Environmental Science and Pollution Research

, Volume 24, Issue 21, pp 17566–17576 | Cite as

Cadmium accumulation characteristics of low-cadmium rice (Oryza sativa L.) line and F1 hybrids grown in cadmium-contaminated soils

  • Kun Li
  • Haiying Yu
  • Tingxuan Li
  • Guangdeng Chen
  • Fu Huang
Research Article


Cadmium (Cd) pollution has threatened severely to food safety and human health. A pot experiment and a field experiment were conducted to investigate the difference of Cd accumulation between rice (Oryza sativa L.) lines and F1 hybrids in Cd-contaminated soils. The adverse effect on biomass of rice lines was greater than that of F1 hybrids under Cd treatments in the pot experiment. The variations of Cd concentration among rice cultivars in different organs were smaller in stem and leaf, but larger in root and ear. Average proportion of Cd in root of F1 hybrids was 1.39, 1.39, and 1.16 times higher than those of rice lines at the treatment of 1, 2, and 4 mg Cd kg−1 soil, respectively. Cd concentrations in ear of F1 hybrids were significantly lower than rice lines with the reduction from 29.24 to 50.59%. Cd concentrations in brown rice of all F1 hybrids were less than 0.2 mg kg−1 at 1 mg Cd kg−1 soil, in which Lu98A/YaHui2816, 5406A/YaHui2816, and C268A/YaHui2816 could be screened out as cadmium-safe cultivars (CSCs) for being safe even at 2 mg Cd kg−1 soil. C268A/YaHui2816 showed the lowest Cd concentration in root among F1 hybrids, while Lu98A/YaHui2816 and 5406A/YaHui2816 showed lower capability of Cd translocation from root to shoot under Cd exposure, which eventually caused the lower Cd accumulation in brown rice. The lower level of Cd translocation contributed to reducing the accumulation of Cd in brown rice had been validated by the field experiment. Thus, Lu98A/YaHui2816, 5406A/YaHui2816, and C268A/YaHui2816 could be considered as potential CSCs to cultivate in Cd-contaminated soils (<2 mg Cd kg−1 soil).


Rice (Oryza sativa L.) lines Cadmium-safe cultivars (CSCs) Accumulation Translocation 



This study was carried out with support from the National Science and Technology Support Program (2015BAD05B01), Sichuan Science and Technology Support Program (2014NZ0008), and the Project of Sichuan Education Department (14ZB0017). The authors also wish to thank Juan Zhan, Daihua Ye, and Hongbing Luo for their important suggestions on the language and construction of this manuscript.


