, Volume 245, Issue 5, pp 965–976 | Cite as

Synergistic effects between [Si-hemicellulose matrix] ligands and Zn ions in inhibiting Cd ion uptake in rice (Oryza sativa) cells

  • Jie Ma
  • Xiuqing Zhang
  • Lijun Wang
Original Article


Main conclusion

Our study demonstrated that Zn alleviated Cd toxicity in the presence of Si in the cell walls by Zn 2+ binding to ligands through the formation of the [Si-hemicellulose matrix]Zn complexes that restrict the uptake of Cd.

The plant cell wall exhibits preferential sites for the accumulation of metals at toxic concentrations. Through modification of wall polysaccharide components, elements, such as silicon (Si) and zinc (Zn), may play active roles in alleviating the toxicity of heavy metals, including cadmium (Cd). However, enhanced tolerance for Cd stress may rely on synergistic effects between nutrient elements. Here, we cultured Si-accumulating suspension cells of rice (Oryza sativa) exposed to Cd and Zn treatments, either separately or in combination, and investigated cells using noninvasive microtest technology (NMT), inductively coupled plasma mass spectroscopy (ICP-MS) and atomic force microscopy (AFM). We found that Zn alleviated Cd toxicity in the presence of Si in the cell walls by binding of Zn2+ to ligands through the formation of the [Si-hemicellulose matrix]Zn complexes and co-precipitates to greatly inhibit Cd2+ uptake into cells. This, in turn, induced the lower expression of Cd-related transporters. This synergistic effect could be decisive for the survival of cells under conditions of high Cd concentrations.


Cadmium (Cd) Zinc (Zn) Silicon (Si) [Si-hemicellulose matrix] ligands Synergistic effects Cell wall Rice (Oryza sativa) single cell 



This work was supported by the National Natural Science Foundation of China (31672222 and 31172027) and the Fundamental Research Funds for the Central Universities (2662015PY206).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

425_2017_2655_MOESM1_ESM.pdf (32 kb)
Table S1. Primers for RT-PCR analysis of the genes (PDF 31 kb)


