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Phosphorus and cadmium interactions in Kandelia obovata (S. L.) in relation to cadmium tolerance

Abstract

This study focused on the cadmium (Cd) tolerance of mangroves with application of phosphate (P) in order to explore whether exogenous P can alleviate Cd stress on these intertidal species. Kandelia obovata (S. L.) seedlings were cultivated in rhizoboxes under different levels of Cd and P concentrations. The speciation distributions of Cd in the rhizosphere and non-rhizosphere sediments were examined by sequential extraction procedures; organic acid in plant tissues and soil solution was measured by high-performance liquid chromatography; Cd and P accumulation in the plants was also determined. Results showed that considerable differences existed in Cd speciation distributions between rhizosphere and non-rhizosphere sediments. Root activity influenced the dynamics of Cd, P application increased the organic acid content in root tissues, P also increased Cd accumulation in roots whilst lowering Cd translocation from root to the above-ground tissues, and a significant positive correlation was found between Cd and P in roots (r = 0.905). It is postulated that Cd detoxification of K. obovata (S. L.) is associated with higher Cd immobilization in the presence of higher P and organic acid contents in root tissue.

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References

  • Boto KG, Wellington JT (1983) Phosphorus and nitrogen nutritional status of a northern Australian mangrove forest. Mar Ecol Prog Ser 11:63–69

    Article  Google Scholar 

  • Bravin M, Martí A, Clairotte M, Hinsinger P (2009) Rhizosphere alkalisation—a major driver of copper bioavailability over a broad pH range in an acidic, copper contaminated soil. Plant Soil 318:257–268

    Google Scholar 

  • Brown SL, Chaney RL, Hallfrisch J, Ryan JA, Berti WR (2004) In situ soil treatments to reduce the phyto- and bioavailability of lead, zinc, and cadmium. J Environ Qual 33:522–31

    CAS  Article  Google Scholar 

  • Cawthray GR (2003) An improved reversed-phase liquid chromatographic method for the analysis of low-molecular mass organic acids in plant root exudates. J Chromatogr A 1011:233–240. doi:10.1016/j.bbr.2011.03.031

    CAS  Article  Google Scholar 

  • Cecile B, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    Article  Google Scholar 

  • Chang K, Roberts JK (1989) Observation of cytoplasmic and vacuolar malate in maize root-tips by 13C-NMR spectroscopy. Plant Physiol 89:197–203

    CAS  Article  Google Scholar 

  • Chang K, Roberts JK (1991) Cytoplasmic malate levels in maize root-tips during KC ion uptake determined by 13C-NMR spectroscopy. Biochim Biophys Acta 1092:29–34

    CAS  Article  Google Scholar 

  • Christensen TH (1984) Cadmium soil sorption at low concentrations: II. Reversibility, effect of changes in solute composition, and effect of soil aging. Water, Air Soil Pollut 21:115–125

    CAS  Article  Google Scholar 

  • Cotter HJ, Capron S (1996) Remediation of contaminated land by formation of heavy metal phosphates. Appl Geochem 11:335–342

    Article  Google Scholar 

  • David JL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44

    Article  Google Scholar 

  • De Wolf H, Rashid R (2008) Heavy metal accumulation in Littoraria scabra along polluted and pristine mangrove areas of Tanzania. Environ Pollut 152:636–43

    Article  Google Scholar 

  • Dinkelaker B, Römheld V, Marschner H (1989) Citric-acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ 12:285–292

    CAS  Article  Google Scholar 

  • di Toppi LS, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Article  Google Scholar 

  • Dong J, Mao WH, Zhang GP, Wu FB, Cai Y (2007) Root excretion and plant tolerance to cadmium toxicity—a review. Plant Soil Environ 53:193–200

    CAS  Google Scholar 

  • Ernst WHO, Verkleij JAC, Schat H (1992) Metal tolerance in plants. Acta Bot Neerl 41:229–248

    CAS  Google Scholar 

  • Feller IC (1995) Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecol Monogr 65:477–505

    Article  Google Scholar 

  • Feller IC, Whigham DF, O’Neill JP, McKee KM (1999) Effects of nutrient enrichment on within-stand nutrient cycling in mangrove ecosystems in Belize. Ecology 80:2193–2205

    Article  Google Scholar 

  • Gadapati WR, Macfie SM (2006) Phytochelatins are only partially correlated with Cd-stress in two species of Brassica. Plant Sci 170:471–480

