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The short-term effect of cadmium on low molecular weight organic acid and amino acid exudation from mangrove (Kandelia obovata (S., L.) Yong) roots

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Abstract

The aim of this study was to evaluate short-term concentration and time effects of cadmium on Kandelia obovata (S., L.) Yong root exudation, thereby evaluating and predicting the ecophysiological effects of mangrove to heavy metals at the root level. Mature K. obovata propagules were cultivated in a sandy medium for 3 months, and then six concentrations of Cd (0, 2.5, 5, 10, 20, and 40 mg L−1) were applied. After exposure time of 24 h and 7 days, respectively, the root exudates of K. obovata were collected and low molecular weight organic acids (LMWOAs) and amino acids of which were analyzed. In addition, we measured glutathione, soluble protein content, and Cd concentration in the plant. We found 10 and 15 types of LMWOAs and amino acids in root exudates of K. obovata with total concentrations ranging from 29.54 to 43.08 mg g−1 dry weight (DW) roots and from 737.35 to 1,452.46 ng g−1 DW roots, respectively. Both of them varied in quality and quantity under different Cd treatment strengths and exposure times. Oxalic, acetic, l-malic, tartaric acid, tyrosine, methionine, cysteine, isoleucine, and arginine were dominant. Both LMWOAs and amino acids excreted from K. obovata roots play a key role in Cd toxicity resistance. The responsiveness of amino acids was less than that of LMWOAs. We suggest that the ecological effect of root-excreted free amino acids in the rhizosphere is mainly based on the role of nutrients, supplemented with detoxification to heavy metals.

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References

  • Boominathan R, Doran PM (2003) Organic acid complexation, heavy metal distribution and the effect of ATPase inhibition in hairy roots of hyperaccumulator plant species. J Biotechnol 101(2):131–146

    Article  CAS  Google Scholar 

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

    Article  CAS  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(1–2):233–240

    CAS  Google Scholar 

  • Chen MC, Wang MK, Chiu CY, Huang PM, King HB (2001) Determination of low molecular weight dicarboxylic acids and organic functional groups in rhizosphere and bulk soils of Tsuga and Yushania in a temperate rain forest. Plant Soil 231(1):37–44

    Article  CAS  Google Scholar 

  • Clemens S, Palmgren MG, Kramer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7(7):309–315

    Article  CAS  Google Scholar 

  • Cobbett CS (2000) Phytochelatin biosynthesis and function in heavy-metal detoxification. Curr Opin Plant Biol 3(3):211–216

    CAS  Google Scholar 

  • Curl EA, Truelove B (1986) The rhizosphere. Springer, New York

    Book  Google Scholar 

  • Defew LH, Mair JM, Guzman HM (2005) An assessment of metal contamination in mangrove sediments and leaves from Punta Mala Bay, Pacific Panama. Mar Pollut Bull 50(5):547–552

    Article  CAS  Google Scholar 

  • di Toppi LS, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41(2):105–130

    Article  Google Scholar 

  • Diaz-Cruz MS, Mendieta J, Monjonell A, Tauler R, Esteban M (1998) Study of the zinc-binding properties of glutathione by differential pulse polarography and multivariate curve resolution. J Inorg Biochem 70(2):91–98

    Article  CAS  Google Scholar 

  • Dixon DP, Cummins I, Cole DJ, Edwards R (1998) Glutathione-mediated detoxification systems in plants. Curr Opin Plant Biol 1(3):258–266

    Article  CAS  Google Scholar 

  • Duarte B, Delgado M, Cacador I (2007) The role of citric acid in cadmium and nickel uptake and translocation, in Halimione portulacoides. Chemosphere 69(5):836–840

    Article  CAS  Google Scholar 

  • Gadapati W, Macfie S (2006) Phytochelatins are only partially correlated with Cd-stress in two species of Brassica. Plant Sci 170(3):471–480

    Article  CAS  Google Scholar 

  • Gonzalez-Mendoza D, Moreno AQ, Zapata-Perez O (2007) Coordinated responses of phytochelatin synthase and metallothionein genes in black mangrove, Avicennia germinans, exposed to cadmium and copper. Aquat Toxicol 83(4):306–314

    Article  CAS  Google Scholar 

  • Grayston SJ, Vaughan D, Jones D (1997) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5(1):29–56

    Article  Google Scholar 

  • Grill E, Winnacker EL, Zenk MH (1985) Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science 230(4726):674–676

    Article  CAS  Google Scholar 

  • Guo TR, Zhang GP, Zhou MX, Wu FB, Chen JX (2007) Influence of aluminum and cadmium stresses on mineral nutrition and root exudates in two barley cultivars. Pedosphere 17(4):505–512

