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Do soil Fe transformation and secretion of low-molecular-weight organic acids affect the availability of Cd to rice?

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Abstract

The bioavailability of cadmium (Cd) to rice may be complicated by chemical and biological factors in the rhizosphere. The aim of this work is to investigate how soil iron (Fe) redox transformations and low-molecular-weight organic acid (LMWOA) exudation from root affect Cd accumulation in rice. Two soils (a paddy soil and a saline soil) with different physicochemical properties were used in this study. Soil redox conditions were changed by flooding and addition of organic matter (OM). Two days after the soil treatments, rice seedlings were transplanted in a vermiculite–soil system and grown for 10 days. We measured pH and Eh, LMWOA, Fe and Cd contents in rice, and their fractions in the soils and vermiculite. Cadmium accumulation in rice declined in both soils upon the flooding and OM treatment. Iron dissolution in the paddy soil and its deposition in the rhizosphere significantly increased upon the OM addition, but the concentration of Fe plaque on the rice root significantly declined. Conversely, although Fe transformed into less active fractions in the saline soil, Fe accumulation on the surface and in the tissue of root was considerably enhanced. The secretion of LMWOA was remarkably induced when the OM was amended in the saline soil, but the same effect was not observed in the paddy soil. Reduction of Cd uptake by rice could be attributed to different factors in the two soils. For the paddy soil, the lowered Cd bioavailability was likely due to the competition of Fe and Cd for the binding sites on the vermiculite surface. For the saline soil, however, rice responded to the low Fe mobility through more LMWOA exudation and Fe plaque formation, and their increases could explain the decrease of rice Cd.

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References

  • Arao T, Kawasaki A, Baba K, Shinsuke M, Shingo M (2009) Effects of water management on cadmium and arsenic accumulation and dimethylarsinic acid concentrations in Japanese rice. Environ Sci Technol 43:9361–9367

    Article  CAS  Google Scholar 

  • Astolfi S, Ortolani MR, Catarcione G, Paolacci AR, Cesco S, Pinton R, Ciaffi M (2014) Cadmium exposure affects iron acquisition in barley (Hordeum vulgare) seedlings. Physiol Plant 152:646–659

    Article  CAS  Google Scholar 

  • Bolan NS, Makino T, Kunhikrishnan A, Kim PJ, Ishikawa S, Murakami M, Naidu R, Kirkham MB (2013) Cadmium contamination and its risk management in rice ecosystems. Adv Agron 119:183–273

    Article  CAS  Google Scholar 

  • Calmano W, Hong J, Forstner U (1993) Binding and mobilization of heavy metals in contaminated sediments affected by pH and redox potential. Water Sci Technol 28(8–9):223–235

    CAS  Google Scholar 

  • Chen LN, Ge Y, Zhang CH, Zhou QS (2009) Effect of submergence on the bioavailability of Cd in a red soil. J Agro-Environ Sci 28(11):2333–2337 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Chen X, Liu DQ, Wang S, Yang YZ, Li YJ, Hu H, Zhang CH, Ge Y (2013) Effects of soil redox condition on the transformations of Fe and Cd in soils and their uptake by rice. Acta Pedol Sin 50(3):118–125 (in Chinese with English abstract)

    Google Scholar 

  • Cieśliński G, Van Rees KCJ, Szmigielska AM, Krishnamurti GSR, Huang PM (1998) Low-molecular-weight organic acids in rhizosphere soils of durum wheat and their effect on cadmium bioaccumulation. Plant Soil 203:109–117

    Article  Google Scholar 

  • Colombo C, Palumbo G, He J-Z, Pinton R, Cesco S (2014) Review on iron availability in soil: interaction of Fe minerals, plants, and microbes. J Soils Sediments 14:538–548

    Article  CAS  Google Scholar 

  • Davranche M, Bollinger J (2000) Release of metals from iron oxyhydroxides under reductive conditions: effect of metal/solid interactions. J Colloid Interface Sci 232:165–173

    Article  CAS  Google Scholar 

  • de Livera J, McLaughlin MJ, Hettiarachchi GM, Kirby JK, Beak DG (2011) Cadmium solubility in paddy soils: effects of soil oxidation, metal sulfides and competitive ions. Sci Total Environ 409(8):1489–1497

    Article  Google Scholar 

  • Du Laing G, Rinklebe J, Vandecasteele B, Meers E, Tack FMG (2009) Trace metal behaviour in estuarine and riverine floodplain soils and sediments: a review. Sci Total Environ 407:3972–3985

    Article  Google Scholar 

  • Gambrell RP (1994) Trace and toxic metals in wetlands—a review. J Environ Qual 23:883–891

    Article  CAS  Google Scholar 

  • Hammer D, Keller C (2002) Changes in the rhizosphere of metal-accumulating plants evidenced by chemical extractants. J Environ Qual 31(5):1561–1569

    Article  CAS  Google Scholar 

  • Hinsinger P, Plassard C, Tang CX, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248(1–2):43–59

    Article  CAS  Google Scholar 

  • Hong J, Wang T (1984) Transformation of chemical elements in controlled pH-Eh system. Environ Inf Sci 6:48–56

    Google Scholar 

  • Hu LF, McBride MB, Cheng H, Wu JJ, Shi JC, Xu JM, Wu LS (2011) Root-induced changes to cadmium speciation in the rhizosphere of two rice (Oryza sativa L.) genotypes. Environ Res 111(3):356–361

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jung MC, Thornton I (1997) Environmental contamination and seasonal variation of metals in soils, plants and waters in the paddy fields around a Pb-Zn mine in Korea. Sci Total Environ 198(2):105–121

    Article  CAS  Google Scholar 

  • Kashem, Singh (2001a) Metal availability in contaminated soils: II. Uptake of Cd, Ni and Zn in rice plants grown under flooded culture with organic matter addition. Nutr Cycl Agroecosyst 61:257–266

    Article  CAS  Google Scholar 

  • Kashem MA, Singh BR (2001b) Metal bioavailability in contaminated soils: I. Effects of flooding and organic matter on the changes in pH, Eh and solubility of Cd, Ni and Zn. Nutr Cyl Agro 61:247–255

    Article  CAS  Google Scholar 

  • Kashem MA, Singh BR (2004) Transformations in solid phase species of metals as affected by flooding and organic matter. Commun Soil Sci Plant Anal 35(9–10):1435–1456

    Article  CAS  Google Scholar 

  • Kögel-Knabner I, Amelung W, Cao ZH, Fiedler S, Frenzel P, Jahn R, Kalbitz K, Kölbl A, Schloter M (2010) Biogeochemistry of paddy soils. Geoderma 157:1–14

    Article  Google Scholar 

  • Li YC, Ge Y, Zhang CH, Zhou QS (2010) Mechanisms for high Cd mobility in a red soil from southern China undergoing gradual reduction. Soil Res 48:371–384

    Google Scholar 

  • Lin Q, Chen YX, Chen HM, Yu YL, Luo YM, Wong MH (2003) Chemical behavior of Cd in rice rhizosphere. Chemosphere 50(6):755–761

    Article  CAS  Google Scholar 

  • Liu MC, Li HF, Xia LJ, Yang LS (2000) Differences of cadmium uptake by rice genotypes and relationship between the iron oxide plaque and cadmium uptake. Acta Sci Circumst 20(5):592–596 (in Chinese)

    CAS  Google Scholar 

  • Liu JG, Qian M, Cai G, Zhu Q, Wong MH (2007) Variations between rice cultivars in root secretion of organic acids and the relationship with plant cadmium uptake. Environ Geochem Health 29:189–195

    Article  CAS  Google Scholar 

  • Liu HJ, Zhang JL, Peter C, Zhang FS (2008) Influence of iron plaque on uptake and accumulation of Cd by rice (Oryza sativa L.) seedlings grown in soil. Sci Total Environ 394(2–3):361–368

    Article  CAS  Google Scholar 

  • Liu JG, Cao CX, Wong MH, Zhang ZJ, Chai YH (2010) Variations between rice cultivars in iron and manganese plaque on roots and the relation with plant cadmium uptake. J Environ Sci 22(7):1067–1072

    Article  CAS  Google Scholar 

  • Liu DQ, Zhang CH, Chen X, Yang YZ, Wang S, Li YJ, Hu H, Ge Y, Cheng WD (2013) Effects of pH, Fe and Cd on the uptake of Fe2+ and Cd2+ by rice. Environ Sci Pollut Res 20:8947–8954. doi:10.1007/s11356-013-1855-y

  • Ma JF, Furukawa J (2003) Recent progress in the research of external Al detoxification in higher plants: a minireview. J Inorg Biochem 9:746–751

    Google Scholar 

  • McLaughlin MJ, Singh BR (1999) Cadmium in soil and plants: a global perspective. In: McLaughlin MJ, Singh BR (eds) Cadmium in soil and plants. Kluwer Academic Publishers, Dordrecht, pp 13–21

    Chapter  Google Scholar 

  • Meharg AA, Norton G, Deacon C, Williams P, Adomako EE, Price A, Zhu YG, Li G, Zhao FJ, McGrath S, Villada A, Sommella A, De Silva PMCS, Brammer H, Dasgupta T, Islam MR (2013) Variation in rice cadmium related to human exposure. Environ Sci Technol 47:5613–5618

