Acclimation of hyperaccumulators to heavy metal-induced stress is crucial for phytoremediation and was investigated using the hyperaccumulator Thlaspi caerulescens and the nonaccumulators T. fendleri and T. ochroleucum. Spatially and spectrally resolved kinetics of in vivo absorbance and fluorescence were measured with a novel fluorescence kinetic microscope. At the beginning of growth on cadmium (Cd), all species suffered from toxicity, but T. caerulescens subsequently recovered completely. During stress, a few mesophyll cells in T. caerulescens became more inhibited and accumulated more Cd than the majority; this heterogeneity disappeared during acclimation. Chlorophyll fluorescence parameters related to photochemistry were more strongly affected by Cd stress than nonphotochemical parameters, and only photochemistry showed acclimation. Cd acclimation in T. caerulescens shows that part of its Cd tolerance is inducible and involves transient physiological heterogeneity as an emergency defence mechanism. Differential effects of Cd stress on photochemical vs nonphotochemical parameters indicate that Cd inhibits the photosynthetic light reactions more than the Calvin-Benson cycle. Differential spectral distribution of Cd effects on photochemical vs nonphotochemical quenching shows that Cd inhibits at least two different targets in/around photosystem II (PSII). Spectrally homogeneous maximal PSII efficiency (F(v)/F(m)) suggests that in healthy T. caerulescens all chlorophylls fluorescing at room temperature are PSII-associated.

Faculty of Biological Sciences and Institute of Physical Biology University of South Bohemia Branišovská 31 CZ 370 05 České Budejovice Čzech Republic

Microbiological Institute ASCR Department of Autotrophic Microorganisms Opatovický mlýn CZ 37981 Třeboň Czech Republic

Photon Systems Instruments Ltd Koláčkova 31 CZ 62100 Brno Czech Republic

Universität Konstanz Mathematisch Naturwissenschaftliche Sektion Fachbereich Biologie D 78457 Konstanz Germany

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Assunção AGL, Costa Martins PDA, De Folter S, Vooijs R, Schat H, Aarts MGM. 2001. Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant, Cell & Environment 24: 217-226.

Assunção AGL, Schat H, Aarts MGM. 2003. Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytologist 159: 351-360.

Baker AJM. 1981. Accumulators and excluders-strategies in the response of plants to heavy metals. Journal of Plant Nutrition 3: 643-654.

Baker AJM, McGrath SP, Sidoli CMD, Reeves RD. 1994. The possibility of situ heavy metal decontamination of polluted soils using crops of metal-accumulating plants. Resources, Conservation, and Recycling 11: 41-49.

Becher M, Talke IN, Krall L, Krämer U. 2004. Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant Journal 37: 251-268.

Bert V, Meerts P, Saumitou-Laprade P, Salis P, Gruber W, Verbruggen N. 2003. Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri. Plant and Soil 249: 9-18.

Bhatia NP, Walsh KB, Orlic I, Siegele R, Ashwath N, Baker AJM. 2004. Studies on spatial distribution of nickel in leaves and stems of the metal hyperaccumulator Stackhousia tryonii using nuclear microprobe (micro-PIXE) and EDXS techniques. Functional Plant Biology 31: 1061-1074.

Bidwell SD, Crawford SA, Woodrow IE, Summer-Knudsen J, Marshal AT. 2004. Sub-cellular localization of Ni in the hyperaccumulator Hybanthus floribundus (Lindley) F. Muell. Plant, Cell & Environment 27: 705-716.

Boyd RS, Davis MA, Wall MA, Balkwill K. 2002. Nickel defends the South African hyperaccumulator Senecio coronatus (Asteraceae) against Helix aspersa (Mollusca: Pulmonidae). Chemoecology 12: 91-97.

Boyd RS, Martens SN. 1994. Nickel hyperaccumulated by Thlaspi montanum var. montanum is acutely toxic to an insect herbivore. Oikos 70: 21-25.

Broadhurst CL, Chaney RL, Angle JS, Erbe EF, Maugel TK. 2004. Nickel localization and response to increasing Ni soil levels in leaves of the Ni hyperaccumulator Alyssum murale. Plant and Soil 265: 225-242.

Brooks RR, Lee J, Reeves RD, Jaffre T. 1977. Detection of nickeliferous rocks by analysis of herbarium species of indicator plants. Journal of Geochemical Exploration 7: 49-57.

Buchauer MJ. 1973. Contamination of soil and vegetation near a zinc smelter by zinc, cadmium, copper, and lead. Environmental Science and Technology 7: 131-135.

Cedeno-Maldonado A, Swader JA, Heath RL. 1972. The cupric ion as an inhibitor of photosynthetic electron transport in isolated chloroplasts. Plant Physiology 50: 698-701.

