Solving the global environmental and agricultural problem of chronic low-level cadmium (Cd) exposure requires better mechanistic understanding. Here, soybean (Glycine max) plants were exposed to Cd concentrations ranging from 0.5 nM (background concentration, control) to 3 µM. Plants were cultivated hydroponically under non-nodulating conditions for 10 weeks. Toxicity symptoms, net photosynthetic oxygen production and photosynthesis biophysics (chlorophyll fluorescence: Kautsky and OJIP) were measured in young mature leaves. Cd binding to proteins [metalloproteomics by HPLC-inductively coupled plasma (ICP)-MS] and Cd ligands in light-harvesting complex II (LHCII) [X-ray absorption near edge structure (XANES)], and accumulation of elements, chloropyll, and metabolites were determined in leaves after harvest. A distinct threshold concentration of toxicity onset (140 nM) was apparent in strongly decreased growth, the switch-like pattern for nutrient uptake and metal accumulation, and photosynthetic fluorescence parameters such as Φ RE10 (OJIP) and saturation of the net photosynthetic oxygen release rate. XANES analyses of isolated LHCII revealed that Cd was bound to nitrogen or oxygen (and not sulfur) atoms. Nutrient deficiencies caused by inhibited uptake could be due to transporter blockage by Cd ions. The changes in specific fluorescence kinetic parameters indicate electrons not being transferred from PSII to PSI. Inhibition of photosynthesis combined with inhibition of root function could explain why amino acid and carbohydrate metabolism decreased in favour of molecules involved in Cd stress tolerance (e.g. antioxidative system and detoxifying ligands).

Czech Academy of Sciences Biology Centre Institute of Hydrobiology Department of Hydrochemistry and Ecosystem Modelling Budějovice Czech Republic

Czech Academy of Sciences Biology Centre Institute of Plant Molecular Biology Department of Plant Biophysics and Biochemistry Budějovice Czech Republic

Czech Academy of Sciences Institute of Geology Department of Geological Processes Praha Czech Republic

University of South Bohemia Faculty of Sciences Department of Experimental Plant Biology České Budějovice Czech Republic

Zobrazit více v PubMed

Andresen  E, Kappel S, Stärk HJ, et al.  2016. Cadmium toxicity investigated at the physiological and biophysical levels under environmentally relevant conditions using the aquatic model plant Ceratophyllum demersum. New Phytologist 210, 1244–1258. PubMed

Andresen  E, Küpper H. 2013. Cadmium toxicity in plants. In: Sigel A, Sigel H, Sigel RKO, eds. Cadmium: from toxicity to essentiality. Dordrecht, The Netherlands: Springer Science + Business Media BV, 395–413. PubMed

Andresen  E, Opitz J, Thomas G, Stärk HJ, Dienemann H, Jenemann K, Dickinson BC, Küpper H. 2013. Effects of Cd & Ni toxicity to Ceratophyllum demersum under environmentally relevant conditions in soft & hard water including a German lake. Aquatic Toxicology 142–143, 387–402. PubMed

Andresen  E, Peiter E, Küpper H. 2018. Trace metal metabolism in plants. Journal of Experimental Botany 69, 909–954. PubMed

Balestrasse  KB, Gallego SN, Benavides MP, Tomaro ML. 2005. Polyamines and proline are affacted by cadmium stress in nodules and roots of soybean plants. Plant and Soil 270, 343–353.

Ben Ammar  W, Nouairi I, Zarrouk M, Jemal F. 2008. The effect of cadmium on lipid and fatty acid biosynthesis in tomato leaves. Biologia 63, 86–93.

Benavides  MP, Gallego SM, Tomaro ML. 2005. Cadmium toxicity in plants. Brazilian Journal of Plant Physiology 17, 21–34.

Caliebe  WA, Murzin V, Kalinko A, Görlitz M. 2019. High-flux XAFS-beamline P64 at PETRA III. AIP Conference Proceedings 2054, 060031.

Clemens  S. 2006. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88, 1707–1719. PubMed

Clemens  S, Aarts MG, Thomine S, Verbruggen N. 2013. Plant science: the key to preventing slow cadmium poisoning. Trends in Plant Science 18, 92–99. PubMed

de Almeida  TBF, Flores RA, de Almeida HJ, de Mello Prado R, Maranhão DDC, Politi JS. 2017. Development and nutrition of soybeans with macronutrients deficiencies. Communications in Soil Science and Plant Analysis 48, 1616–1625.

