxicity
Brunetto, G., de Melo, G. W. B., Terzano, R., Buono, D. D., Astolfi, S., Tomasi, N., Pii, Y., Mimmo, T., & Cesco, S. (2016) · Chemosphere · doi:10.1016/j.chemosphere.2016.07.104 · Cited by 226 · see citing works
A Novel Arsenate Reductase from the Arsenic Hyperaccumulating Fern Pteris vittata
Ellis, D. R., Gumaelius, L., Indriolo, E., Pickering, I. J., Banks, J. A., & Salt, D. E. (2006) · PLANT PHYSIOLOGY · doi:10.1104/pp.106.084079 · Cited by 225 · see citing works
A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes
Hammond, J. P., Bowen, H. C., White, P. J., Mills, V., Pyke, K. A., Baker, A. J. M., Whiting, S. N., May, S. T., & Broadley, M. R. (2006) · New Phytologist · doi:10.1111/j.1469-8137.2006.01662.x · Cited by 223 · see citing works
Metal hyperaccumulation and bioremediation
Shah, K., & Nongkynrih, J. M. (2007) · Biologia Plantarum · doi:10.1007/s10535-007-0134-5 · Cited by 223 · see citing works
A Member of the Heavy Metal P-Type ATPase OsHMA5 Is Involved in Xylem Loading of Copper in Rice
Deng, F., Yamaji, N., Xia, J., & Feng, J. X. (2013) · PLANT PHYSIOLOGY · doi:10.1104/pp.113.226225 · Cited by 220 · see citing works
Seasonal fluctuations of selenium and sulfur accumulation in selenium hyperaccumulators and related nonaccumulators
Galeas, M. L., Zhang, L. H., Freeman, J. L., Wegner, M., & Pilon‐Smits, E. A. H. (2007) · New Phytologist · doi:10.1111/j.1469-8137.2006.01943.x · Cited by 217 · see citing works
Metallophytes—a view from the rhizosphere
Alford, É. R., Pilon‐Smits, E. A. H., & Paschke, M. W. (2010) · Plant and Soil · doi:10.1007/s11104-010-0482-3 · Cited by 217 · see citing works
Effects of zinc toxicity on sugar beet (Beta vulgaris L.) plants grown in hydroponics
Sagardoy, R., Morales, F., López‐Millán, A. F., Abadı́a, A., & Abadı́a, J. (2008) · Plant Biology · doi:10.1111/j.1438-8677.2008.00153.x · Cited by 214 · see citing works
Phytoextraction of heavy metals from contaminated soil, water and atmosphere using ornamental plants: mechanisms and efficiency improvement strategies
Lajayer, B. A., Moghadam, N. K., Maghsoodi, M. R., Ghorbanpour, M., & Kariman, K. (2019) · Environmental Science and Pollution Research · doi:10.1007/s11356-019-04241-y · Cited by 213 · see citing works
Enhanced root-to-shoot translocation of cadmium in the hyperaccumulating ecotype of Sedum alfredii
Lu, L., Tian, S., Yang, X. E., Wang, X., Brown, P. H., Li, T., & He, Z. (2008) · Journal of Experimental Botany · doi:10.1093/jxb/ern174 · Cited by 209 · see citing works
Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics
Hanikenne, M., & Nouet, C. (2011) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2011.04.003 · Cited by 206 · see citing works
Soil Biogeochemistry, Plant Physiology, and Phytoremediation of Cadmium-Contaminated Soils
He, S., He, Z. L., Yang, X., Stoffella, P. J., & Baligar, V. C. (2015) · Advances in agronomy · doi:10.1016/bs.agron.2015.06.005 · Cited by 193 · 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
Transcriptional regulation of metal transport genes and mineral nutrition during acclimatization to cadmium and zinc in the Cd/Zn hyperaccumulator, Thlaspi caerulescens (Ganges population)
Küpper, H., & Kochian, L. V. (2010) · New Phytologist · doi:10.1111/j.1469-8137.2009.03051.x · Cited by 191 · see citing works
Self-citation
Enhancing tonoplast Cd/H antiport activity increases Cd, Zn, and Mn tolerance, and impacts root/shoot Cd partitioning in Nicotiana tabacum L.