  1. Akhter Z, Shamsuddin AKM, Rohman MM, Shalim UM (2003) Studies on heterosis for yield and yield components in wheat. J Biol Sci 3:892–897CrossRefGoogle Scholar
  2. Auger DL, Gray AD, Ream TS, Kato A, Coe EH, Birchler JA (2005) Nonadditive gene expression in diploid and triploid hybrids of maize. Genetics 169:389–397CrossRefGoogle Scholar
  3. Bian RJ, Li LQ, Bao DD, Zheng JW, Zhang XH, Zheng JF, Liu XY, Cheng K, Pan GX (2016) Cd immobilization in a contaminated rice paddy by inorganic stabilizers of calcium hydroxide and silicon slag and by organic stabilizer of biochar. Environ Sci Pollut res 23:1–9CrossRefGoogle Scholar
  4. Chen YH, Liu XY, Wang MX, Wang J, Yan XM (2014) Cadmium tolerance, accumulation and relationship with Cd subcellular distribution in Ricinus communis L. Acta Sci Circumst 34:2440–2446 (in Chinese)Google Scholar
  5. Cheng SH, Zhuang JY, Fan YY, Du JH, Cao LY (2007) Progress in research and development on hybrid rice: a super-domesticate in China. Ann bot 100:959–966CrossRefGoogle Scholar
  6. Codex Alimentarius Commission (2014) CODEX STAN 193-1995, Codex general standard for contaminants and toxins in food and feedGoogle Scholar
  7. Fontanili L, Lancilli C, Suzui N, Dendena B, Yin YG, Ferri A, Ishiii S, Kawachi N, Lucchini G, Fujimaki S, Sacchi GA, Nocito FF (2016) Kinetic analysis of zinc/cadmium reciprocal competitions suggests a possible Zn-insensitive pathway for root-to-shoot cadmium translocation in rice. Rice 9:16–28CrossRefGoogle Scholar
  8. Grant CA, Clarke JM, Duguid S, Chaney RL (2008) Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 390:301–310CrossRefGoogle Scholar
  9. He JY, Zhu C, Ren YF, Yan YP, Cheng C, Jiang DA, Sun ZX (2008) Uptake, subcellular distribution, and chemical forms of cadmium in wide-type and mutant rice. Pedosphere 18:371–377CrossRefGoogle Scholar
  10. He JY, Ren YF, Chen XL, Chen H (2014) Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa L.) under cadmium stress. Ecotox Environ Safe 108:114–119CrossRefGoogle Scholar
  11. Huang Y, Zhang L, Zhang JW, Yuan DJ, Xu CG, Li XH, Zhou DX, Wang SP, Zhang QF (2006) Heterosis and polymorphisms of gene expression in an elite rice hybrid as revealed by a microarray analysis of 9198 unique ESTs. Plant Mol Biol 62:579–591CrossRefGoogle Scholar
  12. Huang XH, Yang SH, Gong JY, Zhao Q, Feng Q, Zhan QL, Zhao Y, Li WJ, Cheng BY, Xia JH, Chen N, Huang T, Zhang L, Fan DL, Chen JY, Zou CC, Lu YQ, Weng QJ, Han B (2016) Genomic architecture of heterosis for yield traits in rice. Nature 537:629–633CrossRefGoogle Scholar
  13. Ichitani K, Taura S, Tezuka T, Okiyama Y, Kuboyama T (2011) Chromosomal location of HWA1, and HWA2, complementary hybrid weakness genes in rice. Rice 4:29–38CrossRefGoogle Scholar
  14. Ishikawa S, Suzui N, Itotanabata 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 11:172–183CrossRefGoogle Scholar
  15. 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. P Natl Acad Sci USA 109:19166–19171CrossRefGoogle Scholar
  16. Ju CL, Zhang F, Gao YF, Zhang W, Yan JB, Dai JR, Li JS (2006) Cloning, chromosome mapping and expression analysis of an R 2 Y 3 -MYB gene under-expressed in maize hybrid. Mol Biol Rep 33:103–110CrossRefGoogle Scholar
  17. Kato M, Ishikawa S, Inagaki K, Chiba K, Hiroaki H, Yanagisawa S, Yoneyama T (2010) Possible chemical forms of cadmium and varietal differences in cadmium concentrations in the phloem sap of rice plants (Oryza sativa L.) Soil Sci Plant Nutr 56:839–847CrossRefGoogle Scholar
  18. Ke S, Cheng XY, Zhang N, Hu HG, Yan Q, Hou LL, Sun X, Chen ZN (2015) Cadmium contamination of rice from various polluted areas of china and its potential risks to human health. Environ Monit Asses 187:1–11CrossRefGoogle Scholar
  19. Khush GS (2013) Strategies for increasing the yield potential of cereals: case of rice as an example. Plant Breed 132:433–436Google Scholar