    CAS  Article  Google Scholar 

  • Galal-Gorchev H (1993) Dietary intake, levels in food and estimated intake of lead, cadmium, and mercury. Food Addit Contam 10:115–128

    CAS  Article  Google Scholar 

  • Gao XP et al (2011) Soil solution dynamics and plant uptake of cadmium and zinc by durum wheat following phosphate fertilization. Plant Soil 338:423–434

    CAS  Article  Google Scholar 

  • Gerke J (1992) Phosphate, aluminum and iron in the soil solution of three different soils in relation to varying concentrations of citric acid. Z Pflanzenernähr Bodenk 155:339–343

    CAS  Article  Google Scholar 

  • Giesler R, Lundstron U (1993) Soil solution chemistry: effect of bulking soil sample. Soil Sci Soc Am J 57:1283–1288

    CAS  Article  Google Scholar 

  • Gonçalves JF, Antes G et al (2009) Cadmium and mineral nutrient accumulation in potato plantlets grown under cadmium stress in two different experimental culture conditions. Plant Physiol Biochem 47:814–821

    Article  Google Scholar 

  • Gout E, Bligny R, Pascal N, Douce R (1993) 13C nuclear magnetic- resonance studies of malate and citrate synthesis and compartmentation in higher-plant cells. J Biol Chem 268:3986–92

    CAS  Google Scholar 

  • Hinsinger P (2001) Trace elements in the rhizosphere. In: Gobran GR, Wenzel WW, Lombi E (eds) Bioavailability of trace elements as related to root induced chemical changes in the rhizosphere. CRC Press, Boca Raton, p 25

    Google Scholar 

  • Hinsinger P, Plassard C, Jaillard B (2006) Rhizosphere: a new frontier for soil biogeochemistry. J Geochem Explor 88:210–213

    CAS  Article  Google Scholar 

  • Jeanjean J, Vincent U, Fedoroff M (1994) Structural modification of calcium hydroxyapatite induced by sorption of cadmium ions. J Solid State Chem 108:68–72

    CAS  Article  Google Scholar 

  • Jones DL, Dennis PG, Owen AG, Van Hees PAW (2003) Organic acid behavior in soils—misconceptions and knowledge gaps. Plant Soil 248:31–41

    CAS  Article  Google Scholar 

  • Jones DL, Edwards AC (1998) Influence of sorption on the biological utilization of two simple carbon substrates. Soil Biol Biochem 30:1895–1902

    CAS  Article  Google Scholar 

  • Kabata-Pendias A, Pendias H (1992) Trace elements in soils and plants, 3rd edn. CRC Press, London

    Google Scholar 

  • Kirk GJD (2004) The biogeochemistry of submerged soils. In The Biogeochemistry of Submerged Soils. pp i–xi

  • Krishnamurti GSR, Cieslinski G, Huang PM, Van Rees KCJ (1997) Kinetics of cadmium release from soil as influenced by organics acids: implication in cadmium availability. J Environ Qual 26:271–277

    CAS  Article  Google Scholar 

  • Krzyszowska AJ, George FV, Michael JB, Mark BD (1996) Ion-chromatographic analysis of low molecular weight organic acids in Spodosol forest floor solutions. Soil Sci Soc Am J 60:1565–1571

    CAS  Article  Google Scholar 

  • Lacerda LD, Carvalho CEV, Tanizaki KF, Ovalle AR, Rezende CE (1993) The biogeochemistry and trace metals distribution of mangrove rhizospheres. Biotropica 25:252–257

    Article  Google Scholar 

  • Lan M, Comerford NB, Fox TR (1995) Organic anions effect on phosphorus release from spodic horizons. Soil Sci Soc Am J 59:1745–1749

    CAS  Article  Google Scholar 

  • Laperche V, Traina SJ (1998) Adsorption of metals by Geomedia: variables, mechanisms, and model applications. Academic Press, pp 255–275

  • Liao H, Wan HY et al (2006) Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance. exudation of specific organic acids from different regions of the intact root system1[W]. Plant Physiol 141:674–684. doi:10.1104/pp.105.076497

    CAS  Article  Google Scholar 

  • Lin P (1999) Mangrove ecosystem in China. Science Press, Beijing, pp 297–316

    Google Scholar 

  • Liu JC, Yan CL et al (2006) Distribution and speciation of some metals in mangrove sediments from Jiulong River estuary, People's Republic of China. Bull Environ Contam Toxicol 76:815–22