Korenkov, V. D., Hirschi, K. D., Crutchfield, J. D., & Wagner, G. J. (2007) · Planta · doi:10.1007/s00425-007-0577-0 · Cited by 189 · see citing works
Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants
Hassan, Z., & Aarts, M. G. M. (2010) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2010.04.003 · Cited by 184 · see citing works
Genes Associated with Heavy Metal Tolerance and Accumulation in Zn/Cd Hyperaccumulator Arabidopsis halleri: A Genomic Survey with cDNA Microarray
Chiang, H.-C., Lo, J.-C., & Yeh, K.-C. (2006) · Environmental Science & Technology · doi:10.1021/es061432y · Cited by 182 · see citing works
The Genetic Basis of Zinc Tolerance in the Metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): An Analysis of Quantitative Trait Loci
Willems, G., Dräger, D. B., Courbot, M., Godé, C., Verbruggen, N., & Saumitou-Laprade, P. (2007) · Genetics · doi:10.1534/genetics.106.064485 · Cited by 182 · see citing works
Characterization of Cd Translocation and Identification of the Cd Form in Xylem Sap of the Cd-Hyperaccumulator Arabidopsis halleri
Ueno, D., Iwashita, T., Zhao, F. J., & Ma, J. F. (2008) · Plant and Cell Physiology · doi:10.1093/pcp/pcn026 · Cited by 177 · see citing works
Mechanisms of cadmium phytoremediation and detoxification in plants
Luo, J., & Zhang, Z. (2021) · The Crop Journal · doi:10.1016/j.cj.2021.02.001 · Cited by 175 · see citing works
Remediation of heavy metal contaminated ecosystem: an overview on technology advancement
Singh, A., & Prasad, S. M. (2014) · International Journal of Environmental Science and Technology · doi:10.1007/s13762-014-0542-y · Cited by 170 · see citing works
Evaluation of phytoextracting cadmium and lead by sunflower, ricinus, alfalfa and mustard in hydroponic culture
Zhi-xin, N. I. U., Sun, L., Sun, T., Li, Y., & Wang, H. (2007) · Journal of Environmental Sciences · doi:10.1016/s1001-0742(07)60158-2 · Cited by 165 · see citing works
The role of ectomycorrhizas in heavy metal stress tolerance of host plants
Luo, Z., Wu, C., Zhang, C., Li, H., Lipka, U., & Polle, A. (2013) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2013.10.018 · Cited by 161 · see citing works
Advances in Genes-Encoding Transporters for Cadmium Uptake, Translocation, and Accumulation in Plants
Tao, J., & Lu, L. (2022) · Toxics · doi:10.3390/toxics10080411 · Cited by 161 · see citing works
A major quantitative trait locus for increasing cadmium-specific concentration in rice grain is located on the short arm of chromosome 7
Ishikawa, S., Abe, T., Kuramata, M., Yamaguchi, M., Ando, T., Yamamoto, T., & Yano, M. (2009) · Journal of Experimental Botany · doi:10.1093/jxb/erp360 · Cited by 154 · see citing works
Genetic engineering strategies for enhancing phytoremediation of heavy metals
Fulekar, M. H., Singh, A., & Bhaduri, A. M. (2009) · AFRICAN JOURNAL OF BIOTECHNOLOGY · doi:10.5897/ajb2009.000-9090 · Cited by 153 · see citing works
Comparative transcriptome combined with morpho‐physiological analyses revealed key factors for differential cadmium accumulation in two contrasting sweet sorghum genotypes
Feng, J., Jia, W., Lv, S., Bao, H., Miao, F., Zhang, X., Wang, J., Li, J., Li, D., Zhu, C., et al. (2017) · Plant Biotechnology Journal · doi:10.1111/pbi.12795 · Cited by 153 · see citing works
Functions and homeostasis of zinc, copper, and nickel in plants
Krämer, U., & Clemens, S. (2005) · Topics in current genetics · doi:10.1007/4735_96 · Cited by 152 · see citing works
Zinc Homeostasis and isotopic fractionation in plants: a review
Caldelas, C., & Weiss, D. J. (2016) · Plant and Soil · doi:10.1007/s11104-016-3146-0 · Cited by 152 · see citing works
Does salicylic acid regulate antioxidant defense system, cell death, cadmium uptake and partitioning to acquire cadmium tolerance in rice?