Chaney RL, Angle JS, McIntosh MS, Reeves RD, Li YM, Brewer EP, Chen KY, Roseberg RJ, Perner H, Synkowski EC, Broadhurst CL, Wang S, Baker AJM. 2005. Using hyperaccumulator plants to phytoextract Soil Ni and Cd. Zeitschrift für Naturforschung 60c: 190-198.

Ciscato M, Valcke R. 1998. Chlorophyll fluorescence imaging of heavy metal treated plants. In: Garab G, ed. Photosynthesis: mechanisms and effects, Vol. IV. Dordrecht, the Netherlands: Kluwer Academic Publishers, 2661-2663.

Cobbett C, Goldsbrough P. 2002. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology 53: 159-182.

Cosio C, DeSantis L, Frey B, Diallo S, Keller C. 2005. Distribution of cadmium in leaves of Thlaspi caerulescens. Journal of Experimental Botany 56: 765-775.

Cuypers A, Vangronsveld J, Clijsters H. 2002. Peroxidases in roots and primary leaves of Phaseolus vulgaris copper and zinc phytotoxicity: a comparison. Journal of Plant Physiology 159: 869-876.

Ebbs S, Lau I, Ahner B, Kochian LV. 2002. Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens (J. & C. Presl). Planta 214: 635-640.

Faller P, Kienzler K, Krieger-Liszkay A. 2005. Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of Photosystem II by competitive binding to the essential Ca2+ site. Biochimica Biophysia Acta 1706: 158-164.

Fergusson JE, Hayes RW, Yong TS, Thiew SH. 1980. Heavy metal pollution by traffic in Christchurch, New Zealand: lead and cadmium content of dust, soil and plant samples. New Zealand Journal of Science 23: 293-310.

Ferimazova N, Küpper H, Nedbal L, Trtílek M. 2002. New insights into photosynthetic oscillations revealed by two-dimensional microscopic measurements of chlorophyll fluorescence kinetics in intact leaves and isolated protoplasts. Photochemistry and Photobiology 76: 501-508.

Franck F, Dewez D, Popovic R. 2005. Changes in the room-temperature emission spectrum of Chlorophyll during fast and slow phases of the Kautsky effect in intact leaves. Photochemistry and Photobiology 81: 431-443.

Franck F, Juneau P, Popovic R. 2002. Resolution of the photosystem I and photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature. Biochimica et Biophysica Acta: Bioenergetics 1556: 239-246.

Frey B, Keller C, Zierold K, Schulin R. 2000. Distribution of Zn in functionally different epidermal cells of the hyperaccumulator Thlaspi caerulescens. Plant, Cell & Environment 23: 675-687.

Genty B, Briantais J, Baker NR. 1989. The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990: 87-92.

Hanson B, Garifullina GF, Lindblom SD, Wangeline A, Ackley A, Kramer K, Norton AP, Lawrence CB, Pilon-Smits EAH. 2003. Selenium accumulation protects Brassica juncea from invertebrate herbivory and fungal infection. New Phytologist 159: 461-469.

Hemelrijk PW, Kwa SLS, Van Grondelle R, Dekker JP. 1992. Spectroscopic properties of LHC-II, the main light-harvesting chlorophyll a/b protein complex from chloroplast membranes. Biochimica Biophysica Acta 1098: 159-166.

Van Hoof NALM, Koevoets PLM, Hakvoort HWJ, Ten Bookum WM, Schat H, Verkleij JAC, Ernst WHO. 2001. Enhanced ATP-dependent copper efflux across the root cell plasma membrane in copper-tolerant Silene vulgaris. Physiologia Plantarum 113: 225-232.

Jhee EM, Boyd RS, Eubanks MD. 2005. Nickel hyperaccumulation as an elemental defense of Streptanthus polygaloides (Brassicaceae): influence of herbivore feeding mode. New Phytologist 168: 331-343.

Joshi MK, Mohanty P. 2004. Chlorophyll a fluorescence as a probe of heavy metal ion toxicity in plants. In: Papageorgiou GC, Govindjee, eds. Chlorophyll a fluorescence: a signature of photosynthesis. Dordrecht, The Netherlands: Springer, 637-661.

Koch M, Al-Shehbaz IA. 2004. Taxonomic and phylogenetic evaluation of the American ‘Thlaspi’ species: identity and relationship to the Eurasian genus Noccaea (Brassicaceae). Systematic Botany 29: 375-384.

Krämer U, Cotterhowells JD, Charnock JM, Baker AJM, Smith JAC. 1996. Free histidine as a metal chelator in plants that accumulate nickel. Nature 379: 635-638.

Krupa Z. 1999. Cadmium against higher-plant photosynthesis - A variety of effects and where they possibly come from. Zeitschrift für Naturforschung C 54: 723-729.