    Article  Google Scholar 

  • Loneragan JF, Grove TS, Robson AD, Snowball K (1979) Phosphorus toxicity as a factor in zinc phosphorus interactions in plants. Soil Sci Soc Am J 43:966–972

    CAS  Article  Google Scholar 

  • Lu RK (1999) Chemistry analysis methods of soil and agriculture. Agricultural Science Publishing House, Beijing

    Google Scholar 

  • Lu HL, Yan CL, Liu JC (2007) Low-molecular-weight organic acids exuded by mangrove (Kandelia candel (L.) Druce) roots and their effect on cadmium species change in the rhizosphere. Environ Exp Bot 61:159–166

    CAS  Article  Google Scholar 

  • Ma LQ, Rao GN (1997) Chemical fractionation of cadmium, copper, nickel and zinc in contaminated soils. J Environ Qual 26:259–264

    CAS  Article  Google Scholar 

  • Ma JF, Hiradate S, Matsumoto H (1998) High aluminum resistance in buck wheat. II. Oxalic acid detoxifies aluminum internally. Plant Physiol 117:753–759

    CAS  Article  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic, London

    Google Scholar 

  • Meach M, Martin E (1991) Mobilization of cadmium and other metals from two soils by root exudates of Zea mays L., Nicotiana tabacum L. and Nicotiana rustica L. Plant Soil 132:187–196

    Google Scholar 

  • Miller A, Cramer M (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36

    Google Scholar 

  • Millet M, Wortham H, Sanusi A, Mirabel P (1997) Low molecular weight organic acids in fogwater in an urban area: Strasbourg (France). Sci Tot Env 206:57–65

    CAS  Article  Google Scholar 

  • Nahakpam S, Shah K (2011) Expression of key antioxidant enzymes under combined effect of heat and cadmium toxicity in growing rice seedlings. Plant Growth Regul 63:23–35

    CAS  Article  Google Scholar 

  • Naidu R, Harter RD (1998) Effect of different organic ligands on cadmium sorption and extractability from soils. Soil Sci Soc Am J 62:644–650

    CAS  Article  Google Scholar 

  • Nakayama E (1981) Chemical speciation of chromium sea water: effect of naturally occurring organic materials on the complex formation of chromium III. Anal Chim Acta 130:289–294

    CAS  Article  Google Scholar 

  • Nedjimi B, Daoud Y (2009) Cadmium accumulation in Atriplex halimus subsp.schweinfurthii and its influence on growth, proline, root hydraulic conductivity and nutrient uptake. Flora 204:316–324

    Article  Google Scholar 

  • Nieboer E, Richardson DHS (1980) The replacement of the nondescript term “heavy metals” by a biologically and chemically significant classification of metal ions. Environ Pollut (Series B) 1:3–26

    CAS  Article  Google Scholar 

  • Norby RJ, Jackson RB (2000) Root dynamics and global change: seeking an ecosystem perspective. New Phytol 147:3–12

    CAS  Article  Google Scholar 

  • Obata H, Umebayashi M (1997) Effects of cadmium on mineral nutrient concentrations in plants differing in tolerance for cadmium. J Plant Nutrition 20:97–105. doi:10.1080/01904169709365236

    CAS  Article  Google Scholar 

  • Osmond CB (1976) Ion absorption and carbon metabolism in cells of higher plants. In: Lüttge U, Pitman MG (eds) Encyclopedia of plant physiology, new series, vol 2, part A. Springer, Berlin, pp 347–372

    Google Scholar 

  • Osmond CB, Laties GG (1969) Compartmentation of malate in relation to ion absorption in beet. Plant Physiol 44:7–14

    CAS  Article  Google Scholar 

  • Pierzynski GM, Hettiarachchi GM (2002) Method for in-situ immobilization and reduction of metal bioavailability in contaminated soils, sediments, and wastes. U.S. Patent No. 6383128

  • Pohlman AA, McColl JG (1986) Kinetics of metal dissolution from forest soils by soluble organic acids. J Environ Qual 15:86–92

    CAS  Article  Google Scholar 

  • Rauser WE, Ackerley CA (1987) Localization of cadmium in granules within differentiating and mature root cells. Can J Bot 65:643–646

    CAS  Article  Google Scholar 

  • Renella G, Mench M (2004) Hydrolase activity, microbial biomass and community structure in long-term Cd-contaminated soils. Soil Biol Biochem 36:443–451