Guo, B., Liang, Y., & Zhu, Y. (2008) · Journal of Plant Physiology · doi:10.1016/j.jplph.2008.01.002 · Cited by 151 · see citing works
Natural Molecular Mechanisms of Plant Hyperaccumulation and Hypertolerance towards Heavy Metals
Skuza, L., Szućko-Kociuba, I., Filip, E., & Bożek, I. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23169335 · Cited by 148 · see citing works
An Improved Grafting Technique for Mature Arabidopsis Plants Demonstrates Long-Distance Shoot-to-Root Transport of Phytochelatins in Arabidopsis
Chen, A. P., Komives, E. A., & Schroeder, J. I. (2006) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.072637 · Cited by 146 · see citing works
Progress in the genetic understanding of plant iron and zinc nutrition
Ghandilyan, A., Vreugdenhil, D., & Aarts, M. G. M. (2006) · Physiologia Plantarum · doi:10.1111/j.1399-3054.2006.00646.x · Cited by 144 · see citing works
Cadmium uptake and xylem loading are active processes in the hyperaccumulator Sedum alfredii
Lu, L., Tian, S., Yang, X., Li, T., & He, Z. L. (2008) · Journal of Plant Physiology · doi:10.1016/j.jplph.2008.09.001 · Cited by 143 · see citing works
Physiological, genetic, and molecular characterization of a high-Cd-accumulating rice cultivar, Jarjan
Ueno, D., Koyama, E., Yamaji, N., & Feng, J. X. (2010) · Journal of Experimental Botany · doi:10.1093/jxb/erq383 · Cited by 139 · see citing works
Amino Acid Polymorphisms in Strictly Conserved Domains of a P-Type ATPase HMA5 Are Involved in the Mechanism of Copper Tolerance Variation in Arabidopsis
Kobayashi, Y., Kuroda, K., Kimura, K., Southron, J. L., Furuzawa, A., Kimura, K., Iuchi, S., Kobayashi, M., Taylor, G. J., & Koyama, H. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.119933 · Cited by 137 · see citing works
Zinc biofortification in rice: leveraging agriculture to moderate hidden hunger in developing countries
Zaman, Q. U., Aslam, Z., Yaseen, M., Ihsan, M. Z., Khaliq, A., Fahad, S., Bashir, S., Ramzani, P. M. A., & Naeem, M. S. (2017) · Archives of Agronomy and Soil Science · doi:10.1080/03650340.2017.1338343 · Cited by 129 · see citing works
Tandem Quadruplication of HMA4 in the Zinc (Zn) and Cadmium (Cd) Hyperaccumulator Noccaea caerulescens
Lochlainn, S. Ó., Bowen, H. C., Fray, R. G., Hammond, J. P., King, G. J. W., White, P. J., Graham, N. S., & Broadley, M. R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017814 · Cited by 128 · see citing works
Abscisic acid enhances lead translocation from the roots to the leaves and alleviates its toxicity in Populus × canescens
Shi, W., Liu, W., Yu, W., Zhang, Y., Ding, S., Li, H., Mrak, T., Kraigher, H., & Luo, Z. (2018) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2018.09.024 · Cited by 126 · see citing works
Functional analyses of T a HMA 2, a P 1B‐type ATP ase in wheat
Tan, J., Wang, J., Chai, T., Zhang, Y., Feng, S., Li, Y., Zhao, H., Liu, H., & Chai, X. (2013) · Plant Biotechnology Journal · doi:10.1111/pbi.12027 · Cited by 124 · see citing works
Phytoremediation using genetically engineered plants to remove metals: a review
Özyiğit, İ. İ., Can, H., & Doğan, İ. (2020) · Environmental Chemistry Letters · doi:10.1007/s10311-020-01095-6 · Cited by 124 · see citing works
