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Metabolic Responses to Lead of Metallicolous and Nonmetallicolous Populations of Armeria maritima

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Abstract

Metabolic responses to Pb(NO3)2 (Pb) ions of excised leaves of metallicolous (MPs) and nonmetallicolous populations (NMPs) of Armeria maritima, cultivated on normal soil, were examined. Detached leaves were exposure to Pb for 24 h, and metabolic parameters were investigated. Pb decreased the photosynthesis (Pn) rate and photosystem II (PSII) activity, whereas the photochemical efficiency of PSII remained unchanged. In both populations, Pb ions caused increase in O2 uptake of dark-treated leaves; however, respiration after Pn was not affected. Pb increased superoxide dismutase activity in MP leaves and malondialdehyde content in NMP leaves. Other metabolites after Pb treatment were increased (proline or H2O2) or decreased (malate). Ascorbate peroxidase activity and adenosine triphosphate content decreased more in MP than in NMP leaves. Our results indicate that A. maritima is well adapted to heavy metal-contaminated soils, and we discuss potential causes of the stimulation of respiration by Pb ions and possible reasons for the tolerance to oxidative stress of plants growing in a metal-rich habitat.

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Abbreviations

APX:

Ascorbate peroxidase

CAT:

Catalase

ETC:

Electron transport chain

Fv/Fm:

Photochemical efficiency of PSII

GPX:

Guaiacol peroxidase

LEDR:

Light-enhanced dark respiration

ME:

Malic enzyme

MDH:

Malate dehydrogenase

MDA:

Malondialdehyde

MP:

Metallicolous population

NMP:

Non-metallicolous population

Pb:

Pb(NO3)2

Pn:

Net photosynthesis

PSII:

Photosystem II

R:

Respiration

ROS:

Reactive oxygen species

RWC:

Relative water content

SOD:

Superoxide dismutase

References

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 55:373–379

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bazzaz FA, Carlson RW, Rolfe GE (1974) The effect of heavy metals on plants: Part I. Inhibition of gas exchange in sunflower by Pb, Cd, Ni and Tl. Environ Pollut 7:241–246

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  Google Scholar 

  • Bertrand M, Poirier I (2005) Photosynthetic organisms and excess of metals. Photosynthetica 43:345–353

    Article  CAS  Google Scholar 

  • Borecký J, Vercesi AE (2005) Plant uncoupling mitochondrial protein and alternative oxidase: energy metabolism and stress. Biosci Rep 25:271–286

    Article  Google Scholar 

  • Boucher N, Carpentier R (1999) Hg2+, Cu2+, and Pb2+-induced changes in photosystem II photochemical yield and energy storage in isolated thylakoid membranes: a study using simultaneous fluorescence and photoacoustic measurements. Photosynth Res 59:167–174

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Casati P, Drincovich MF, Edwards G, Andreo CS (1999) Malate metabolism b NADP-malic enzyme in plant defense. Photosynth Res 61:99–105

    Article  CAS  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  CAS  Google Scholar 

  • Clijsters H, Van Assche F (1985) Inhibition of photosynthesis by heavy metals. Photosynth Res 7:31–40

    Article  CAS  Google Scholar 

  • Dahmani-Muller H, van Oort F, Gélie B, Balabane M (2000) Strategies of heavy metal uptake by three plant species growing near a metal smelter. Environ Pollut 109:231–238

    Article  CAS  Google Scholar 

  • Doubnerová V, Ryšlavá H (2011) What can enzymes of C4 photosynthesis do for C3 plants under stress? Plant Sci 180:575–583

    Article  Google Scholar 

  • Drożak A, Romanowska E (2006) Acclimation of mesophyll and bundle sheath chloroplasts of maize to different irradiances during growth. Biochim Biophys Acta 1757:1539–1546

    Article  Google Scholar 

  • Gardeström P, Wigge B (1988) Influence of photorespiration on ATP/ADP ratios in the chloroplasts, mitochondria, and cytosol, studied by rapid fractionation of barley (Hordeum vulgare) protoplasts. Plant Physiol 88:69–76