    Article  CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53(366):1–11

    Article  CAS  Google Scholar 

  • Harbison P (1986) Mangrove muds—a sink and a source for trace metals. Mar Pollut Bull 17(6):246–250

    Article  CAS  Google Scholar 

  • Hissin PJ, Hilf R (1976) A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 74(1):214–226

    Article  CAS  Google Scholar 

  • Hoagland D, Arnon D (1950) The water culture method for growing plants without soil. Calif Agric Exp Station Circ 347(1):32

    Google Scholar 

  • Krishnamurti G, Cieslinski G, Huang P, Van Rees K (1997) Kinetics of cadmium release from soils as influenced by organic acids: implication in cadmium availability. J Environ Qual 26(1):271–277

    Article  CAS  Google Scholar 

  • Kuo Y, Lambein F, Ikegami F, Van Parijs R (1982) Isoxazolin-5-ones and amino acids in root exudates of pea and sweet pea seedlings. Plant Physiol 70(5):1283–1289

    Article  CAS  Google Scholar 

  • Lee K, Bae DW, Kim SH, Han HJ, Liu X, Park HC, Lim CO, Lee SY, Chung WS (2010) Comparative proteomic analysis of the short-term responses of rice roots and leaves to cadmium. J Plant Physio 167(3):161–168

    Article  CAS  Google Scholar 

  • Liu JC, Yan CL, Macnair MR, Hu J, Li YH (2006) Distribution and speciation of some metals in mangrove sediments from Jiulong River Estuary, People's Republic of China. Bull Environ Contam Toxicol 76(5):815–822

    Article  Google Scholar 

  • Liu Y, Tam NFY, Yang JX, Pi N, Wong MH, Ye ZH (2009) Mixed heavy metals tolerance and radial oxygen loss in mangrove seedlings. Mar Pollut Bull 58(12):1843–1849

    Article  CAS  Google Scholar 

  • Lobinski R, Potin-Gautier M (1998) Metals and biomolecules—bioinorganic analytical chemistry. Analusis Mag 26(6):M21–M24

    Article  CAS  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(2):159–166

    Article  CAS  Google Scholar 

  • Macfarlane GR, Burchett MD (2001) Photosynthetic pigments and peroxidase activity as indicators of heavy metal stress in the grey mangrove, Avicennia marina (Forsk.) Vierh. Mar Pollut Bull 42(3):233–240

    Article  CAS  Google Scholar 

  • MacFarlane G, Pulkownik A, Burchett M (2003) Accumulation and distribution of heavy metals in the grey mangrove, Avicennia marina (Forsk.) Vierh.: biological indication potential. Environ Pollut 123(1):139–151

    Article  CAS  Google Scholar 

  • Meier S, Alvear M, Borie F, Aguilera P, Ginocchio R, Cornejo P (2011) Influence of copper on root exudate patterns in some metallophytes and agricultural plants. Ecotoxicol Environ Saf 75:8–15

    Article  Google Scholar 

  • Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711–760

    Article  CAS  Google Scholar 

  • Mench 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(2):187–196

    CAS  Google Scholar 

  • Mucha AP, Almeida CMR, Bordalo AA, Vasconcelos MTSD (2005) Exudation of organic acids by a marsh plant and implications on trace metal availability in the rhizosphere of estuarine sediments. Estuarine Coastal Shelf Sci 65(1–2):191–198

    Article  CAS  Google Scholar 

  • Mucha AP, Almeida CMR, Bordalo AA, Vasconcelos M (2010) LMWOA (low molecular weight organic acid) exudation by salt marsh plants: natural variation and response to Cu contamination. Estuarine Coastal Shelf Sci 88(1):63–70

    Article  CAS  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(1):23–35

    Article  CAS  Google Scholar 

  • Nardi S, Concheri G, Pizzeghello D, Sturaro A, Rella R, Parvoli G (2000) Soil organic matter mobilization by root exudates. Chemosphere 41(5):653–658

    Article  CAS  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(4):316–324

    Article  Google Scholar 

  • Neumann G, Martinoia E (2002) Cluster roots—an underground adaptation for survival in extreme environments. Trends Plant Sci 7(4):162–167

    Article  CAS  Google Scholar 

  • Pohlmeier A (2004) Metal speciation, chelation and complexing ligands in plants. In: Prasad MNV (ed) Heavy metal stress in plants: from biomolecules to ecosystems. Springer, New Delhi

    Google Scholar 

  • Polle A, Schützendübel A (2004) Heavy metal signalling in plants: linking cellular and organismic responses. In: Hirt H, Shinozaki K (eds) Plant responses to abiotic stress. Springer, Berlin/Heidelberg, pp 187–215