Heavy metal transport by AtHMA4 involves the N‐terminal degenerated metal binding domain and the C‐terminal His11 stretch
Verret, F., Gravot, A., Auroy, P., Prévéral, S., Forestier, C., Vavasseur, A., & Richaud, P. (2005) · FEBS Letters · doi:10.1016/j.febslet.2005.01.065 · Cited by 124 · see citing works
Variation in HMA4 gene copy number and expression among Noccaea caerulescens populations presenting different levels of Cd tolerance and accumulation
Craciun, A. R., Meyer, C.-L., Chen, J., Roosens, N. H. C., Groodt, R. D., Hilson, P., & Verbruggen, N. (2012) · Journal of Experimental Botany · doi:10.1093/jxb/ers104 · Cited by 122 · see citing works
Characteristics of cadmium accumulation and tolerance in novel Cd-accumulating crops, Avena strigosa and Crotalaria juncea
Uraguchi, S., Watanabe, I., Yoshitomi, A., Kiyono, M., & Kuno, K. (2006) · Journal of Experimental Botany · doi:10.1093/jxb/erl056 · Cited by 122 · see citing works
Comparison of three types of oil crop rotation systems for effective use and remediation of heavy metal contaminated agricultural soil
Yang, Y., Zhou, X., Tie, B., Peng, L., Li, H., Wang, K., & Zeng, Q. (2017) · Chemosphere · doi:10.1016/j.chemosphere.2017.08.140 · Cited by 120 · see citing works
Identification of a Novel Major Quantitative Trait Locus Controlling Distribution of Cd Between Roots and Shoots in Rice
Ueno, D., Koyama, E., Kono, I., Ando, T., Yano, M., & Feng, J. X. (2009) · Plant and Cell Physiology · doi:10.1093/pcp/pcp160 · Cited by 117 · see citing works
Coping With Metal Toxicity – Cues From Halophytes
Nikalje, G. C., & Suprasanna, P. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.00777 · Cited by 110 · see citing works
Sulfur in Plants An Ecological Perspective
Hawkesford, M. J., & Kok, L. J. D. (2007) · Plant ecophysiology · doi:10.1007/978-1-4020-5887-5 · Cited by 108 · see citing works
A Critical Review of the Arsenic Uptake Mechanisms and Phytoremediation Potential ofPteris vittata
Danh, L. T., Truong, P. N. V., Mammucari, R., & Foster, N. R. (2013) · International Journal of Phytoremediation · doi:10.1080/15226514.2013.798613 · Cited by 107 · see citing works
Cd-induced changes in leaf proteome of the hyperaccumulator plant Phytolacca americana
Zhao, L., Sun, Y.-L., Cui, S., Chen, M., Yang, H., Liu, H., Chai, T., & Huang, F. (2011) · Chemosphere · doi:10.1016/j.chemosphere.2011.06.029 · Cited by 107 · see citing works
Plant Cd2+ and Zn2+ status effects on root and shoot heavy metal accumulation in Thlaspi caerulescens
Papoyan, A., Piñeros, M., & Kochian, L. V. (2007) · New Phytologist · doi:10.1111/j.1469-8137.2007.02073.x · Cited by 104 · see citing works
Self-citation
Phytoextraction of Cd-Contaminated Soils: Current Status and Future Challenges
Li, J., Baker, A. J. M., Ye, Z., Wang, H., & Shu, W. (2012) · Critical Reviews in Environmental Science and Technology · doi:10.1080/10643389.2011.574105 · Cited by 104 · see citing works
Reduction of heavy metal load in food chain: technology assessment
Singh, A., & Prasad, S. M. (2011) · Reviews in Environmental Science and Bio/Technology · doi:10.1007/s11157-011-9241-z · Cited by 102 · see citing works
Phytotoxicity of mercury in Indian mustard (Brassica juncea L.)