    CAS  Article  Google Scholar 

  • Rezvani M, Zaefarian F, Miransari M, Nemat- Zadeh GA (2011) Uptake and translocation of cadmium and nutrients by Aeluropus littoralis. Arch Agron Soil Sci 58:1413–1425

    Article  Google Scholar 

  • Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Mol Biol 52:527–560

    CAS  Article  Google Scholar 

  • Sauvé S, Hendershot W, Allen HE (2000) Solid-solution partitioning of metals in contaminated soils: dependence on pH, total metal burden, and organic matter. Environ Sci Technol 34:1125–1131

    Google Scholar 

  • Schwab AP, Zhu DS, Banks MK (2008) Influence of organic acids on the transport of heavy metals in soil. Chemosphere 72:986–994

    CAS  Article  Google Scholar 

  • Sparrow LA, Salardini AA, Bishop AC et al (1993) Field studies of cadmium in potatoes (Solanum tuberosum L) II. Response of cvv. Russet and Kennebec to two double superphophates of different cadmium concentration [J]. A ust J A gric Res 44:855–861

    CAS  Article  Google Scholar 

  • Strobel BW (2001) Influence of vegetation on low-molecular-weight carboxylic acids in soil solution—a review. Geoderma 99:169–198

    CAS  Article  Google Scholar 

  • Strom L, Owen AG, Godbold DL, Jones DL (2002) Organic acid mediated P mobilization in the rhizosphere and uptake by maize roots. Soil Biol Biochem 34:703–710

    CAS  Article  Google Scholar 

  • Sun JY, Shen ZG (2007) Effects of Cd stress on photosynthetic characteristics and nutrient uptake of cabbages with different Cd-tolerance. Chin J Appl Ecol 18:2605–10

    CAS  Google Scholar 

  • Tessier A, Campbell PGC, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51:844–851

    CAS  Article  Google Scholar 

  • Verkleij JA, Schat H (1990) Mechanisms of metal tolerance in higher plants. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Boca Raton, pp 179–94

    Google Scholar 

  • Wang BL, Xie ZM (2008) Influence of phosphorus on the transform and translocation of lead, zinc and cadmium in the soil-plant system. Environ Sci 29:3225–322 (In Chinese)

    CAS  Google Scholar 

  • Wang J (1991) Computer-simulated evaluation of possible mechanisms for quenching heavy metal ion activity in plant vacuoles. Plant Physiol 97:1154–1160

    CAS  Article  Google Scholar 

  • Wojcik M, Vangronsveld J, Tukiendorf A (2005) Cadmium tolerance in Thlaspi caerulescens—I. Growth parameters, metal accumulation and phytochelatin synthesis in response to cadmium. Environ Exp Bot 53:151–161

    CAS  Google Scholar 

  • Xie XY, Weiss DJ et al (2012) The short-term effect of cadmium on low molecular weight organic acid and amino acid exudation from mangrove (Kandelia obovata (S. L.) Yong) roots. Environ Sci Pollut Res. doi:10.1007/s11356-012-1031-9

    Google Scholar 

  • Xu Y, Schwartz FW (1994) Lead immobilization by hydroxyapatite in aqeous solutions. J Contam Hydrol 15:187–206

    CAS  Article  Google Scholar 

  • Zwonitzer J, Pierzynski GM, Hettiarachchi GM (2003) Effects of phosphorus additions on lead, cadmium, and zinc bioavailabilities in a metal-contaminated soil. Water Air Soil Pollut 143:193–209

    CAS  Article  Google Scholar 

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Acknowledgments

This work was jointly supported by the National Important Scientific Research Program of China (2013CB956504) and National Natural Science Foundation of China (31170471, 30970527). The authors would like to thank Prof. John Merefield for assistance with English grammar.

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Correspondence to Chongling Yan.

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Responsible editor: Elena Maestri

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Du, J., Yan, C. & Li, Z. Phosphorus and cadmium interactions in Kandelia obovata (S. L.) in relation to cadmium tolerance. Environ Sci Pollut Res 21, 355–365 (2014). https://doi.org/10.1007/s11356-013-1910-8

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  • DOI: https://doi.org/10.1007/s11356-013-1910-8

Keywords

  • Cadmium
  • Phosphorus
  • Organic acid
  • Mangrove
  • Rhizosphere