    Article  Google Scholar 

  • Gupta D, Huang H, Yang X, Razafindrabe B, Inouhe M (2010) The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione. J Hazard Mater 177:437–444

    Article  CAS  Google Scholar 

  • Hohorst HJ (1965) L-malate. Determination with malic acid dehydrogenase and DNP. In: Bergmeyer HU (ed) Methods in enzymatic analysis. Academic Press, New York, pp 328–332

    Chapter  Google Scholar 

  • Hossain MA, Asada K (1984) Inactivation of ascorbate peroxidase in spinach chloroplasts on dark addition of hydrogen peroxide: its protection by ascorbate. Plant Cell Physiol 25:1285–1295

    CAS  Google Scholar 

  • Hurth MA, Suh SJ, Kretzschmar T, Geis T, Bregnate M, Gambale F et al (2005) Impaired pH homeostasis in Arabidopsis, lacking the vacuolar dicarboxylate transporter and analysis of carboxylic acid transport across the tonoplast. Plant Physiol 137:901–910

    Article  CAS  Google Scholar 

  • Iba K (2002) Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu Rev Plant Biol 53:225–245

    Article  CAS  Google Scholar 

  • Islam E, Liu D, Li T, Yang X, Jin X, Mahmood Q et al (2008) Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 154:914–926

    Article  CAS  Google Scholar 

  • Israr M, Jewell A, Kumar D, Sahi SV (2011) Interactive effects of lead, copper, nickel and zinc on growth, metal uptake and antioxidative metabolism of Sesbania drummondii. J Hazard Mater 186:1520–1526

    Article  CAS  Google Scholar 

  • Köhl KI (1997) Do Armeria maritima (Mill.) Willd. Ecotypes from metalliferous soils and non-metalliferous soils differ in growth response under Zn stress? A comparison by a new artificial soil method. J Exp Bot 48:1959–1967

    Article  Google Scholar 

  • Kosugi H, Kikugawa K (1985) Thiobarbituric acid reaction of aldehydes and oxidized lipids in glacial acetic acid. Lipids 20:915–920

    Article  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  Google Scholar 

  • Lamoreaux RJ, Chaney WR (1978) The effect of cadmium on net photosynthesis, transpiration, and dark respiration of excised silver maple leaves. Physiol Plant 43:231–236

    Article  CAS  Google Scholar 

  • Lance C, Rustin P (1984) The central role of malate in plant metabolism. Physiol Vég 22:625–641

    CAS  Google Scholar 

  • Laporte MM, Shen B, Tarczynski MC (2002) Engineering for drought avoidance: expression of maize NADP-malic enzyme in tobacco results in altered stomatal function. J Exp Bot 53:699–705

    Article  CAS  Google Scholar 

  • León AM, Palma JM, Corpas FJ, Gómez M, Romero-Puertas MC, Chatterjee D et al (2002) Antioxidative enzymes in cultivars of pepper plants with different sensitivity to cadmium. Plant Physiol Biochem 40:813–820

    Article  Google Scholar 

  • Ling Q, Hong F (2009) Effects of Pb2+ on the structure and function of photosystem II of Spirodela polyrrhiza. Biol Trace Elem Res 129:251–260

    Article  CAS  Google Scholar 

  • Liu MQ, Yanai J, Jiang RF, Zhang F, McGrath SP, Zhao FJ (2008) Does cadmium play a physiological role in the hyperaccumulator Thlaspi caerulescens? Chemosphere 71:1276–1283

    Article  CAS  Google Scholar 

  • Liu N, Lin ZF, Lin GZ, Song LY, Chen SW, Mo H et al (2010) Lead and cadmium induced alterations of cellular functions in leaves of Alocasia macrorrhiza L. Schott. Ecotoxicol Environ Saf 73:1238–1245

    Article  CAS  Google Scholar 

  • Lösch R (2004) Plant mitochondrial respiration under the influence of heavy metals. In: Prasad MNV (ed) Heavy metal stress in plants: from biomolecules to ecosystems, 2nd edn. Springer, Berlin, pp 182–200