  1. Adamis PD, Gomes DS, Pinto MLC, Panek AD, Eleutherio EC (2004) The role of glutathione transferases in cadmium stress. Toxicol Lett 154:81–88CrossRefPubMedGoogle Scholar
  2. Ahmed M, Kamran A, Asif M, Qadeer U, Ahmed ZI, Goyal A (2013) Silicon priming: a potential source to impart abiotic stress tolerance in wheat: a review. Aust J Crop Sci 7:484Google Scholar
  3. Ammar WB, Zarrouk M, Nouairi I (2015) Zinc alleviates cadmium effects on growth, membrane lipid biosynthesis and peroxidation in Solanum lycopersicum leaves. Biologia 70:198–207CrossRefGoogle Scholar
  4. Aravind P, Prasad MNV (2003) Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L.: a free floating freshwater macrophyte. Plant Physiol Biochem 41:391–397CrossRefGoogle Scholar
  5. Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702CrossRefPubMedGoogle Scholar
  6. Brzóska MM, Moniuszko-Jakoniuk J (2001) Interactions between cadmium and zinc in the organism. Food Chem Toxicol 39:967–980CrossRefPubMedGoogle Scholar
  7. Chakravarty B, Srivastava S (1997) Effect of cadmium and zinc interaction on metal uptake and regeneration of tolerant plants in linseed. Agr Ecosyst Environ 61:45–50CrossRefGoogle Scholar
  8. Chou TS, Chao YY, Huang WD, Hong CY, Kao CH (2011) Effect of magnesium deficiency on antioxidant status and cadmium toxicity in rice seedlings. J Plant Physiol 168:1021–1030CrossRefPubMedGoogle Scholar
  9. Da Cunha KPV, do Nascimento CWA (2009) Silicon effects on metal tolerance and structural changes in maize (Zea mays L.) grown on a cadmium and zinc enriched soil. Water Air Soil Pollut 197:323–330CrossRefGoogle Scholar
  10. Das P, Samantaray S, Rout GR (1997) Studies on cadmium toxicity in plants: a review. Environ Pollut 98:29–36CrossRefPubMedGoogle Scholar
  11. Egan SK, Bolger PM, Carrington CD (2007) Update of US FDA’s total diet study foodlist and diets. J Exp Sci Environ Epidemiol 17:573–582CrossRefGoogle Scholar
  12. Epstein E (2009) Silicon: its manifold roles in plants. Ann Appl Biol 155:155–160CrossRefGoogle Scholar
  13. Ghareeb H, Bozsó Z, Ott PG, Repenning C, Stahl F, Wydra K (2011) Transcriptome of silicon-induced resistance against Ralstonia solanacearum in the silicon non-accumulator tomato implicates priming effect. Physiol Mol Plant P 75:83–89Google Scholar
  14. Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494CrossRefGoogle Scholar
  15. Grotz N, Fox T, Connolly E, Park W, Guerinot ML, Eide D (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc Natl Acad Sci USA 95:7220–7224CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gu HH, Zhan SS, Wang SZ, Tang YT, Chaney RL, Fang XH, Cai XD, Qiu RL (2012) Silicon-mediated amelioration of zinc toxicity in rice (Oryza sativa L.) seedlings. Plant Soil 350:193–204CrossRefGoogle Scholar
  17. Guerinot ML (2000) The ZIP family of metal transporters. BBA-Biomembr 1465:190–198CrossRefGoogle Scholar
  18. Guerriero G, Hausman JF, Legay S (2016) Silicon and the plant extracellular matrix. Front Plant Sci 7:463CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11CrossRefPubMedGoogle Scholar
  20. Hassan MJ, Zhang G, Wu F, Wei K, Chen Z (2005) Zinc alleviates growth inhibition and oxidative stress caused by cadmium in rice. J Plant Nutr Soil Sci 168:255–261CrossRefGoogle Scholar
  21. Ishimaru Y, Kakei Y, Shimo H, Bashir K, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) A rice phenolic efflux transporter is essential for solubilizing precipitated apoplasmic iron in the plant stele. J Biol Chem 286:24649–24655CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kalis EJ, Davis TA, Town RM, Leeuwen HPV (2009) Impact of ionic strength on Cd (II) partitioning between alginate gel and aqueous media. Environ Sci Technol 43:1091–1096CrossRefPubMedGoogle Scholar
  23. Kumari M, Sinhal VK, Srivastava A, Singh VP (2011) Zinc alleviates cadmium induced toxicity in Vigna radiata (L.) Wilczek. J Phytol 3:43–46Google Scholar
  24. Liang Y, Sun W, Zhu YG, Christie P (2007) Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environ Pollut 147:422–428CrossRefPubMedGoogle Scholar
  25. Lin YF, Aarts MG (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206CrossRefPubMedGoogle Scholar
  26. Lin HM, Fang CX, Li YZ, Lin WW, He JY, Lin RY, Lin WX (2017) Cadmium-stress mitigation through gene expression of rice and silicon addition. Plant Growth Regul 81:91–101CrossRefGoogle Scholar
  27. Liu J, Ma J, He CW, Li XL, Zhang WJ, Xu FS, Lin YJ, Wang LJ (2013) Inhibition of cadmium ion uptake in rice (Oryza sativa) cells by a wall-bound form of silicon. New Phytol 200:691–699CrossRefPubMedGoogle Scholar
  28. Lu LL, Tian SK, Yang XE, Wang XC, Brown P, Li TQ, He ZL (2008) Enhanced root-to-shoot translocation of cadmium in the hyperaccumulating ecotype of Sedum alfredii. J Exp Bot 59:3203–3213CrossRefPubMedPubMedCentralGoogle Scholar
  29. Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37CrossRefPubMedGoogle Scholar
  30. Ma JF (2004) Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci Plant Nutr 50:11–18CrossRefGoogle Scholar
  31. Ma J, Cai HM, He CW, Zhang WJ, Wang LJ (2015) A hemicellulose-bound form of silicon inhibits cadmium ion uptake in rice (Oryza sativa) cells. New Phytol 206:1063–1074CrossRefPubMedGoogle Scholar
  32. Ma J, Sheng H, Li X, Wang LJ (2016) iTRAQ-based proteomic analysis reveals the mechanisms of silicon-mediated cadmium tolerance in rice (Oryza sativa) cells. Plant Physiol Biochem 104:71–80CrossRefPubMedGoogle Scholar
  33. Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedling. Plant Physiol 132:272–281CrossRefPubMedPubMedCentralGoogle Scholar