Krupa Z, Öquist G, Huner NPA. 1993. The effects of cadmium on photosynthesis of Phaseolus vulgaris- a fluorescence analysis. Physiologia Plantarum 88: 626-630.

Küpper H, Kroneck PMH. 2005. Heavy metal uptake by plants and cyanobacteria. In: Sigel A, Sigel H, Sigel RKO, eds. Metal ions in biological systems. New York, NY, USA: Marcel Dekker Inc, 97-142.

Küpper H, Küpper F, Spiller M. 1996. Environmental relevance of heavy metal substituted chlorophylls using the example of water plants. Journal of Experimental Botany 47: 259-266.

Küpper H, Küpper F, Spiller M. 1998. In situ detection of heavy metal substituted chlorophylls in water plants. Photosynthesis Research 58: 125-133.

Küpper H, Küpper FC, Spiller M. 2006. [Heavy metal]-chlorophylls formed in vivo during heavy metal stress and degradation products formed during digestion, extraction and storage of plant material. In: Grimm B, Porra R, Rüdiger W, Scheer H, eds Chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications. Advances in Photosynthesis and Respiration, Vol. 25. Dordrecht, the Netherlands: Kluwer Academic Publishers, 67-77.

Küpper H, Lombi E, Zhao FJ, McGrath SP. 2000a. Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212: 75-84.

Küpper H, Lombi E, Zhao FJ, Wieshammer G, McGrath SP. 2001. Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. Journal of Experimental Botany 52: 2291-2300.

Küpper H, Mijovilovich A, Meyer-Klaucke W, Kroneck PMH. 2004. Tissue- and age-dependent differences in the complexation of cadmium and zinc in the Cd/Zn hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by X-ray absorption spectroscopy. Plant Physiology 134: 748-757.

Küpper H, Šetlík I, Spiller M, Küpper FC, Prášil O. 2002. Heavy metal-induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. Journal of Phycology 38: 429-441.

Küpper H, Šetlík I, Trtílek M, Nedbal L. 2000b. A microscope for two-dimensional measurements of vivo chlorophyll fluorescence kinetics using pulsed measuring light, continuous actinic light and saturating flashes. Photosynthetica 38: 553-570.

Küpper H, Spiller M, Küpper F. 2000c. Photometric method for the quantification of chlorophylls and their derivatives in complex mixtures: fitting with gauss-peak-spectra. Analytical Biochemistry 286: 247-256.

Küpper H, Zhao FJ, McGrath SP. 1999. Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiology 119: 305-311.

Lagerwerff JV, Specht AW. 1970. Contamination of roadside soil and vegetation with cadmium, nickel, lead, and zinc. Environmental Science and Technology 4: 583-586.

Lane TW, Morel FMM. 2000. A biological function for cadmium in marine diatoms. Proceedings of National Academy of Sciences, USA 97: 4627-4631.

Lasat MM, Baker AJM, Kochian LV. 1996. Physiological characterization of root Zn2+ absorption and translocation to shoots in Zn hyperaccumulator and nonaccumulator species of Thlaspi. Plant Physiology 112: 1715-1722.

Lasat MM, Baker AJM, Kochian LV. 1998. Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens. Plant Physiology 118: 875-883.

Lombi E, Zhao FJ, Dunham SJ, McGrath SP. 2000. Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytologist 145: 11-20.

Macnair MR, Bert V, Huitson SB, SaumitouLaprade P, Petit D. 1999. Zinc tolerance and hyperaccumulation are genetically independent characters. Proceedings of the Royal Society of London, Series B 266: 2175-2179.

Martens SN, Boyd RS. 1994. The ecological significance of nickel hyperaccumulation: a plant chemical defense. Oecologia 98: 379-384.

Maxwell K, Johnson GN. 2000. Chlorophyll fluorescence: a practical guide. Journal of Experimental Botany 51: 659-668.

McBride MB, Barrett KA, Martinez CE. 2005. Zinc and cadmium distribution and leaching in a metalliferous peat. Water Air and Soil Pollution 171: 67-80.

McBride MB, Richards BK, Steenhuis T, Russo JJ, Sauvé S. 1997. Mobility and solubility of toxic metals and nutrients in soil fifteen years after sewage sludge application. Soil Science 162: 487-500.

McGrath SP, Zhao FJ. 2003. Phytoextraction of metals and metalloids from contaminated soils. Current Opinion in Biotechnology 14: 277-282.

Mitani T, Ogawa M. 1998. Cadmium leaching by acid rain from cadmium-enriched activated sludge applied in soil. Journal of Environmental Science and Health A33: 1569-1581.

