Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe

Thlaspi caerulescens J. & C. Presl is a distinctive metallophyte of central and western Europe that almost invariably hyperaccumulates Zn to > 1.0% of shoot dry biomass in its natural habitats, and can hyperaccumulate Ni to > 0.1% when growing on serpentine soils. Populations from the Ganges region of southern France also have a remarkable ability to accumulate Cd in their shoots to concentrations well in excess of 0.01% without apparent toxicity symptoms. Because hyperaccumulation of Cd appears to be highly variable in this species, the relationship between Cd tolerance and metal accumulation was investigated for seven contrasting populations of T. caerulescens grown under controlled conditions in solution culture. The populations varied considerably in average plant biomass (3.1fold), shoot : root ratio (2.2-fold), Cd hyperaccumulation (3.5-fold), shoot : root Cd-concentration ratio (3.1-fold), and shoot Cd : Zn ratio (2.6-fold), but the degree of hyperaccumulation of Cd and Zn were strongly correlated. Two populations from the Ganges region were distinct in exhibiting high degrees of both Cd tolerance and hyperaccumulation (one requiring 3 m M Cd for optimal growth), whereas across the other five populations there was an inverse relationship between Cd tolerance and hyperaccumulation, as has been noted previously for Zn. Metal hyperaccumulation was negatively correlated with shoot : root ratio, which could account quantitatively for the differences between populations in shoot Zn (but not Cd) concentrations. On exposure to 30 m m M Cd, the two Ganges populations showed marked reductions in shoot Zn and Fe concentrations, although Cd accumulation was not inhibited by elevated Zn; in the other five populations, 30 m M Cd had little or no effect on Zn or Fe accumulation but markedly reduced shoot Ca concentration. These results support a proposal that Cd is taken up predominantly via a high-affinity uptake system for Fe in the Ganges populations, but via a loweraffinity pathway for Ca in other populations. Total shoot Cd accumulated per plant was much more closely related to population Cd tolerance than Cd hyperaccumulation, indicating that metal tolerance may be the more important selection criterion in developing lines with greatest phytoremediation potential.

[1]  D. R. Hoagland,et al.  The Water-Culture Method for Growing Plants Without Soil , 2018 .

[2]  Mark Tester,et al.  Nonselective cation channels in plants. , 2003, Annual review of plant biology.

[3]  Edward J Calabrese,et al.  Toxicology rethinks its central belief , 2003, Nature.

[4]  N. Verbruggen,et al.  Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri , 2003, Plant and Soil.

[5]  M. Tester,et al.  Arabidopsis thaliana root non-selective cation channels mediate calcium uptake and are involved in growth. , 2002, The Plant journal : for cell and molecular biology.

[6]  Rossana Henriques,et al.  Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects , 2002, Plant Molecular Biology.

[7]  A. J. Pollard,et al.  The Genetic Basis of Metal Hyperaccumulation in Plants , 2002 .

[8]  M. Macnair.  Within and between population genetic variation for zinc accumulation in Arabidopsis halleri. , 2002, New Phytologist.

[9]  M. Palmgren,et al.  A long way ahead: understanding and engineering plant metal accumulation. , 2002, Trends in plant science.

[10]  Valérie Bert,et al.  Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? , 2002, The New phytologist.

[11]  M. Guerinot,et al.  Expression of the IRT1 Metal Transporter Is Controlled by Metals at the Levels of Transcript and Protein Accumulation Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.001263. , 2002, The Plant Cell Online.

[12]  C. Curie,et al.  IRT1, an Arabidopsis Transporter Essential for Iron Uptake from the Soil and for Plant Growth Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.001388. , 2002, The Plant Cell Online.

[13]  B. Shipley,et al.  The balanced‐growth hypothesis and the allometry of leaf and root biomass allocation , 2002 .

[14]  M. Hawkesford,et al.  Influence of Iron Status on Cadmium and Zinc Uptake by Different Ecotypes of the Hyperaccumulator Thlaspi caerulescens 1 , 2002, Plant Physiology.