  34. Nan Z, Li J, Zhang J, Cheng G (2002) Cadmium and zinc interactions and their transfer in soil-crop system under actual field conditions. Sci Total Environ 285:187–195CrossRefPubMedGoogle Scholar
  35. Neumann D, ZurNieden U (2001) Silicon and heavy metal tolerance of higher plants. Phytochemistry 56:685–692CrossRefPubMedGoogle Scholar
  36. Niyogi S, Wood CM (2004) Biotic ligand model, a flexible tool for developing site-specific water quality guidelines for metals. Environ Sci Technol 38:6177–6192CrossRefPubMedGoogle Scholar
  37. Ohshima H, Kondo T (1990) Relationship among the surface potential, Donnan potential and charge density of ion-penetrable membranes. Biophys Chem 38:117–122CrossRefPubMedGoogle Scholar
  38. Palmgren MG, Clemens S, Williams LE, Krämer U, Borg S, Schjørring JK, Sanders D (2008) Zinc biofortification of cereals: problems and solutions. Trends Plant Sci 13:464–473CrossRefPubMedGoogle Scholar
  39. Prabagar S, Hodson MJ, Evans DE (2011) Silicon amelioration of aluminium toxicity and cell death in suspension cultures of Norway spruce [Picea abies (L.) Karst.]. Environ Exp Bot 70:266–276CrossRefGoogle Scholar
  40. Qiu RL, Thangavel P, Hu PJ, Senthilkumar P, Ying RR, Tang YT (2011) Interaction of cadmium and zinc on accumulation and sub-cellular distribution in leaves of hyperaccumulator Potentilla griffithii. J Hazard Mater 186:1425–1430CrossRefPubMedGoogle Scholar
  41. Ramesh SA, Shin R, Eide DJ, Schachtman DP (2003) Differential metal selectivity and gene expression of two zinc transporters from rice. Plant Physiol 133:126–134CrossRefPubMedPubMedCentralGoogle Scholar
  42. Sánchez-Thomas R, Moreno-Sanchez R, Garcia-Garcia JD (2016) Accumulation of zince protects against cadmium stress in photosynthetic Euglena gracilis. Environ Exp Bot 131:19–31CrossRefGoogle Scholar
  43. Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130CrossRefGoogle Scholar
  44. Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167CrossRefPubMedPubMedCentralGoogle Scholar
  45. Sebastian A, Prasad MNV (2014) Cadmium minimization in rice. A review. Agron Sustain Dev 34:155–173CrossRefGoogle Scholar
  46. Sherbakova TA, Masyukova YA, Safonova TA et al (2005) Conserved motif CMLD in silicic acid transport proteins of diatoms. Mol Biol 39:269–280CrossRefGoogle Scholar
  47. Song A, Li P, Li Z, Fan F, Nikolic M, Liang Y (2011) The alleviation of zinc toxicity by silicon is related to zinc transport and antioxidative reactions in rice. Plant Soil 344:319–333CrossRefGoogle Scholar
  48. Sun J, Wang R, Zhang X, Yu Y, Zhao R, Li Z, Chen S (2013) Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiol Biochem 65:67–74CrossRefPubMedGoogle Scholar
  49. Szuster-Ciesielska A, Stachura A, Słotwińska M, Kamińska T, Śnieżko R, Paduch R, Abramczyk D, Filar J, Kandefer-Szerszeń M (2000) The inhibitory effect of zinc on cadmium-induced cell apoptosis and reactive oxygen species (ROS) production in cell cultures. Toxicology 145:159–171CrossRefPubMedGoogle Scholar
  50. Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK (2011) The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot 62:4843–4850CrossRefPubMedPubMedCentralGoogle Scholar
  51. Takahashi R, Bashir K, Ishimaru Y, Nishizawa NK, Nakanishi H (2012) The role of heavy-metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signal Behav 7:1605–1607CrossRefPubMedPubMedCentralGoogle Scholar
  52. Thomas J, Darvill A, Albersheim P (1989) Isolation and structural characterization of the pectic polysaccharide rhamnogalacturonan II from walls of suspension-cultured rice cells. Carbohydr Res 185:261–277CrossRefGoogle Scholar
  53. Tsai CC, Hung HH, Liu CP, Chen YT, Pan CY (2012) Changes in plasma membrane surface potential of PC12 cells as measured by Kelvin probe force microscopy. PLoS One 7:e33849CrossRefPubMedPubMedCentralGoogle Scholar
  54. Wagner JG (1993) Accumulation of cadmium in crop plants and its consequences to human health. Adv Agron 51:173–210CrossRefGoogle Scholar
  55. Wang LJ, Wang YH, Chen Q, Cao W, Li M, Zhang FS (2000) Silicon-induced cadmium tolerance of rice seedlings. J Plant Nutr 23:1397–1406CrossRefGoogle Scholar
  56. Yang JL, Zhu XF, Peng YX, Zheng C, Li GX, Liu Y, Shi YZ, Zheng SJ (2011) Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiol 155:1885–1892CrossRefPubMedPubMedCentralGoogle Scholar
  57. Ye M, Song Y, Long J, Wang R, Baerson SR, Pan Z, Zhu-Salzman K, Xie J, Cai K, Luo S, Zeng R (2013) Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proc Natl Acad Sci USA 110:E3631–E3639CrossRefPubMedPubMedCentralGoogle Scholar
  58. Yu P, Yuan J, Zhang H, Deng X, Ma M, Zhang H (2016) Engineering metal-binding sites of bacterial CusF to enhance Zn/Cd accumulation and resistance by subcellular targeting. J Hazard Mater 302:275–285CrossRefPubMedGoogle Scholar
  59. Zhang CC, Wang LJ, Nie Q, Zhang WX, Zhang FS (2008) Long-term effects of exogenous silicon on cadmium translocation and toxicity in rice (Oryza sativa L.). Environ Exp Bot 62:300–307CrossRefGoogle Scholar
  60. Zhao H, Eide D (1996) The yeast ZRT1 gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation. Proc Natl Acad Sci USA 93:2454–2458CrossRefPubMedPubMedCentralGoogle Scholar
  61. Zonia L, Munnik T (2007) Life under pressure: hydrostatic pressure in cell growth and function. Trends Plant Sci 12:90–97CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.College of Resources and EnvironmentHuazhong Agricultural UniversityWuhanChina

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