Nedbal L, Soukupová J, Kaftan D, Whitmarsh J, Trtílek M. 2000. Kinetic imaging of chlorophyll fluorescence using modulated light. Photosynthesis Research 66: 3-12.

Nedbal L, Whitmarsh J. 2004. Chlorophyll fluorescence imaging of leaves and fruits. In: Chlorophyll a fluorescence - a signature of photosynthesis. Advances in Photosynthesis and Respiration, Vol. 19. Dordrecht, the Netherlands: Springer, 389-407.

Ouzounidou G, Moustakas M, Strasser RJ. 1997. Sites of action of copper in the photosynthetic apparatus of maize leaves: kinetic analysis of chlorophyll fluorescence, oxygen evolution, absorption changes and thermal dissipation as monitored by photoacoustic signals. Australian Journal of Plant Physiology 24: 81-90.

Oxborough K. 2004. Using chlorophyll a fluorescence imaging to monitor photosynthetic performance. In: Papageorgiou GC, Govindjee, eds. Chlorophyll a fluorescence: a signature of photosynthesis. Dordrecht, the Netherlands: Springer, 409-428.

Papageorgiou GC, Govindjee. 2004. Chlorophyll a fluorescence: a signature of photosynthesis. Dordrecht, the Netherlands: Springer.

Papoyan A, Kochian LV. 2004. Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. characterization of a novel heavy metal transporting ATPase. Plant Physiology 136: 3814-3823.

Peer WA, Mahmoudian M, Freeman JL, Lahner B, Richards EL, Reeves RD, Murphy AS, Salt DE. 2006. Assessment of plants from the Brassicaceae family as genetic models for the study of nickel and zinc hyperaccumulation. New Phytologist 172: 248-260.

Peer WA, Mamoudian M, Lahner B, Reeves RD, Murphy AS, Salt DE. 2003. Development of a model plant to study the molecular genetics of metal hyperaccumulation. Part I: Germplasm analysis of 20 Brassicaceae accessions from Austria, France, Turkey, and USA. New Phytologist 159: 421-430.

Pence NS, Larsen PB, Ebbs SD, Letham DLD, Lasat MM, Garvin DF, Eide D, Kochian LV. 2000. The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proceedings of National Academy of Sciences, USA 97: 4956-4960.

Pollard AJ, Powell KD, Harper FA, Smith JAC. 2002. The genetic basis of metal hyperaccumulation in plants. Critical Reviews in Plant Sciences 21: 539-566.

Poschenrieder C, Tolrà R, Barceló J. 2006. Can metals defend plants against biotic stress? Trends in Plant Science 11: 288-293.

Prasad MNV, Hagemeyer J. 1999. Heavy metal stress in plants: from molecules to ecosystems. Berlin, Germany: Springer.

Rohácek K. 2002. Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40: 13-29.

Ruban AV, Horton P. 1994. Spectroscopy of non-photochemical and photochemical quenching of chlorophyll fluorescence in leaves; evidence for a role of the light-harvesting complex of photosystem II in the regulation of energy dissipation. Photosynthesis Research 40: 181-190.

Sagner S, Kneer R, Wanner G, Cosson JP, Deus-Neumann B, Zenk MH. 1998. Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminata. Phytochemistry 47: 339-347.

Salt DE, Prince RC, Baker AJM, Raskin I, Pickering IJ. 1999. Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environmental Science and Technology 33: 712-717.

Schat H, Llugany M, Vooijs R, Hartley-Whitaker J, Bleeker PM. 2002. The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and nonhyperaccumulator metallophytes. Journal of Experimental Botany 53: 2381-2392.

Shen ZG, Zhao FJ, McGrath SP. 1997. Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non-hyperaccumulator Thlaspi ochroleucum. Plant, Cell & Environment 20: 898-906.

Siebke K, Weis E. 1995a. Assimilation images of leaves of Glechoma hederacea: analysis of non-synchronous stomata related oscillations. Planta 196: 155-165.

Siebke K, Weis E. 1995b. Imaging of chlorophyll-a-fluorescence in leaves: topography of photosynthetic oscillations in leaves of Glechoma hederacea. Photosynthesis Research 45: 225-237.

Van Geen A, Adkins JF, Boyle EA, Nelson CH, Palanques A. 1997. A 120 yr record of widespread contamination from mining of the Iberian pyrite belt. Geology 25: 291-294.

Wang J, Zhao FJ, Meharg AA, Raab A, Feldmann J, McGrath SP. 2002. Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiology 130: 1552-1561.

Webb SM, Gaillard JF, Ma LQ, Tu C. 2003. XAS speciation of arsenic in a hyper-accumulating fern. Environmental Science and Technology 37: 754-760.

Weber M, Harada E, Vess C, Von Roepenack-Lahaye E, Clemens S. 2004. Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors Plant Journal 37: 269-281.

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