  • Qin GQ, Yan CL, Lu HL (2007) Influence of heavy metals on the carbohydrate and phenolics in mangrove, Aegiceras corniculatum L., seedlings. Bull Environ Contam Toxicol 78(6):440–444

    Article  Google Scholar 

  • Renella G, Egamberdiyeva D, Landi L, Mench M, Nannipieri P (2006) Microbial activity and hydrolase activities during decomposition of root exudates released by an artificial root surface in Cd-contaminated soils. Soil Biol Biochem 38(4):702–708

    Article  CAS  Google Scholar 

  • Sandnes A, Eldhuset TD, Wollebaek G (2005) Organic acids in root exudates and soil solution of Norway spruce and silver birch. Soil Biol Biochem 37(2):259–269

    Article  CAS  Google Scholar 

  • Shah K, Dubey R (1998) A 18 kDa cadmium inducible protein complex: its isolation and characterisation from rice (Oryza sativa L.) seedlings. J Plant Physiol 152(4):448–454

    Article  CAS  Google Scholar 

  • Soudek P, Petrová S, Vanek T (2011) Heavy metal uptake and stress responses of hydroponically cultivated garlic (Allium sativum L.). Environ Exp Bot 74:289–295

    Article  CAS  Google Scholar 

  • Strobel BW, Bernhoft I, Borggaard OK (1999) Low-molecular-weight aliphatic carboxylic acids in soil solutions under different vegetations determined by capillary zone electrophoresis. Plant Soil 212(2):115–121

    Article  CAS  Google Scholar 

  • Strobel BW, Hansen HCB, Borggaard OK, Andersen MK, Raulund-Rasmussen K (2001) Composition and reactivity of DOC in forest floor soil solutions in relation to tree species and soil type. Biogeochemistry 56(1):1–26

    Article  CAS  Google Scholar 

  • Tam NFY, Wong YS (1996) Retention and distribution of heavy metals in mangrove soils receiving wastewater. Environ Pollut 94(3):283–291

    Article  CAS  Google Scholar 

  • Tam NFY, Wong YS (2000) Spatial variation of heavy metals in surface sediments of Hong Kong mangrove swamps. Environ Pollut 110(2):195–205

    Article  CAS  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(2):151–161

    CAS  Google Scholar 

  • Wong YS, Tam NFY, Chen GZ, Ma H (1997) Response of Aegiceras corniculatum to synthetic sewage under simulated tidal conditions. Hydrobiologia 352:89–96

    Article  CAS  Google Scholar 

  • Wu FB, Zhang GP (2002) Genotypic variation in kernel heavy metal concentrations in barley and as affected by soil factors. J Plant Nutr 25(6):1163–1173

    Article  CAS  Google Scholar 

  • Xu WH, Liu H, Ma QF, Xiong ZT (2007) Root exudates, rhizosphere Zn fractions, and Zn accumulation of ryegrass at different soil Zn levels. Pedosphere 17(3):389–396

    Article  CAS  Google Scholar 

  • Youssef R, Chino M (1989) Root-induced changes in the rhizosphere of plants, 1: pH changes in relation to the bulk soil. Soil Sci Plant Nutr 35(3):461–468

    Article  Google Scholar 

  • Zeng FR, Chen S, Miao Y, Wu FB, Zhang GP (2008) Changes of organic acid exudation and rhizosphere pH in rice plants under chromium stress. Environ Pollut 155(2):284–289

    Article  CAS  Google Scholar 

  • Zhang FQ, Wang YS, Lou ZP, Dong JD (2007) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67(1):44–50

    Article  CAS  Google Scholar 

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Acknowledgements

This work was jointly supported by National Natural Science Foundation of China (no. 30530150, no. 30970527, and no. 31000244) and the Fundamental Research Funds for the Central Universities (no. 2010121093). The authors would like to thank Miss Chen Qiong and Mr. Chen Yongfeng from the agricultural product quality and safety supervision and testing center in Xiamen for the determination of amino acids. We also thank Dr. John Merefield for assistance with English grammar.

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  1. Laboratory of Pollution Ecology, School of Life Sciences, Xiamen University, Xiamen, 361005, People’s Republic of China

    Xiangyu Xie, Dominik J. Weiss, Bosen Weng, Jingchun Liu, Haoliang Lu & Chongling Yan

  2. Department of Earth Science and Engineering, Imperial College London, London, SW72AZ, UK

    Dominik J. Weiss

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  1. Xiangyu Xie
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  2. Dominik J. Weiss
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Correspondence to Chongling Yan.

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Xie, X., Weiss, D.J., Weng, B. et al. 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 20, 997–1008 (2013). https://doi.org/10.1007/s11356-012-1031-9

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