    Chapter  Google Scholar 

  • Lyubenova L, Schröder P (2011) Plants for waste water treatment—effects of heavy metals on the detoxification system of Typha latifolia. Bioresour Technol 102:996–1004

    Article  CAS  Google Scholar 

  • Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13

    Article  CAS  Google Scholar 

  • Martinoia E, Rentsch D (1994) Malate compartmentation—responses to a complex metabolism. Annu Rev Plant Physiol Plant Mol Biol 45:447–467

    Article  CAS  Google Scholar 

  • Martinoia E, Maeshima M, Neuhaus HE (2007) Vacuolar transporters and their essential role in plant metabolism. J Exp Bot 58:83–102

    Article  CAS  Google Scholar 

  • Mattioni C, Gabbrielli R, Vangronsveld J, Clijsters H (1997) Nickel and cadmium toxicity and enzymatic activity in Ni-tolerant and non-tolerant populations of Silene italica Pers. J Plant Physiol 150:173–177

    Article  CAS  Google Scholar 

  • Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cell. Proc Natl Acad Sci USA 96:8271–8276

    Article  CAS  Google Scholar 

  • Nicito FF, Espen L, Crema B, Cocucci M, Sacchi GA (2008) Cadmium induces acidosis in maize root cells. New Phytol 17:700–711

    Article  Google Scholar 

  • Olko A, Abratowska A, Żyłkowska J, Wierzbicka M, Tukiendorf A (2008) Armeria maritima from a calamine heap–initial studies on physiologic–metabolic adaptations to metal-enriched soil. Ecotoxicol Environ Saf 69:209–218

    Article  CAS  Google Scholar 

  • Parys E, Romanowska E (2000) Relationship between postillumination burst of CO2 and enhancement of respiration in tall fescue leaves. Acta Physiol Plant 22:135–142

    Article  Google Scholar 

  • Parys E, Romanowska E, Siedlecka M, Poskuta JW (1998) The effect of lead on photosynthesis and respiration in detached leaves and in mesophyll protoplasts of Pisum sativum. Acta Physiol Plant 20:313–322

    Article  CAS  Google Scholar 

  • Piechalak A, Tomaszewska B, Barałkiewicz D (2003) Enhancing phytoremediative ability of Pisum sativum by EDTA application. Phytochemistry 64:1239–1251

    Article  CAS  Google Scholar 

  • Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73:149–156

    Article  CAS  Google Scholar 

  • Rasmusson AG, Fernie AR, van Dongen JT (2009) Alternative oxidase: a defence against metabolic fluctuations? Physiol Plant 137:371–382

    Article  CAS  Google Scholar 

  • Roelfsema MRG, Hedrich R (2005) In the light of stomatal opening: new insights into “the Watergate”. New Phytol 167:665–691

    Article  CAS  Google Scholar 

  • Romanowska E, Igamberdiev AU, Parys E, Gardeström P (2002) Stimulation of respiration by Pb2+ in detached leaves and mitochondria of C3 and C4 plants. Physiol Plant 116:148–154

    Article  CAS  Google Scholar 

  • Romanowska E, Wasilewska W, Fristedt R, Vener AV, Zienkiewicz M (2012) Phosphorylation of PSII proteins in maize thylakoids in the presence of Pb ions. J Plant Physiol 169:345–352

    Article  CAS  Google Scholar 

  • Sakano K (2001) Metabolic regulation of pH in plant cells: role of cytoplasmic pH in defence reaction and secondary metabolism. Int Rev Cytol 206:1–44

    Article  CAS  Google Scholar 

  • Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V et al (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6:2180–2198

    Article  CAS  Google Scholar 

  • Scheibe R (2004) Malate valves to balance cellular energy supply. Physiol Plant 120:21–26