[15]  S. McGrath,et al.  Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. , 2002, Journal of experimental botany.

[16]  J. Bothwell,et al.  Calcium uptake by plant cells--channels and pumps acting in concert. , 2001, Trends in plant science.

[17]  J F Harper,et al.  Phylogenetic relationships within cation transporter families of Arabidopsis. , 2001, Plant physiology.

[18]  J. Morel,et al.  Distribution and Metal-Accumulating Behavior of Thlaspi caerulescens and Associated Metallophytes in France , 2001 .

[19]  Mark G. M. Aarts,et al.  Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens , 2001 .

[20]  Mark G. M. Aarts,et al.  Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens: Zinc transporters of Thlaspi caerulescens , 2001 .

[21]  G. Sacchi,et al.  Physiological evidence for a high-affinity cadmium transporter highly expressed in a Thlaspi caerulescens ecotype. , 2001, The New phytologist.

[22]  H. Küpper,et al.  Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri , 2000, Planta.

[23]  B. Gélie,et al.  Strategies of heavy metal uptake by three plant species growing near a metal smelter. , 2000, Environmental pollution.

[24]  D. Salt,et al.  Possible Molecular Mechanisms Involved in Nickel, Zinc and Selenium Hyperaccumulation in Plants , 2000, Biotechnology & genetic engineering reviews.

[25]  Hendrik Poorter,et al.  The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review , 2000 .

[26]  P J White,et al.  Calcium channels in higher plants. , 2000, Biochimica et biophysica acta.

[27]  M. Macnair,et al.  Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae). , 2000, The New phytologist.

[28]  L. Kochian,et al.  The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[29]  F. Morel,et al.  A biological function for cadmium in marine diatoms. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  M. Leblanc,et al.  Zinc and cadmium hyperaccumulation by Thlaspi caerulescens from metalliferous and nonmetalliferous sites in the Mediterranean area: implications for phytoremediation. , 2000, The New phytologist.

[31]  Steven N. Whiting,et al.  Positive responses to Zn and Cd by roots of the Zn and Cd hyperaccumulator Thlaspi caerulescens , 2000 .

[32]  M. Macnair,et al.  Zinc tolerance and hyperaccumulation are genetically independent characters , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[33]  F. Morel,et al.  Modulation of cadmium uptake in phytoplankton by seawater CO2 concentration , 1999, Nature.

[34]  J. Cullen.  Oceanography: Iron, nitrogen and phosphorus in the ocean , 1999, Nature.

[35]  L. Toppi,et al.  Response to cadmium in higher plants , 1999 .

[36]  M. Koch,et al.  Systematics and evolutionary history of heavy metal tolerant Thlaspi caerulescens in Western Europe: evidence from genetic studies based on isozyme analysis , 1998 .

[37]  Baker,et al.  Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in thlaspi caerulescens , 1998, Plant physiology.

[38]  J. Ward,et al.  The plant cDNA LCT1 mediates the uptake of calcium and cadmium in yeast. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Marc Leblanc,et al.  The potential of Thlaspi caerulescens for phytoremediation of contaminated soils , 1998, Plant and Soil.

[40]  Fox,et al.  The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants , 1998, Plant physiology.

[41]  P. Meerts,et al.  Heavy metal tolerance and accumulation in metallicolous and non-metallicolous populations of Thlaspi caerulescens from continental Europe , 1997, Plant Ecology.

[42]  S. McGrath,et al.  Zinc and cadmium uptake by the hyperaccumulator Thlaspi caerulescens in contaminated soils and its effects on the concentration and chemical speciation of metals in soil solution , 1997, Plant and Soil.

[43]  S. McGrath,et al.  Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non‐hyperaccumulator Thlaspi ochroleucum , 1997 .

[44]  Sally Brown,et al.  Phytoremediation of soil metals. , 1997, Current opinion in biotechnology.

[45]  S. McGrath,et al.  Heavy metal uptake and chemical changes in the rhizosphere of Thlaspi caerulescens and Thlaspi ochroleucum grown in contaminated soils , 1997, Plant and Soil.