  20. Kosolsaksakul P, Farmer JG, Oliver IW, Graham MC (2014) Geochemical associations and availability of cadmium (Cd) in a paddy field system, northwestern Thailand. Environ Pollut 187:153–161CrossRefGoogle Scholar
  21. Li L, Zhou WH, Dai HX, Cao FB, Zhang GP, Wu FB (2012) Selenium reduces cadmium uptake and mitigates cadmium toxicity in rice. J Hazard Mater 235:343–351Google Scholar
  22. Li B, He WX, Wang CQ, Guo YM, Zhang JZ (2014) Selecting for cadmium exclusion or low accumulation rice cultivars in slight-moderate pollution area under field conditions. Pol J Environ Stud 23:1347–1353Google Scholar
  23. Lin LJ, He J, Wang X, Wang J, Lv XL, Liao MA, Wang ZH, Tang Y, Liang D, Xia H, Lai YS (2016) Cadmium accumulation characteristics of F1 hybrids by reciprocal hybridizing of Solanum nigrum in two climate-ecology regions. Environ Sci Pollut Res 23:1–8CrossRefGoogle Scholar
  24. Liu JG, Liang JS, Li KQ, Zhang ZJ, Yu BY, 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
  25. Liu JG, Min Q, Cai GL, Yang JC, Zhu QS (2007) 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
  26. 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
  27. Liu WT, Zhou QX, Zhang YL, Wei SH (2010b) Lead accumulation in different Chinese cabbage cultivars and screening for pollution-safe cultivars. J Environ Manag 91:781–788CrossRefGoogle Scholar
  28. Liu JG, Qu P, Zhang W, Dong Y, Li L, Wang MX (2014) Variations among rice cultivars in subcellular distribution of Cd: the relationship between translocation and grain accumulation. Environ Exp Bot 107:25–31CrossRefGoogle Scholar
  29. Lu RK (1999) Analysis of soil agrochemistry. Chinese Agricultural Science and Technology Press, Beijing (in Chinese)Google Scholar
  30. NFHSC (2010) National food hygienic standard of China. GB/T, pp 4789–2010Google Scholar
  31. Nocito FF, Lancilli C, Dendena B, Lucchini G, Sacchi GA (2011) Cadmium retention in rice roots is influenced by cadmium availability, chelation and translocation. Plant Cell Environ 34:994–1008CrossRefGoogle Scholar
  32. Rafiq MT, Aziz R, Yang XE, Xiao WD, Rafiq MK, Ali B, Li TQ (2014) Cadmium phytoavailability to rice (Oryza sativa L.) grown in representative Chinese soils. A model to improve soil environmental quality guidelines for food safety. Ecotox Environ Safe 103:101–107CrossRefGoogle Scholar
  33. Satoh-Nagasawa N, Mori M, Nakazawa N, Kawamoto T, Naqato Y, Sakurai K, Takahashi H, Watanabe A, Akaqi H (2012) Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol 53:213–224CrossRefGoogle Scholar
  34. Tanaka K, Fujimaki S, Fujiwara T, Yoneyama T, Hayashi H (2007) Quantitative estimation of the contribution of the phloem in cadmium transport to grains in rice plants (Oryza sativa L.) Soil Sci Plant Nutr 53:72–77CrossRefGoogle Scholar
  35. Tang H, Li TX, Yu HY, Zhang XZ (2016) Cadmium accumulation characteristics and removal potentials of high cadmium accumulating rice line grown in cadmium-contaminated soils. Environ Sci Pollut Res 23:15351–15357CrossRefGoogle Scholar
  36. Tezuka K, Miyadate H, Katou K, Kodama I, Matsumoto A, Kawamoto T, Masaki S, Satoh H, Yamaguchi M, Sakurai K, Takahashi H, Nagasawasatoh N, Watanabe A, Fujimura T, Akagi H (2010) A single recessive gene controls cadmium translocation in the cadmium hyperaccumulating rice cultivar Cho-Ko-Koku. Theor App Genet 120:1175–1182CrossRefGoogle Scholar
  37. Touceda-González M, Brader G, Antonielli L, Ravindran VB, Waldner G, Friesl-Hanl W, Corretto E, Campisano A, Pancher M, Sessitsch A (2015) Combined amendment of immobilizers and the plant growth-promoting strain Burkholderia phytofirmans PsJN favours plant growth and reduces heavy metal uptake. Soil Biol Biochem 91:140–150CrossRefGoogle Scholar
  38. Ueno D, Kono I, Yokosho K, Ando T, Yano M, Ma JF (2009) A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa). New Phytol 182:644–653CrossRefGoogle Scholar