Dudev  T, Lim C. 2014. Competition among metal ions for protein binding sites: determinants of metal ion selectivity in proteins. Chemical Reviews 114, 538–556. PubMed

Durand  TC, Sergeant K, Planchon S, Carpin S, Label P, Morabito D, Hausman JF, Renaut J. 2010. Acute metal stress in Populus tremula × P. alba (717-1B4 genotype): leaf and cambial proteome changes induced by cadmium 2+. Proteomics 10, 349–368. PubMed

Fagioni  M, Zolla L. 2009. Does the different proteomic profile found in apical and basal leaves of spinach reveal a strategy of this plant toward cadmium pollution response? Journal of Proteome Research 8, 2519–2529. PubMed

George  GN, Hedman B, Hodgson KO. 1998. An edge with XAS. Nature Structural and Molecular Biology 5, 645–647. PubMed

Hall  LJ. 2002. Cellular mechanism for heavy metal detoxification and tolerance. Journal of Experimental Botany 53, 1–11. PubMed

Haouari  CC, Nasraoui AH, Bouthour D, Houda MD, Daib CB, Mnai J, Gouia H. 2012. Response of tomato (Solanum lycopersicon) to cadmium toxicity: growth, element uptake, chlorophyll content and photosynthesis rate. African Journal of Plant Science 6, 1–7.

Hasan  SA, Fariduddin Q, Ali B, Hayat S, Ahmad A. 2009. Cadmium: toxicity and tolerance in plants. Journal of Environmental Botany 30, 165–174. PubMed

Hayat  S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A. 2012. Role of proline under changing environments: a review. Plant Signaling & Behavior 7, 1456–1466. PubMed PMC

Hédiji  H, Djebali W, Cabasson C, et al.  2010. Effects of long-term cadmium exposure on growth and metabolomic profile of tomato plants. Ecotoxicology and Environmental Safety 73, 1965–1974. PubMed

Hermans  C, Chen J, Coppens F, Inzé D, Verbruggen N. 2011. Low magnesium status in plants enhances tolerance to cadmium exposure. New Phytologist 192, 428–436. PubMed

Jahangir  M, Abdel-Farid BA, Choi YH, Verpoorte R. 2008. Metal ion-induced metabolite accumulation in Brassica rapa. Journal of Plant Physiology 165, 1429–1437. PubMed

Keunen  E, Peshev D, Vangronsveld J, Van Den Ende W, Cuypers A. 2013. Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant, Cell & Environment 36, 1242–1255. PubMed

Kieffer  P, Dommes J, Hoffmann L, Hausman JF, Renaut J. 2008. Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics 8, 2514–2530. PubMed

Küpper  H, Andresen E. 2016. Mechanisms of metal toxicity in plants. Metallomics 8, 269–285. PubMed

Küpper  H, Benedikty Z, Morina F, Andresen E, Mishra A, Trtílek M. 2019a. Analysis of OJIP chlorophyll fluorescence kinetics and QA reoxidation kinetics by direct fast imaging. Plant Physiology 179, 369–381. PubMed PMC

Küpper  H, Bokhari SNH, Jaime-Pérez N, Lyubenova L, Ashraf N, Andresen E. 2019b. Ultratrace metal speciation analysis by coupling of sector-field ICP-MS to high-resolution size exclusion and reversed-phase liquid chromatography. Analytical Chemistry 91, 10961–10969. PubMed

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

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 RJ, Rüdiger W, Scheer H, eds. Chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications. Dordrecht, The Netherlands: Springer-Verlag, 67–77.

Küpper  H, Leitenmaier B. 2013. Cadmium-accumulating plants. In: Sigel A, Sigel H, Sigel RKO, eds. Cadmium: from toxicity to essentiality. Dordrecht, The Netherlands: Springer Science + Business Media BV, 373–394. PubMed

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

Küpper  H, Parameswaran A, Leitenmaier B, Trtílek M, Setlík I. 2007a. Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytologist 175, 655–674. PubMed

Küpper  H, Seibert S, Parameswaran A. 2007b. Fast, sensitive, and inexpensive alternative to analytical pigment HPLC: quantification of chlorophylls and carotenoids in crude extracts by fitting with Gauss peak spectra. Analytical Chemistry 79, 7611–7627. PubMed

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

Leitenmaier  B, Küpper H. 2013. Compartmentation and complexation of metals in hyperaccumulator plants. Frontiers in Plant Science 4, 374. PubMed PMC

Lux  A, Martinka M, Vaculík M, White PJ. 2011. Root responses to cadmium in the rhizosphere: a review. Journal of Experimental Botany 62, 21–37. PubMed

Maret  W, Moulis JM. 2013. The bioinorganic chemistry of cadmium in the context of its toxicity. In: Sigel A, Sigel H, Sigel RKO, eds. Cadmium: from toxicity to essentiality. Dordrecht, The Netherlands: Springer Science + Business Media BV, 1–29. PubMed

McLaughlin  MJ, Parker DR, Clarke JM. 1999. Metals and micronutrients—food safety issues. Field Crops Research 60, 143–163.

