Abstract
We investigated responses of Lemna gibba L. to exposure to UO2 2+ and AsO4 3− under variable PO4 3− concentration. Total plant phosphorus (Ptot) in L. gibba and accumulation of dissolved organic carbon (DOC) in the media were quantified and tested for correlation with plant yield and initial concentrations of PO4 3−, UO2 2+ and AsO4 3−. The accumulation of DOC in medium was high under low PO4 3− supply and increased loading of either UO2 2+ or AsO4 3−. The Ptot was low in high initial concentration of UO2 2+ and AsO4 3− as well under acute low PO4 3− supply. The DOC accumulation correlated negatively to the Ptot. This reveals interaction between PO4 3− and UO2 2+ or AsO4 3− in the medium interferes with the uptake process of PO4 3−. Hence, the DOC accumulation is exudation of low molecular weight organic substance by L. gibba in response to the reduced Ptot: biomass ratio (carbon in the yield) due to delimited acquisition of phosphorus from the medium. It is a homeostatic regulation of the stoichiometry, which is disturbed during the interaction between PO4 3− and UO2 2+ or AsO4 3−. Further investigations are necessary to relate these interactions to traditional resource stoichiometry elements of C, N, and P.
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References
Abbas HK, Gronwald JW, Plaisance KL, Paul RN, Lee YW (2001) Histone deacetylase activity and phytotoxic effects following exposure of duckweed (Lemna pausicostata L.) to apicidin and HC-toxin. Phytopathology 91(12):1141–1148
Abedin MDJ, Cresser MS, Maharg AA, Feldmann J, Cotter-hower J (2002a) Arsenic accumulation and metabolism in rice (Oryza sativa L.). Environ Sci Technol 36:962–968
Abedin MDJ, Feldmann J, Maharg AA (2002b) Uptake kinetics of arsenic species in rice plants. Plant Physiol 128:1120–1128
Arosio P, Levi S (2002) Ferritin, iron homeostasis, and oxidative damage. Free Radic Biol Med 33(4):457–463
Bowker DW, Duffield AN, Denny P (1980) Methods for the isolation, sterilization and cultivation of Lemnaceae. Freshw Biol 10:385–388
Bozzo GG, Raghothama KG, Plaxton WC (2002) Purification and characterization of two secreted purple acid phosphatase isozymes from phosphate-starved tomato (Lycopersicon esculentum) cell cultures. Eur J Biochem 269(24):6278–6286
Briat J-F, Lebrun M (1999) Plant responses to metal toxicity. Comptes Rendus de l’Academie des Sciences—Series III—Sciences de la Vie 322(1):43–54
Caussy D (2003) Case studies of the impact of understanding bioavailability: arsenic. Ecotoxicol Environ Saf 56(1):164–173
Chiang P-N, Wang MK, Chiu CY, Chou S-Y (2006) Effects of cadmium amendments on low-molecular-weight organic acid exudates in rhizosphere soils of tobacco and sunflower. Environ Toxicol 21(5):479–488
Clemens S (2003) Molekulare Mechanismen der Aufnahme, Detoxifizierung und Akkumulation von Metallen. Martin-Luther-Universität Halle-Wittenberg, Halle
Cobbett C (2003) Heavy metals and plants—model systems and hyperaccumulators. New Phytol 159(2):289–293
Crichton RR (1995) Metal homeostasis at the cellular and molecular level. J Inorg Biochem 59(2–3):96
Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47
Desbrosses-Fonrouge A-G, Voigt K, Schröder A, Arrivault S, Thomine S, Krämer U (2005) Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Lett 579(19):4165–4174
Ebbs SD, Brady DJ, Kochian LV (1998) Role of uranium speciation in the uptake and translocation of uranium by plants. J Exp Bot 49:1183–1190
Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LW (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3(6):540–550
Elvira E, Carpena RO, Meharg AA (2003) High-affinity phosphate/arsenate transport in white lupin (Lupinus albus) is relatively insensitive to phosphate status. New Phytol 158:165–173
Finlay JA, Allan VJM, Conner A, Callow ME, Basnakova G, Macaskie LE (1999) Phosphate release and heavy metal accumulation by biofilm-immobilized and chemically-coupled cells of a Citrobacter sp. pre-grown in continuous culture. Biotechnol Bioeng 63(1):87–97
Fitz WJ, Wenzel WW, Zhang H, Nurmi J, Stipek K, Fischerova Z, Schweiger P, Köllensperger G, Ma LQ, Stingeder G (2003) Rhizosphere characteristics of the arsenic hyperaccumulator Pteris vittata L. and monitoring of phytoremoval efficiency. Environ Sci Technol 37(21):5008–5014
Gilbert GA, Knight JD, Allan DL, Vance CP (1998) Acid phosphatase activity in phosphorous-deficient white lupin roots. United States Department of Agriculture Agricultural Research Service, Tekran
Greenberg BM, Huang X-D, Dixon DG (1992) Applications of the aquatic higher plant Lemna gibba for ecotoxicological assessment. J Aquat Ecosyst Health 1:147–155
Guo L, Warnken KW, Santschi PH (2007) Retention behavior of dissolved uranium during ultrafiltration: implications for colloidal U in surface waters. Mar Chem 107(2):156–166
Gurzau ES, Neagu C, Gurzau AE (2003) Essential metals—case study on iron. Ecotoxicol Environ Saf 56(1):190–200
Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237(2):173–195
Hütter LA (1992) Wasser und Wasseruntersuchung, 5th edn. OttoSalle Verlag, Frankfurt am Main
Kay AD, Rostampour S, Sterner RW (2006) Ant stoichiometry: elemental homeostasis in stage-structured colonies. Funct Ecol 20:1037–1044
Knight B, Zhao FJ, McGrath SP, Shen ZG (1997) 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. Plant Soil 197(1):71–78
Konieczynski P, Wesolowski M (2007) Total phosphorus and its extractable form in plant drugs. Interrelation with selected micro- and macroelements. Food Chem 103(1):210–216
Kraemer U (2003) Phytoremediation to phytochelatin—plant trace metal homeostasis. New Phytol 158(1):4–6
Kraemer U (2009) The dilemma of controlling heavy metal accumulation in plants. New Phytol 181(1):3–5
Krämer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581(12):2263–2272
Li XX, Franceschi VR (1990) Distribution of peroxisomes and glycolate metabolism in relation to calcium oxalate formation in Lemna minor L. Eur J Cell Biol 51:9–16
Mazen AMA, Zhang D, Franceschi VR (2004) Calcium oxalate formation in Lemna minor physiological and ultrastructural aspects of high capacity calcium sequestration. New Phytol 161(2):435–448
Meharg AM, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Physiol 154:29–43
Meharg AA, Macnair MR (1992) Suppression of the phosphate uptake system: a mechanism of arsenate tolerance in Holcus lanatus. J Exp Bot 43:519–524
Mkandawire M, Dudel EG (2005) Assignment of Lemna gibba L. (duckweed) bioassay for in situ ecotoxicity assessment. Aquat Ecol 39:151–165
Mkandawire M, Lyubun YV, Kosterin PV, Dudel EG (2004) Toxicity of arsenic species to Lemna gibba L. and influence of phosphate on arsenic bioavailability. Environ Toxicol 19(1):26–35
Mkandawire M, Vogel K, Taubert B, Dudel EG (2007) Phosphate regulates uranium(VI) toxicity to Lemna gibba L. G3. Environ Toxicol 22(1):9–16
Nakazato H, Okamoto T, Ishikawa K, Okuyama H (1997) Purification and characterization of phosphatase inducibly synthesized in Spirodela oligorrhiza grown under phosphate-deficient conditions. Plant Physiol Biochem 35(6):437–446
Nakazato H, Okamoto T, Nishikoori M, Washio K, Morita N, Haraguchi K, Thompson GA Jr, Okuyama H (1998) The glycosylphosphatidylinositol-anchored phosphatase from Spirodela oligorrhiza is a purple acid phosphatase. Plant Physiol 118(3):1015–1020
Palit S, Sharma A, Talukder G (1994) Effects of cobalt on plants. Bot Rev 60(2):149–181
Penuelas J, Sardans J (2009) Ecology: elementary factors. Nature 460(7257):803–804
Pulsawat W, Leksawasdi N, Rogers PL, Foster LJR (2003) Anions effects on biosorption of Mn(II) by extracellular polymeric substance (EPS) from Rhizobium etli. Biotechnol Lett 25(15):1267–1270
Ratkowsky DA, Sale PWG, Tennakoon SB, Johnson D, Simpson PG (1997) Models for pasture yield in response to phosphate application. Aust J Exp Agric 37(8):905–912
Rufyikiri G, Thiry Y, Declerck S (2003) Contribution of hyphae and roots to uranium uptake and translocation by arbuscular mycorrhizal carrot roots under root-organ culture conditions. New Phytol 158(2):391–399
Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University, Princeton
Tu S, Ma L, Luongo T (2004) Root exudates and arsenic accumulation in arsenic hyperaccumulating Pteris vittata and non-hyperaccumulating Nephrolepis exaltata. Plant Soil 258(1):9–19
Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181(4):759–776
Wang Z, Zhang S, Shan X-Q (2004) Effects of low-molecular-weight organic acids on uptake of lanthanum by wheat roots. Plant Soil 261(1):163–170
Wasaki J, Ando M, Ozawa K, Omura M, Osaki M, Ito H, Matsui H, Tadano T (1997) Properties of secretory acid phosphatase from lupin roots under phosphorus-deficient conditions. Soil Sci Plant Nutr 43:981–986
Yu JQ, Matsui Y (1997) Effects of root exudates of cucumber (Cucumis sativus) and allelochemicals on ion uptake by cucumber seedlings. J Chem Ecol 23(3):817–827
Zenk MH (1996) Heavy metal detoxification in higher plants—a review. Gene 179(1):21–30
Zhang C, McManus M (2000) Identification and characterization of two distinct acid phosphatases in cell walls of white clover. Plant Physiol Biochem 38:259–270
Acknowledgment
The study was done partially under the frameworks of BMBF Project grant 02WB0222 and NATO Project grant EST CLG 980821. PD Dr. Martin Mkandawire is very grateful to support and guidance from Prof. Dr. Wolfgang Pompe. Dr. Barbara Darr and Mr. Carsten Müller worked on the initial investigation of DOC exudation with Lemna gibba.
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Mkandawire, M., Gert Dudel, E. Homeostatic regulation of elemental stoichiometry by Lemna gibba L. G3 when nutrient interact with toxic metals. Ecotoxicology 21, 456–464 (2012). https://doi.org/10.1007/s10646-011-0805-z
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DOI: https://doi.org/10.1007/s10646-011-0805-z