  39. Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. P Natl Acad Sci USA 107:16500–16505CrossRefGoogle Scholar
  40. Uraguchi S, Fujiwara T (2012) Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice 5:1–8CrossRefGoogle Scholar
  41. Uraguchi S, Fujiwara T (2013) Rice breaks ground for cadmium-free cereals. Curr Opin Plant Biol 16:328–334CrossRefGoogle Scholar
  42. 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 60:2677–2688CrossRefGoogle Scholar
  43. Wan YN, Yu Y, Wang Q, Qiao YH, Li HF (2016) Cadmium uptake dynamics and translocation in rice seedling: influence of different forms of selenium. Ecotox Environ Safe 133:127–134Google Scholar
  44. Wang FJ, Wang M, Liu ZP, Shi Y, Han TQ, Ye YY, Gong N, Sun JW, Zhu C (2015) Different responses of low grain-Cd-accumulating and high grain-Cd-accumulating rice cultivars to Cd stress. Plant Physiol Bioch 96:261–269CrossRefGoogle Scholar
  45. Xia SL, Deng RB, Zhang Z, Liu CF, Shi GR (2016) Variations in the accumulation and translocation of cadmium among pak choi cultivars as related to root morphology. Environ Sci Pollut Res 23:9832–9842Google Scholar
  46. Xie PP, Deng JW, Zhang HM, Ma YH, Cao DJ, Ma RX, Liu RJ, Liu C, Liang YG (2015) Effects of cadmium on bioaccumulation and biochemical stress response in rice (Oryza sativa L.) Ecotox Environ Safe 122:392–398CrossRefGoogle Scholar
  47. Xie LH, Tang SQ, Wei XJ, Shao GN, Jiao GA, Sheng ZH, Luo J, Hu PS (2017) The cadmium and lead content of the grain produced by leading Chinese rice cultivars. Food Chem 217:217–224CrossRefGoogle Scholar
  48. Xue M, Zhou YH, Yang ZY, Lin BY, Yuan JG, Wu SS (2013) Comparisons in subcellular and biochemical behaviors of cadmium between low-Cd and high-Cd accumulation cultivars of pakchoi (Brassica chinensis L.) Front Env Sci Eng 8:226–238CrossRefGoogle Scholar
  49. Yao WY, Sun L, Zhou H, Yang F, Mao DH, Wang JR, Chen LH, Zhang GY, Dai JP, Xiao GY, Chen CY (2015) Additive, dominant parental effects control the inheritance of grain cadmium accumulation in hybrid rice. Mol Breeding 35:1–10CrossRefGoogle Scholar
  50. 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
  51. Yu LL, Zhu JY, Huang QQ, Su DC, Jiang RF, Li HF (2014) Application of a rotation system to oilseed rape and rice fields in Cd-contaminated agricultural land to ensure food safety. Ecotox Environ Safe 108:28–293CrossRefGoogle Scholar
  52. Yuan LY, Yang SG, Liu BX, Zhang M, Wu KQ (2012) Molecular characterization of a rice metal tolerance protein, OsMTP1. Plant Cell Rep 31:67–79CrossRefGoogle Scholar
  53. 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
  54. Zhan J, Wei SH, Niu RC, Li YM, Wang SS, Zhu JG (2013) Identification of rice cultivar with exclusive characteristic to Cd using a field-polluted soil and its foreground application. Environ Sci Pollut Res 20:2645–2650CrossRefGoogle Scholar
  55. Zhang HJ, Zhang XZ, Li TX, Huang F (2013) Variation of cadmium uptake, translocation among rice lines and detecting for potential cadmium-safe cultivars. Environ Earth Sci 71:277–286Google Scholar
  56. Zhao BH, Zhang HX, Xi LL, Zhu QS, Yang JC (2006) Concentrations and accumulation of cadmium in different organs of hybrid rice. Zhongguo Shuidao Kexue 20:306–312 (in Chinese)Google Scholar
  57. Zhou H, Zeng M, Zhou X, Liao BH, Peng PQ, Hu M, Zhu W, Wu YJ, Zou ZJ (2015) Heavy metal translocation and accumulation in iron plaques and plant tissues for 32 hybrid rice (Oryza sativa L.) cultivars. Plant Soil 386:317–329CrossRefGoogle Scholar
  58. Zhu Y, Yu H, Wang J, Fang W, Yuan J, Yang Z (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 Agr Food Chem 55:1045–1052CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.College of ResourcesSichuan Agricultural UniversitySichuanPeople’s Republic of China
  2. 2.College of AgronomySichuan Agricultural UniversitySichuanPeople’s Republic of China

Personalised recommendations