Abstract
Background and aims
Water spinach is a common leafy vegetable in Asia, with a strong ability to accumulate cadmium (Cd) in its edible parts. The aims of this study were to investigate the effects of cultivar variation and water management on Cd accumulation in this plant.
Methods
Three experiments were conducted: a soil pot trial with 32 cultivars, a rhizobox trial with 4 cultivars under flooded and non-flooded conditions and an uptake kinetics trial with 2 cultivars.
Results
There were significant differences in Cd accumulation between the different cultivars, and Cd concentrations in shoots were significantly lower in the flooded (0.25–1.4, mean 0.90 mg kg−1 DW) than in the non-flooded (1.9–4.7, 3.2 mg kg−1) treatments. Cultivars with a low Cd accumulation had a lower Cd bioavailability and mobility in the rhizosphere soil, higher Cd combined with Fe plaque on roots, lower Cd uptake capacity by roots, and lower Cd transfer factors than those with a high Cd accumulation.
Conclusions
Water spinach grown under anaerobic conditions effectively reduces Cd accumulation in edible parts. Low Cd-accumulating cultivars tend to possess a high ability to reduce Cd bioavailability in rhizosphere soil, as well as decrease Cd uptake, and translocation from root to shoot.






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Arao T, Ishikawa S (2006) Genotypic differences in cadmium concentration and distribution of soybeans and rice. Jarq-Japn Agric Res Q 40:21–30
Arao T, Ae N, Sugiyama M, Takahashi M (2003) Genotypic differences in cadmium uptake and distribution in soybeans. Plant Soil 251:247–253
Arao T, Kawasaki A, Baba K, Mori S, Matsumoto S (2009) Effects of water management on cadmium and arsenic accumulation and dimethylarsinic acid concentrations in Japanese rice. Environ Sci Technol 43:9361–9367
Begg MCB, Kirk GJD, Mackenzie AF, Neue HU (1994) Root-induced iron oxidation and pH changes in the lowland rice rhizosphere. New Phytol 128:469–477
Chan DY, Hale BA (2004) Differential accumulation of Cd in durum wheat cultivars: uptake and retranslocation as sources of variation. J Exp Bot 55:2571–2579
Chang AC, Page AL, Foster KW, Jones TE (1982) A comparison of cadmium and zinc accumulation by four cultivars of barley grown in sludge-amended soils. J Environ Qual 11:409–412
Chao DY, Silva A, Baxter I, Huang YS, Nordborg M, Danku J, Lahner B, Yakubova E, Salt DE (2012) Genome-wide association studies identify Heavy Metal ATPase3 as the primary determinant of natural variation in leaf cadmium in Arabidopsis thaliana. Plos Genet 8(9):e1002923
Chen F, Dong J, Wang F, Wu F, Zhang G, Li G, Chen Z, Chen J, Wei K (2007) Identification of barley genotypes with low grain Cd accumulation and its interaction with four microelements. Chemosphere 67:2082–2088
Cheng H, Chen DT, Tam NFY, Chen GZ, Li SY, Ye ZH (2012) Interactions among Fe2+, S2−, and Zn2+ tolerance, root anatomy, and radial oxygen loss in mangrove plants. J Exp Bot 63(7):2619–2630
Cheng H, Wang MY, Wong MH, Ye ZH (2014) Does radial oxygen loss and iron plaque formation on roots alter Cd and Pb uptake and distribution in rice plant tissues? Plant Soil 375:137–148
Clemens S, Palmgren MG, Kramer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315
Clemens S, Aarts MGM, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18(2):92–99
Colmer TD (2003) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deepwater rice (Oryza sativa L.). Ann Bot 91:301–309
Deng H, Ye ZH, Wong MH (2009) Lead, zinc and iron (Fe2+) tolerance in wetland plants and relation to root anatomy and spatial pattern of ROL. Environ Exp Bot 65:353–362
Dunbar KR, McLaughlin MJ, Reid RJ (2003) The uptake and partitioning of cadmium in two cultivars of potato (Solanum tuberosum L.). J Exp Bot 54:349–354
Esteban E, Moreno E, Peñalosa J, Cabrero JI, Millán R, Zornoza P (2008) Short and long-term uptake of Hg in white lupin plants: kinetics and stress indicators. Environ Exp Bot 62:316–322
Fitz WJ, Wenzel WW (2002) Arsenic transformation in the soil-rhizosphere-plant system: fundamentals and potential application to phytoremediation. J Biotechnol 99:259–278
Florijn PJ, Van Beusichem ML (1993) Cadmium distribution in maize inbred lines: effects of pH and level of Cd supply. Plant Soil 153:79–84
Gleason SM, Ewel KC, Hue N (2003) Soil redox conditions and plant-soil relationships in a Micronesian mangrove forest. Estuar Coast Shelf Sci 56:1065–1074
Göthberg A, Greger M, Bengtsson BE (2002) Accumulation of heavy metals in water spinach (Ipomoea aquatica) cultivated in the Bangkok region, Thailand. Environ Toxicol Chem 21(9):1934–1939
Grant CA, Clarke JM, Duguid S, Chaney RL (2008) Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 390:301–310
Greger M, Landberg T (2008) Role of rhizosphere mechanisms in Cd uptake by various wheat cultivars. Plant Soil 312:195–205
Hang XS, Wang HY, Zhou JM, Ma CL, Du CW, Chen XQ (2009) Risk assessment of potentially toxic element pollution in soils and rice (Oryza sativa) in a typical area of the Yangtze River Delta. Environ Pollut 157:2542–2549
Harrison HA (1986) Carrot response to sludge application and bed type. J Am Soc Hortic Sci 11:211–215
Hart JJ, Welch RM, Norvell WA, Sullivan LA, Kochian LV (1998) Characterization of cadmium binding, uptake, and translocation in intact seedlings of bread and durum wheat cultivars. Plant Physiol 116:1413–1420
Hinesly TD, Alexander DE, Ziegler EL, Barrett GL (1978) Zinc and Cd accumulation by corn inbreds grown on sludge amended soil. Agron J 70:425–428
Hseu ZY, Jien SH, Wang SH, Deng HW (2013) Using EDDS and NTA for enhanced phytoextraction of Cd by water spinach. J Environ Manag 117:58–64
Huang SS, Liao QL, Hua M, Wu XM, Bi KS, Yan CY, Chen B, Zhang XY (2007) Survey of heavy metal pollution and assessment of agricultural soil in Yang zhong district, Jiangsu Province, China. Chemosphere 67:2148–2155
Ishikawa S, Suzui N, Ito-Tanabata S, Ishii S, Igura M, Abe T, Kuramata M, Kawachi N, Fujimaki S (2011) Real-time imaging and analysis of differences in cadmium dynamics in rice cultivars (Oryza sativa) using positron-emitting 107Cd tracer. BMC Plant Biol 11:172
Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, Senoura T, Hase Y, Arao T, Nishizawa NK, Nakanishi H (2012) Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc Natl Acad Sci U S A 109(47):19166–19171
Jensen CR, Luxmoore RJ, Van-Gundy SD, Stolzy LH (1969) Root air space measurements by a pycnometer method. Agron J 61:474–475
Kabala C, Singh BR (2001) Fractionation and mobility of copper, lead and zinc in soil profiles in the vicinity of a copper smelter. J Environ Qual 30:485–495
Keon NE, Swartz CH, Brabander DJ, Harvey C, Hemond HF (2001) Validation of an arsenic sequential extraction method for evaluating mobility in sediments. Environ Sci Technol 35:2778–2784
Kirk GJD, Bajita JB (1995) Root-induced oxidation, pH changes and zinc solubilization in the rhizosphere of lowland rice. New Phytol 131:129–137
Kludze HK, Delaune RD, Patrick WH (1993) Aerenchyma formation and methane and oxygen exchange in rice. Soil Sci Soc Am J 51:368–391
Li B, Wang X, Qi XL, Huang L, Ye ZH (2012) Identification of rice cultivars with low brown rice mixed cadmium and lead contents and their interactions with the micronutrients iron, zinc, nickel and manganese. J Environ Sci 24:1790–1798
Liu J, Qian M, Cai G, Yang J, Zhu Q (2007) Uptake and translocation of Cd in different rice cultivars and the relation with Cd accumulation in rice grain. J Hazard Mater 143:443–447
Liu JC, Yan CL, Zhang RF, Lu HL, Qin GQ (2008) Speciation changes of cadmium in mangrove (Kandelia candel (L.)) rhizosphere sediments. Bull Environ Contam Toxicol 80:231–236
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 22:1067–1072
Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62(1):21–37
Macfie SM, Crowder AA (1987) Soil factors influencing ferric hydroxide plaque formation on roots of Typha latifolia L. Plant Soil 102:177–184
Marcussen H, Joergensen K, Holm PE, Brocca D, Simmons RW, Dalsgaard A (2008) Element contents and food safety of water spinach (Ipomoea aquatica Forssk.) cultivated with wastewater in Hanoi, Vietnam. Environ Monit Assess 139:77–91
María-Cervantes A, Conesa HM, González-Alcaraz MN, Álvarez-Rogel J (2010) Rhizosphere and flooding regime as key factors for the mobilisation of arsenic and potentially harmful metals in basic, mining-polluted salt marsh soils. Appl Geochem 25:1722–1733
Mei XQ, Ye ZH, Wong MH (2009) The relationship of root porosity and radial oxygen loss on arsenic tolerance and uptake in rice grains and straw. Environ Pollut 157:2550–2557
Mei XQ, Wong MH, Yang Y, Dong HY, Qiu RL, 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
Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H (2011) OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189:190–199
Otte ML, Rozema J, Koster L, Haarsma MS, Broekman RA (1989) Iron plaque on roots of Aster tripolium L.: interaction with zinc uptake. New Phytol 111:309–317
Pribyl DW (2010) A critical review of the conventional SOC to SOM conversion factor. Geoderma 156:75–83