Shiyab, S., Chen, J., Han, F. X., Monts, D. L., Matta, F. B., Gu, M., & Su, Y. (2009) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2008.06.002 · Cited by 99 · see citing works
Multiomics and biotechnologies for understanding and influencing cadmium accumulation and stress response in plants
Yan, Y., Alseekh, S., Zhu, Z., Zhou, K., & Fernie, A. R. (2024) · Plant Biotechnology Journal · doi:10.1111/pbi.14379 · Cited by 99 · see citing works
Xylem loading process is a critical factor in determining Cd accumulation in the shoots of Solanum melongena and Solanum torvum
Mori, S., Uraguchi, S., Ishikawa, S., & Arao, T. (2009) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2009.05.006 · Cited by 99 · see citing works

PHYSIOLOGICAL AND MOLECULAR MECHANISMS OF HEAVY METAL TOLERANCE AND TRANSPORT IN THE HYPERACCUMULATOR PLANT SPECIES, THLASPI CAERULESCENS
Papoyan, A. (2006) · eCommons (Cornell University) · Cited by 1 · see citing works
Self-citation
A novel CPx‐ATPase from the cadmium hyperaccumulator Thlaspi caerulescens
Bernard, C., Roosens, N., Czernic, P., Lebrun, M., & Verbruggen, N. (2004) · FEBS Letters · doi:10.1016/j.febslet.2004.05.036 · Cited by 248 · see citing works
Mechanisms of Zinc Tolerance in the Heavy Metal Hyperaccumulator Thlaspi caerulescens
Klein, M. A. (2006) · eCommons (Cornell University) · Cited by 1 · see citing works
Investigating Heavy-metal Hyperaccumulation using Thlaspi caerulescens as a Model System
Milner, M. J., & Kochian, L. V. (2008) · Annals of Botany · doi:10.1093/aob/mcn063 · Cited by 328 · see citing works
Self-citation
Heavy metal tolerance and accumulation in Thlaspi caerulescens, a heavy metal hyperaccumulating plant species = Zware metalen tolerantie en accumulatie in Thlaspi caerulescens, een zware metalen hyperaccumulerende plantensoort
van de Mortel, J. E. (2007) · doi:10.18174/19687

Authors: Papoyan, A., & Kochian, L. V.
Affiliations: Agricultural Research Service (US)
ORCID: Kochian, Leon V.
Venue: Plant Physiology
Publisher: Oxford University Press (OUP)
Published: 2004-11-01
Volume: 136
Issue: 3
Pages: 3814-3823
ISSN: 0032-0889 (ISSN-L)
1532-2548
DOI: 10.1104/pp.104.044503
PMC: PMC527178
OpenAlex: W2123745023
Semantic Scholar: 8e938def94c5ef68f22244b1eeb0db7b43e78bb9
Cited by: 322
References: 23
Citations by year: 2026: 2 · 2025: 7 · 2024: 9 · 2023: 9 · 2022: 13 · 2021: 14 · 2020: 12 · 2019: 8 · 2018: 12 · 2017: 16 · 2016: 15 · 2015: 12 · 2014: 15 · 2013: 22 · 2012: 16
FWCI: 15.97
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)
Funders: National Science Foundation (0129844)
U.S. Department of Agriculture
Topics: Physical Sciences › Environmental Science › Pollution › Heavy metals in environment
Physical Sciences › Chemistry › Analytical Chemistry › Heavy Metals in Plants
Physical Sciences › Environmental Science › Water Science and Technology › Heavy Metal Pollution Remediation
Keywords: Thlaspi caerulescens, heavy metal hyperaccumulation, cadmium tolerance, zinc accumulation, P-type ATPase, metal efflux, metallothionein, metal-binding peptides, xylem loading, phytoremediation, metal tolerance genes
MeSH terms: Adenosine Triphosphatases, Amino Acid Sequence, Molecular Sequence Data, Saccharomyces cerevisiae, Gene Expression, Sequence Alignment, Genes, Plant, Sequence Homology, Amino Acid, Metals, Heavy, Organisms, Genetically Modified, 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

Identification of Thlaspi caerulescens Genes That May Be Involved in Heavy Metal Hyperaccumulation and Tolerance. Characterization of a Novel Heavy Metal Transporting ATPase

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks