Environmental Science and Pollution Research

, Volume 22, Issue 21, pp 16590–16599 | Cite as

Screening of Cd-safe genotypes of Chinese cabbage in field condition and Cd accumulation in relation to organic acids in two typical genotypes under long-term Cd stress

  • Xu WangEmail author
  • Yi Shi
  • Xin Chen
  • Bin Huang
Research Article


A 65-day field experiment was conducted to select cadmium (Cd)-safe genotypes (CSGs) among 21 Chinese cabbage genotypes in a low Cd-contaminated soil (0.66 mg kg−1). Seven CSGs were identified based on their Cd tolerance, shoot Cd concentrations, Cd enrichment factors (EFs), and translocation factors (TFs). Then, Beijingxin3, a typical CSG, together with Qiuxiang, a typical non-CSG for comparison, was selected for a subsequent 80-day field micro-plot experiment under four levels of Cd stress to evaluate the reliability of CSG screening and the role of organic acids in Cd accumulation and tolerance. Beijingxin3 was confirmed to be safe to grow in soil with Cd level up to 3.39 mg kg−1, with Cd accumulation in its shoots well below the permitted level, and Qiuxiang was still poor in tolerating low Cd stress (1.31 mg kg−1). With increasing the Cd stress, Cd accumulation and citrate concentrations increased in shoots and roots of both genotypes, and oxalate concentrations increased significantly in Beijingxin3 roots. Both oxalate and citrate concentrations were significantly positively related to Cd accumulation for Beijingxin3 roots. High accumulation in oxalate and citrate induced by Cd stress in Beijingxin3 roots could benefit its internal tolerance to long-term Cd stress with more Cd accumulation in its roots and less Cd accumulation in its shoots.


Cadmium Chinese cabbage genotype (Brassica pekinensis L.) Organic acid Tolerance Field experiment Long-term Cd stress 



We gratefully acknowledge the financial support from the National Science and Technology Infrastructure Program of the Ministry of Science and Technology of P.R. China (2012BAD14B02-2).


  1. Arao T, Ae N, Sugiyama M, Takahashi M (2003) Genotypic differences in cadmium uptake and distribution in soybeans. Plant Soil 251:247–253CrossRefGoogle Scholar
  2. Chen Y, Shen Z, Li X (2004) The use of vetiver grass (Vetiveria zizanioides) in the phytoremediation of soils contaminated with heavy metals. Appl Geochem 19:1553–1565CrossRefGoogle Scholar
  3. Chen Y, Li TQ, Han X, Ding ZL, Yang XE, Jin YF (2012) Cadmium accumulation in different pakchoi cultivars and screening for pollution-safe cultivars. J Zhejiang Univ Sci B 13(6):494–502CrossRefGoogle Scholar
  4. Chinese Ministry of Agriculture (2008) Cultivated area and yield of vegetable crops in China in 2006. Chin Veg 1:65–66 (in Chinese) Google Scholar
  5. Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486CrossRefGoogle Scholar
  6. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11CrossRefGoogle Scholar
  7. He JY, Zhu C, Ren YF, Yan YP, Jiang D (2006) Genotypic variation in grain cadmium concentration of lowland rice. J Plant Nutr Soil Sci 169:711–716CrossRefGoogle Scholar
  8. Hooda PS, Alloway BJ (1993) Effects of time and temperature on the bioavailability of Cd and Pb from sludge-amended soils. J Soil Sci 44:97–110CrossRefGoogle Scholar
  9. Ji PH, Sun TH, Song YF, Ackland ML, Liu Y (2011) Strategies for enhancing the phytoremediation of cadmium-contaminated agricultural soils by Solanum nigrum L. Environ Pollut 159:762–768CrossRefGoogle Scholar
  10. Kirkham MB (2006) Cadmium in plants on polluted soils: effects of soil factors, hyperaccumulation, and amendments. Geoderma 137:19–32CrossRefGoogle Scholar
  11. Kurz H, Schulz R, Romheld V (1999) Selection of cultivars to reduce the concentration of cadmium and thallium in food and fodder plants. J Plant Nutr Soil Sci 162:323–328CrossRefGoogle Scholar
  12. Li JT, Qiu JW, Wang XW, Zhong Y, Lan C, Shu WS (2006) Cadmium contamination in orchard soils and fruit trees and its potential health risk in Guangzhou, China. Environ Pollut 143:159–165CrossRefGoogle Scholar
  13. Li XH, Zhou QX, Wei SH, Ren WJ (2012) Identification of cadmium-excluding welsh onion (Allium fistulosum L.) cultivars and their mechanisms of low cadmium accumulation. Environ Sci Pollut Res 19:1773–1780CrossRefGoogle Scholar
  14. Liu JG, Liang JS, Li KQ, Zhang ZJ, Yu BY, Lu XL, Yang JC, Zhu QS (2003) Correlations between cadmium and mineral nutrients in absorption and accumulation in various genotypes of rice under cadmium stress. Chemosphere 52:1467–1473CrossRefGoogle Scholar
  15. Liu JG, Zhu QS, Zhang ZJ, Xu JK, Yang JC, Wong MH (2005) Variations in cadmium accumulation among rice cultivars and types and the selection of cultivars for reducing cadmium in the diet. J Sci Food Agric 85:147–153CrossRefGoogle Scholar
  16. Liu JG, Qian M, Cai GL, Yang JC, Zhu QS (2007a) Uptake and translocation of Cd in different rice cultivars and the relation with Cd accumulation in rice grain. J Hazard Mater 143:443–447CrossRefGoogle Scholar
  17. Liu JG, Qian M, Cai GL, Zhu QS, Wong MH (2007b) Variations between rice cultivars in root secretion of organic acids and the relationship with plant cadmium uptake. Environ Geochem Health 29:189–195CrossRefGoogle Scholar
  18. Liu WT, Zhou QX, Sun YB, Liu R (2009a) Identification of Chinese cabbage genotypes with low cadmium accumulation for food safety. Environ Pollut 157:1961–1967CrossRefGoogle Scholar
  19. Liu ZL, He XY, Chen W, Yuan FH, Yan K, Tao DL (2009b) Accumulation and tolerance characteristics of cadmium in a potential hyperaccumulator—Lonicera japonica Thunb. J Hazard Mater 169:170–175CrossRefGoogle Scholar
  20. Liu WT, Zhou QX, An J, Sun YB, Liu R (2010a) Variations in cadmium accumulation among Chinese cabbage cultivars and screening for Cd-safe cultivars. J Hazard Mater 173:737–743CrossRefGoogle Scholar
  21. Liu WT, Zhou QX, Zhang YL, Wei S (2010b) Lead accumulation in different Chinese cabbage cultivars and screening for pollution-safe cultivars. J Environ Manag 91(3):781–788CrossRefGoogle Scholar
  22. Liu WT, Zhou QX, Zhang ZN, Hua T, Cai Z (2011) Evaluation of cadmium phytoremediation potential in Chinese cabbage cultivars. J Agric Food Chem 59(15):8324–8330CrossRefGoogle Scholar
  23. Ma JF (2006) Physiological mechanisms of Al resistance in higher plants. Soil Sci Plant Nutr 51:609–612CrossRefGoogle Scholar
  24. Ma Z, Miyasaka SC (1998) Oxalate exudation by taro in response to Al. Plant Physiol 118:861–865CrossRefGoogle Scholar
  25. Ma JF, Zheng SJ, Matsumoto H (1997) Detoxifying aluminum with buckwheat. Nature 390:569–570CrossRefGoogle Scholar
  26. Nigam R, Srivastava S, Prakash S, Srivastava MM (2000) Effect of organic acids on the availability of cadmium in wheat. Chem Speciat Bioavailab 12:125–132CrossRefGoogle Scholar
  27. Peter MC (2002) Ecological risk assessment (ERA) and hormesis. Sci Total Environ 288:131–140CrossRefGoogle Scholar
  28. Pilon-Smits EAH, Freeman JL (2006) Environmental cleanup using plants: biotechnological advances and ecological considerations. Front Ecol Environ 4:203–210CrossRefGoogle Scholar
  29. Pinto AP, Simöes I, Mota AM (2008) Cadmium impact on root exudates of sorghum and maize plants: a speciation study. J Plant Nutr 31:1746–1755CrossRefGoogle Scholar
  30. Saber NE, Abdel-Moneim AM, Barakat SY (1999) Role of organic acids in sunflower tolerance to heavy metals. Biol Plant 42(1):65–73CrossRefGoogle Scholar
  31. Sugiyama M, Ae N, Hajika M (2011) Developing of a simple method for screening soybean seedling cadmium accumulation to select soybean genotypes with low seed cadmium. Plant Soil 341:413–422CrossRefGoogle Scholar
  32. Sun RL, Zhou QX, Jin CX (2006) Cadmium accumulation in relation to organic acids in leaves of Solanum nigrum L. as a newly found cadmium hyperaccumulator. Plant Soil 285:125–134CrossRefGoogle Scholar
  33. Sun YB, Zhou QX, Wang L, Liu WT (2009) Cadmium tolerance and accumulation characteristics of Bidens pilosa L. as a potential Cd-hyperaccumulator. J Hazard Mater 161:808–814CrossRefGoogle Scholar
  34. Sun RL, Zhou QX, Wei SH (2011) Cadmium accumulation in relation to organic acids and nonprotein thiols in leaves of the recently found Cd hyperaccumulator Rorippa globosa and the Cd accumulating plant Rorppa islandica. J Plant Growth Regul 30:83–91CrossRefGoogle Scholar
  35. Sun JY, Cui J, Luo CL, Gao L, Chen YH, Shen ZG (2013) Contribution of cell walls, nonprotein thiols, and organic acids to cadmium resistance in two cabbage varieties. Arch Environ Contam Toxicol 64:243–252CrossRefGoogle Scholar
  36. Ueno D, Ma JF, Iwashita T, Zhao FJ, McGrath SP (2005) Identification of the form of Cd in the leaves of a superior Cd accumulating ecotype of Thlaspi caerulescens using 113Cd-NMR. Planta 221:928–936CrossRefGoogle Scholar
  37. Wang JL, Yuan JG, Yang ZY, Huang BF, Zhou YH, Xin JL, Gong YL, Yu H (2009) Variation in cadmium accumulation among 30 cultivars and cadmium subcellular distribution in 2 selected cultivars of water spinach (Ipomoea aquatica Forsk.). J Agric Food Chem 57:8942–8949CrossRefGoogle Scholar
  38. Wei SH, Zhou QX (2008) Screen of Chinese weed species for cadmium tolerance and accumulation characteristics. Int J Phytoremediation 10:584–597CrossRefGoogle Scholar
  39. Wei SH, Zhou QX, Wang X (2005) Identification of weed plants excluding the absorption of heavy metals. Environ Int 31:829–834CrossRefGoogle Scholar
  40. Wei SH, Zhou QX, Koval PV (2006) Flowering stage characteristics of cadmium hyperaccumulator Solanum nigrum L. and their significance to phytoremediation. Sci Total Environ 369:441–446CrossRefGoogle Scholar
  41. Yang XE, Baligar VC, Foster JC, Martens (1997) Accumulation and transport of nickel in relation to organic acids in ryegrass and maize with different nickel levels. Plant Soil 196:271–276CrossRefGoogle Scholar
  42. 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 124:1019–1026CrossRefGoogle Scholar
  43. Yang XE, Jin XF, Feng Y, Islam E (2005) Molecular mechanisms and genetic basis of heavy metal tolerance/hyperaccumulation in plants. J Integr Plant Biol 47:1025–1035CrossRefGoogle Scholar
  44. Yang Y, Zhang FS, Li HF, Jiang RF (2009) Accumulation of cadmium in the edible parts of six vegetable species grown in Cd-contaminated soils. J Environ Manag 90:1117–1122CrossRefGoogle Scholar
  45. Yang JX, Guo HT, Ma YB, Wang LQ, Wei DP, Hua L (2010) Genotypic variations in the accumulations of Cd exhibited by different vegetables. J Environ Sci 22(8):1246–1252CrossRefGoogle Scholar
  46. Yu H, Wang JL, Fang W, Yuan JG, Yang ZY (2006) Cadmium accumulation in different rice cultivars and screening for pollution-safe cultivars of rice. Sci Total Environ 370:302–309CrossRefGoogle Scholar
  47. Zeng FR, Mao Y, Cheng WD, Wu FB, Zhang GP (2008) Genotypic and environmental variation in chromium, cadmium and lead concentrations in rice. Environ Pollut 153:309–314CrossRefGoogle Scholar
  48. Zhang GP, Fukami M, Sekimoto H (2002) Influence of cadmium on mineral concentrations and yield components in wheat genotypes differing in Cd tolerance at seedling stage. Field Crop Res 77:93–98CrossRefGoogle Scholar
  49. Zhang HJ, Wei ZG, Zhao HY, Yang HX, Li HX, Hu F (2009) Effects of low-molecular-weight organic acids on gadolinium accumulation and transportation in tomato plants. Biol Trace Elem Res 127:81–93CrossRefGoogle Scholar
  50. Zhang ZH, Rengel Z, Chang H, Meney K, Pantelic L, Tomanovic R (2012) Phytoremediation potential of Juncus subsecundus in soils contaminated with cadmium and polynuclear aromatic hydrocarbons (PAHs). Geoderma 175–176:1–8CrossRefGoogle Scholar
  51. Zhang SR, Lin HC, Deng LJ, Gong GS, Jia YX, Xu XX, Li T, Li Y, Chen H (2013) Cadmium tolerance and accumulation characteristics of Siegesbeckia orientalis L. Ecol Eng 51:133–139CrossRefGoogle Scholar
  52. Zhu Y, Yu H, Wang JL, Fang W, Yuan JG, Yang ZY (2007) Heavy metal accumulations of 24 Asparagus bean cultivars grown in soil contaminated with Cd alone and with multiple metals (Cd, Pb and Zn). J Agric Food Chem 55:1045–1052CrossRefGoogle Scholar
  53. 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 34:1055–1064CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.State Key Laboratory of Forest and Soil Ecology, Institute of Applied EcologyChinese Academy of SciencesShenyangChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.College of ScienceShenyang Agriculture UniversityShenyangChina

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