[46]  L. Kochian,et al.  Physiological Characterization of Root Zn2+ Absorption and Translocation to Shoots in Zn Hyperaccumulator and Nonaccumulator Species of Thlaspi , 1996, Plant physiology.

[47]  A. J. Pollard,et al.  Quantitative genetics of zinc hyperaccumulation in Thlaspi caerulescens. , 1996, The New phytologist.

[48]  A. Baker,et al.  Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. & C. Presl (Brassicaceae). , 1994, The New phytologist.

[49]  P. Hatton,et al.  Localization of zinc and cadmium in Thlaspi caerulescens (Brassicaceae), a metallophyte that can hyperaccumulate both metals , 1992 .

[50]  H. Marschner.  Mineral Nutrition of Higher Plants , 1988 .

[51]  J. Wilson.  A review of evidence on the control of shoot: root ratio , 1988 .

[52]  M. J. Ingrouille,et al.  THLASPI CAERULESCENS J. & C. PRESL. (T. ALPESTRE L.) IN BRITAIN. , 1986, The New phytologist.

[53]  Robert R. Brooks,et al.  European species of Thlaspi L. (Cruciferae) as indicators of nickel and zinc , 1983 .

[54]  A. Stebbing,et al.  Hormesis--the stimulation of growth by low levels of inhibitors. , 1982, The Science of the total environment.

[55]  R. Davis,et al.  UPPER CRITICAL LEVELS OF TOXIC ELEMENTS IN PLANTS , 1977 .

[56]  Werner Mathys,et al.  The Role of Malate, Oxalate, and Mustard Oil Glucosides in the Evolution of Zinc‐Resistance in Herbage Plants , 1977 .

[57]  L. Audus.  Whole Plants , 1968, Nature.

[58]  K. Abromeit.  Music Received , 2023, Notes.

[59]  Enzo Lombi,et al.  Phytoremediation of metals, metalloids, and radionuclides , 2002 .

[60]  S. McGrath,et al.  Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense , 2000 .

[61]  D. Salt,et al.  Mechanisms of metal hyperaccumulation in plants , 2000 .

[62]  Alan J. M. Baker,et al.  Metal Hyperaccumulator Plants: A Review of the Ecology and Physiology of a Biological Resource for Phytoremediation of Metal-Polluted Soils , 2000 .

[63]  H. Schat,et al.  Metal-specific pattern of tolerance, uptake, and transport of heavy metals in hyperaccumulating and non-hyperaccumulating metallophytes. , 2000 .

[64]  I. Raskin,et al.  Phytoremediation of toxic metals : using plants to clean up the environment , 2000 .

[65]  R. Boyd.  Hyperaccumulation as a plant defensive strategy , 1998 .

[66]  Alan J. M. Baker,et al.  Zinc and Cadmium Uptake by Hyperaccumulator Thlaspi caerulescens Grown in Nutrient Solution , 1995 .

[67]  S. McGrath,et al.  The Potential for the Use of Metal-Accumulating Plants for the in Situ Decontamination of Metal-Polluted Soils , 1993 .

[68]  Alan J. M. Baker,et al.  TERRESTRIAL HIGHER PLANTS WHICH HYPERACCUMULATE METALLIC ELEMENTS. A REVIEW OF THEIR DISTRIBUTION, ECOLOGY AND PHYTOCHEMISTRY , 1989 .

[69]  D. Delmer,et al.  Annual review of plant physiology and plant molecular biology , 1988 .

[70]  A. Baker.  ACCUMULATORS AND EXCLUDERS ?STRATEGIES IN THE RESPONSE OF PLANTS TO HEAVY METALS , 1981 .

[71]  P. Duvigneaud,et al.  ACCUMULATION DE METAUX LOURDS TOXIQUES DANS DIVERS ECOSYSTEMES TERRESTRES POLLUES PAR DES RETOMBEES D'ORIGINE INDUSTRIELLE , 1974 .

[72]  E. Hewitt,et al.  Plant mineral nutrition. , 1974 .