    Article  CAS  Google Scholar 

  • Mei XQ, Wong MH, Yang Y, Dong HY, Ye ZH (2012) The effects of radial oxygen loss on arsenic tolerance and uptake in rice and on its rhizosphere. Environ Pollut 165:109–117

    Article  CAS  Google Scholar 

  • Mimmo T, Del Buono D, Terzano R, Tomasi N, Vigani G, Crecchio C, Pinton R, Zocchi G, Cesco S (2014) Rhizospheric organic compounds in the soil–microorganism–plant system: their role in iron availability. Eur J Soil Sci 65:629–642

    Article  CAS  Google Scholar 

  • Muehe EM, Obst M, Hitchcock A, Tyliszczak T, Behrens S, Schröder C, Byrne JM, Michel FM, Krämer U, Kappler A (2013) Fate of Cd during microbial Fe(III) mineral reduction by a novel and Cd-tolerant Geobacter species. Environ Sci Technol 47:14099–14109

    Article  CAS  Google Scholar 

  • Neubauer SC, Emerson D, Megonigal JP (2007) Microbial oxidation and reduction of iron in the root zone and influences on metal mobility. In: Violante A, Huang PM, Gadd GM (eds) Biophysico-chemical processes of heavy metals and metalloids in soil environments. John Wiley & Sons, Hoboken

    Google Scholar 

  • Shao GS, Chen MX, Wang WX, Mou RX, Zhang GP (2007) Iron nutrition affects cadmium accumulation and toxicity in rice plants. Plant Growth Regul 53(1):33–42

    Article  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

    Article  CAS  Google Scholar 

  • Tripathi RD, Tripathi P, Dwivedi S, Kumar A, Mishra A, Chauhan PS, Norton GJ, Nautiyal CS (2014) Roles for root iron plaque in sequestration and uptake of heavy metals and metalloids in aquatic and wetland plants. Metallomics 6:1789–1800

    Article  CAS  Google Scholar 

  • Wang MY, Chen AK, Wong MH, Qiu RL, Chen H, Ye ZH (2011) Cadmium accumulation in and tolerance of rice (Oryza sativa L.) varieties with different rates of radial oxygen loss. Environ Pollut 159:1730–1736

    Article  CAS  Google Scholar 

  • Williams PN, Lei M, Sun GX, Huang Q, Lu Y, Deacon C, Meharg AA, Zhu YG (2009) Occurrence and partitioning of cadmium, arsenic and lead in mine impacted paddy rice: Hunan, China. Environ Sci Technol 43:637–642

    Article  CAS  Google Scholar 

  • Yang YY, Jung JY, Song WY, Suh HS, Lee Y (2000) Identification of rice varieties with high tolerance or sensitivity to lead and characterization of the mechanism of tolerance. Plant Physiol 124:1019–1026

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zhang CH, Ge Y, Yao H, Chen X, Hu MK (2012) Iron oxidation-reduction and its impacts on cadmium bioavailability in paddy soils: a review. Front Environ Sci Eng 6(4):509–517

    Article  CAS  Google Scholar 

  • Zheng SJ, Ma JF, Matsumoto H (1998a) High aluminum resistance in buckwheat: I. Al-induced specific secretion of oxalic acid from root tips. Plant Physiol 117:745–751

    Article  Google Scholar 

  • Zheng SJ, Ma JF, Matsumoto H (1998b) Continuous secretion of organic acids is related to aluminium resistance during relatively long-term exposure to aluminum stress. Physiol Plant 103:209–214

    Article  CAS  Google Scholar 

  • Zhu XF, Zheng C, Hu YT, Jiang T, Liu Y, Dong NY, Yang JL, Zheng SJ (2011) Cadmium-induced oxalate secretion from root apex is associated with cadmium exclusion and resistance in Lycopersicon esulentum. Plant Cell Environ 34:1055–1064

    Article  CAS  Google Scholar 

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Acknowledgments

This work was funded by National Science Foundation of China (30700479); Research Fund for the Doctoral Program of Higher Education of China (20090097110035, 20110097110004); Research Fund of State Key Laboratory of Soil and Sustainable Agriculture, Nanjing Institute of Soil Science, Chinese Academy of Science (Y052010019); and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD). The authors deeply appreciate the valuable comments made by Prof. William Hendershot in McGill University on the manuscript and the technical assistance in the rice LMWOA analysis provided by Prof. Shaojian Zheng and Dr. Xiaofang Zhu in Zhejiang University.

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Correspondence to Ying Ge.

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Responsible editor: Elena Maestri

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Chen, X., Yang, Y., Liu, D. et al. Do soil Fe transformation and secretion of low-molecular-weight organic acids affect the availability of Cd to rice?. Environ Sci Pollut Res 22, 19497–19506 (2015). https://doi.org/10.1007/s11356-015-5134-y

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