    Article  CAS  Google Scholar 

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    Article  Google Scholar 

  • Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52

    Article  CAS  Google Scholar 

  • Smeets K, Cuypers A, Lambrechts A, Semane B, Hoet P, Van Laere A et al (2005) Induction of oxidative stress and antioxidative mechanisms in Phaseolus vulgaris after Cd application. Plant Physiol Biochem 43:437–444

    Article  CAS  Google Scholar 

  • Smith AMO, Ratcliffe RG, Sweetlove JL (2004) Activation and function of mitochondrial uncoupling protein in plants. J Biol Chem 279:51944–51952

    Article  CAS  Google Scholar 

  • Szarek-Łukaszewska G, Słysz A, Wierzbicka M (2004) Response of Armeria maritima (Mill.) Willd. to Cd, Zn and Pb. Acta Biol Cracov Ser Bot 46:19–24

    Google Scholar 

  • Taylor NL, Day DA, Millar AH (2004) Targets of stress-induced oxidative damage in plant mitochondria and their impact on cell carbon/nitrogen metabolism. J Exp Bot 55:1–10

    Article  CAS  Google Scholar 

  • Vallee BL, Ulmer DD (1972) Biochemical effects of mercury, cadmium and lead. Annu Rev Biochem 41:91–128

    Article  CAS  Google Scholar 

  • van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206

    Article  Google Scholar 

  • van Dongen JT, Gupta KJ, Ramírez-Aguilar SJ, Araújo WL, Nunes-Nesi A, Fernie AR (2011) Regulation of plant respiration: a role for alternative metabolic pathways. J Plant Physiol 168:1434–1443

    Article  Google Scholar 

  • Verdoni N, Mench M, Cassagne C, Bessoule JJ (2001) Fatty acid composition of tomato leaves as biomarkers of metal-contaminated soils. Environ Toxicol Chem 20:382–388

    Article  CAS  Google Scholar 

  • Wang X, Ze Y, Wu X, Chen L, Huang H, Liu J et al (2009) Effect of Pb2+ on the kinetic and spectral characterization of ribulose-1,5-bisphosphate carboxylase/oxygenase. Chin J Chem 27:727–731

    Article  CAS  Google Scholar 

  • Yadov SK (2010) Heavy metal toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179

    Article  Google Scholar 

  • Yamauchi Y, Furutera A, Seki K, Toyoda Y, Tanaka K, Sugumito Y (2008) Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat-stressed plants. Plant Physiol Biochem 46:786–793

    Article  CAS  Google Scholar 

  • Yang HM, Zhang HY, Wang GX (2004) Effects of heavy metals on stomatal movements in broad bean leaves. Russ J Plant Physiol 51:516–520

    Article  Google Scholar 

  • Yang HM, Zhang HY, Tang QL, Wang GX (2006) Extracellular calcium is involved in stomatal movement through the regulation of water channels in broad bean. Plant Growth Regul 50:79–83

    Article  CAS  Google Scholar 

  • Yoshimura Y, Kubota F, Ueno O (2004) Structural and biochemical bases of photorespiration in C4 plants: quantification of organelles and glycine decarboxylase. Planta 220:307–317

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Grant No. NN 303 393636 from the Polish Ministry of Science and Higher Education. We thank E. Przedpełska-Wąsowicz and B. Wróblewska for help with antioxidant determination.

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Authors and Affiliations

  1. Department of Molecular Plant Physiology, Faculty of Biology, Warsaw University, Miecznikowa 1, 02 096, Warsaw, Poland

    Eugeniusz Parys, Wioleta Wasilewska, Maria Siedlecka, Maksymilian Zienkiewicz, Anna Drożak & Elżbieta Romanowska

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  1. Eugeniusz Parys
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  2. Wioleta Wasilewska
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  3. Maria Siedlecka
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  6. Elżbieta Romanowska
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Correspondence to Elżbieta Romanowska.

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Parys, E., Wasilewska, W., Siedlecka, M. et al. Metabolic Responses to Lead of Metallicolous and Nonmetallicolous Populations of Armeria maritima . Arch Environ Contam Toxicol 67, 565–577 (2014). https://doi.org/10.1007/s00244-014-0057-z

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