Mishra  S, Stärk H-J, Küpper H. 2014. A different sequence of events than previously reported leads to arsenic-induced damage in Ceratophyllum demersum L. Metallomics 6, 444–454. PubMed

Nazar  R, Iqbal N, Masood A, Khan MIR, Syeed S, Khan NA. 2012. Cadmium toxicity in plants and role of mineral nutrients in its alleviation. American Journal of Plant Sciences 3, 1476–1489.

Perfus-Barbeoch  L, Leonhardt N, Vavasseur A, Forestier C. 2002. Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. The Plant Journal 32, 539–548. PubMed

Polatajko  A, Feldmann I, Hayen H, Jakubowski N. 2011. Combined application of a laser-ablation-ICP-MS assay for screening and ESI-FTICR for identification of a Cd-binding protein in Spinacia oleracea L. after exposure to Cd. Metallomics 3, 1001–1008. PubMed

Rabêlo  FHS, Fernie AR, Navazas A, Borgo L, Keunen E, Silva BKDAD, Cuypers A. 2018. A glimpse into the effect of sulfur supply on metabolite profiling, glutathione and phytochelatins in Panicum maximum cv. Massai exposed to cadmium. Environmental and Experimental Botany 151, 76–88.

Ravel  B, Newville M. 2005. ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. Journal of Synchrotron Radiation 12, 537–541. PubMed

Sárvári  E, Fodor F, Cseh E, Varga A, Záray G, Zolla L. 1999. Relationship between changes in ion content of leaves and chlorophyll-protein composition in cucmber under Cd and Pb stress. Zeitschrift für Naturforschung C 54, 746–753.

Schat  H, Sharma SS, Vooijs R. 1997. Heavy metal-induced accumulation of free proline in a metal-tolerant and a nontolerant ecotype of Silene vulgaris. Physiologia Plantarum 101, 477–482.

Shamsi  IH, Jilani G, Guo-Ping Z, Kang W. 2008. Cadmium stress tolerance through potassium nutrition in soybean. Asian Journal of Chemistry 20, 1099–1108.

Siddiqi  MY, Glass ADM. 1981. Utilization index: a modified approach to the estimation and comparison of nutrient utilization efficiency in plants. Journal of Plant Nutrition 4, 289–302.

Thomas  G, Stärk HJ, Wellenreuther G, Dickinson BC, Küpper H. 2013. Effects of nanomolar copper on water plants—comparison of biochemical and biophysical mechanisms of deficiency and sublethal toxicity under environmentally relevant conditions. Aquatic Toxicology 140-141, 27–36. PubMed

Uchida  R. 2000. Essential nutrients for plant growth: nutrient functions and deficiency symptoms. In: Silva JA, Uchida R, eds. Plant nutrient management in Hawaii’s soils, approaches for tropical and subtropical agriculture. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa, 31–55.

Upchurch  RG. 2008. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnology Letters 30, 967–977. PubMed

Villiers  F, Ducruix C, Hugouvieux V, Jarno N, Ezan E, Garin J, Junot C, Bourguignon J. 2011. Investigating the plant response to cadmium exposure by proteomic and metabolomic approaches. Proteomics 11, 1650–1663. PubMed

Walker  D. 1990. The use of the oxygen electrode and fluorescence probes in simple measurements of photosynthesis, 2nd edn. Sheffield, UK: Robert Hill Institute, The University of Sheffield.

Zhao  F, McGrath SP, Crosland AR. 1994. Comparison of three wet digestion methods for the determination of plant sulphur by inductively coupled plasma atomic emission spectrometry (ICP-AES). Communications in Soil Science and Plant Analysis 25, 407–418.

Massive Accumulation of Strontium and Barium in Diplonemid Protists

The Influence of Calcium on the Growth, Morphology and Gene Regulation in Gemmatimonas phototrophica

Interaction Between Zn Deficiency, Toxicity and Turnip Yellow Mosaic Virus Infection in Noccaea ochroleucum