Reddy CN, Patrick WH Jr (1977) Effect of redox potential and pH on the uptake of Cd and Pb by rice plants. J Environ Qual 6:259–262
Redjala T, Sterckeman T, Morel JL (2009) Cadmium uptake by roots: Contribution of apoplast and of high- and low-affinity membrane transport systems. Environ Exp Bot 67:235–242
Rivera-Becerril F, Calantzis C, Turnau K, Caussanel J-P, Belimov AA, Gianinazzi S, Strasser RJ, Gianinazzi-Pearson V (2002) Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes. J Exp Bot 53:1177–1185
Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24(5):2155–2167
Satarug S, Baker JR, Urbenjapol S, Haswell-Elkins M, Reilly PEB, Willams DJ (2003) A global perspective on cadmium pollution and toxicity in non-occupationally exposed population. Toxicol Lett 137:65–83
Stolt P, Asp H, Hultin S (2006) Genetic variation in wheat cadmium accumulation on soils with different cadmium concentrations. J Agron Crop Sci 192:201–208
Tessier A, Campbell P, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51:851–884
Thomas GM, Harrison HC (1991) Genetic line effects on parameters influencing cadmium concentration in lettuce (Lactuca sativa L.). J Plant Nutr 14:953–962
Tripathi R, 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
Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci U S A 107(38):16500–16505
Uraguchi S, Fujiwara T (2013) Rice breaks ground for cadmium-free cereals. Curr Opin Plant Biol 16(3):328–334
Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S (2009) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60:2677–2688
Van der Vliet L, Peterson C, Hale B (2007) Cd accumulation in roots and shoots of durum wheat: the roles of transpiration rate and apoplastic bypass. J Exp Bot 58:2939–2947
Vymazal J, Švehla J (2013) Iron and manganese in sediments of constructed wetlands with horizontal subsurface flow treating municipal sewage. Ecol Eng 50:69–75
Wang JL, Wei F, Yang ZY (2007) Inter-and Intra-specific variations of Cd accumulation of 13 leafy vegetable species grown in Cd contaminated soils. J Agric Food Chem 34:1154–1158
Wang MY, Chen AK, Wong MH, Qiu RL, Cheng 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
Wang X, Ye ZH, Li B, Huang LN, Meng M, Shi JB, Jiang GB (2014) Growing rice aerobically markedly decreases mercury accumulation by reducing both Hg bioavailability and the production of MeHg. Environ Sci Technol 48:1878–1885
Wei S, Twardowska I (2013) Main rhizosphere characteristics of the Cd hyperaccumulator Rorippa globosa (Turcz.) Thell. Plant Soil 372:669–681
Wiengweera A, Greenway H, Thomson CJ (1997) The use of agar nutrient solution to simulate lack of convection in waterlogged soils. Ann Bot 80:115–123
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. Sci Total Environ 43:637–642
Xu XY, McGrath SP, Meharg AA, Zhao FJ (2008) Growing rice aerobically markedly decreases arsenic accumulation. Environ Sci Technol 42:5574–5579
Yang JX, Liu Y, Ye ZH (2012) Root-induced changes (pH, Eh, Fe2+ and speciation of Pb and Zn) in rhizosphere soils of four wetland plants with different ROL. Pedosphere 22:518–527
Youssef RA, Chino M (1989) Root-induced changes in the rhizosphere of plants II. Distribution of heavy metal across the rhizosphere in soil. Soil Sci Plant Nutr 35:609–621
Zhao FJ, Jiang RF, Dunham SJ, McGrath SP (2006) Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri. New Phytol 172:646–654
Zheng SN, Zhang MK (2011) Effect of moisture regime on the redistribution of heavy metals in paddy soil. J Environ Sci 23:434–443
Zhuang P, Zou B, Li NY, Li ZA (2009) Heavy metal contamination in soils and food crops around Dabaoshan Mine in Guangdong, China: implication for human health. Environ Geochem Health 31:707–715
Acknowledgments
This work was funded by the National Natural Science Foundation of China (30770417), a Start-up Research Grant for Newly Recruited Professors/(Research) Chair Professors, The Hong Kong Institute of Education (RG24/13-14R) and National ‘863’ projects of China (2012AA061510). We thank Prof. A.J.M. Baker (The Universities of Melbourne and Queensland, Australia) for help in the initial preparation and improvement of this paper and the anonymous reviewers for their helpful suggestions.
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Xiao, Q., Wong, M.H., Huang, L. et al. Effects of cultivars and water management on cadmium accumulation in water spinach (Ipomoea aquatica Forsk.). Plant Soil 391, 33–49 (2015). https://doi.org/10.1007/s11104-015-2409-5
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DOI: https://doi.org/10.1007/s11104-015-2409-5
