Skip to main content
SpringerLink
Log in

Cadmium Uptake, Translocation, and Tolerance in AHA1OX Arabidopsis thaliana

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Information on cadmium (Cd) uptake and transport is essential to understand better the physiology of Cd tolerance in plants. In this study, Cd uptake, translocation, and tolerance were investigated in AHA1 (Arabidopsis plasma membrane H+-ATPase gene) overexpressed plants. Exposed to 10 µM CdCl2, AHA1OX showed a higher root elongation, accumulated more Cd, and maintained better integrity of nucleus membrane of root tips in comparison to the control plant (WT), suggesting that AHA1OX was more Cd tolerant than WT. To investigate Cd tolerance mechanism of AHA1OX plants, we measured the activity of plasma membrane H+-ATPase and the secretion of citrate. Results indicated that treatment with 10 µM of Cd stimulated the activity of plasma membrane H+-ATPase and the secretion of citrate, while 30 µM of Cd inhibited them. AHA1OX had higher activity of H+-ATPase and secretion of citrate than WT. Addition of citrate enhanced root-to-shoot translocation of Cd significantly. A higher root-to-shoot Cd translocation was observed in AHA1OX than in WT plants. Treatment with low temperature or metabolic inhibitor (carbonyl cyanide m-chlorophenylhydrazone) inhibited Cd uptake and translocation. The study of Cd forms using sequential extraction indicated that Cd was mainly present as a protein-bound form, and AHA1OX had more water-soluble Cd than WT. Taken together, our results suggested that the Cd tolerance of AHA1OX was associated with its root-to-shoot Cd translocation and secretion of citrate, which converts Cd2+ into less toxic and more easily transportable forms in plant cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Ann Rev Plant Biol 53:159–182

    Article  CAS  Google Scholar 

  2. McGrath SP, Zhao FJ, Lombi E (2001) Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil 232:207–214

    Article  CAS  Google Scholar 

  3. Song WY, Martinoia E, Lee J (2004) A novel family of cys-rich membrane proteins mediates cadmium resistance in Arabidopsis. Plant Physiol 135:1027–1039

    Article  CAS  PubMed  Google Scholar 

  4. Bernard C, Roosens N, Czernic P et al (2004) A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Lett 569:140–148

    Article  CAS  PubMed  Google Scholar 

  5. Janicka-Russak M, Kabala K, burzynski M et al (2008) Response of plasma membrane H+-ATPase to heavy metal stress in Cucumis sativus roots. J Exp Bot 59:3721–3728

    Article  CAS  PubMed  Google Scholar 

  6. Li ZS, Lu YP, Zhen RG et al (1997) A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato) cadmium. Proc Natl Acad Sci U S A 94:42–47

    Article  CAS  PubMed  Google Scholar 

  7. Bovet L, Eggmann T, Meylan-Bettex M et al (2003) Transcript levels of AtMRPs after cadmium treatment: induction of AtMRP3. Plant Cell Environ 26:371–381

    Article  CAS  Google Scholar 

  8. Papoyan A, Kochian LV (2004) Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol 136:3814–3823

    Article  CAS  PubMed  Google Scholar 

  9. Guo JB, Dai XJ, Xu WZ et al (2008) Overexpressing GSH1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere 72:1020–1026

    Article  CAS  PubMed  Google Scholar 

  10. Palmgren MG (2001) Plant plasma membrane H+ -ATPases: powerhouses for nutrient uptake. Ann Rev Plant Biol 52:817–845

    Article  CAS  Google Scholar 

  11. Young JC, Krysan PJ, Sussman MR (2001) Efficient screening of Arabidopsis T-DNA insertion lines using degenerate primers. Plant Physiol 125:513–518

    Article  CAS  PubMed  Google Scholar 

  12. Wu Y, Shen H, Chen JH (2008) Aluminum-resistance of AHA1 transgenic Arabidopsis thaliana: physiological analysis. Chin J Appl Ecol 19:1125–1130

    CAS  Google Scholar 

  13. Chen JH, Shen H, Wu Y (2008) Analysis of expression pattern of AHA1 gene promoter in Arabidopsis thaliana. Plant Physiol Comm 44:87–92

    CAS  Google Scholar 

  14. Harper JF, Surowy TK, Sussman MR (1989) Molecular cloning and sequence of cDNA encoding the plasma membrane proton pump (H+-ATPase) of Arabidopsis thaliana. Proc Natl Acad Sci U S A 86:1234–1238

    Article  CAS  PubMed  Google Scholar 

  15. Shen H, He LF, Sasaki T et al (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress: up-regulation of transcription, translation and threonine-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiol 138:287–296

    Article  CAS  PubMed  Google Scholar 

  16. Sahuquilloa A, Loapez-Saancheza JF, Rubioa R et al (1999) Use of a certified reference material for extractable trace metals to assess sources of uncertainty in the BCR three-stage sequential extraction procedure. Anal Chim Acta 382:317–327

    Article  Google Scholar 

  17. Karcz W, Kurtyka R (2007) Effect of cadmium on growth, proton extrusion and membrane potential in maize coleoptile segments. Biol Plant 51:713–719

    Article  CAS  Google Scholar 

  18. Liu J, Qian M, Cai G, Zhu Q et al (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  PubMed  Google Scholar 

  19. Duarte B, Delgado M, Cacador I (2007) The role of citric acid in cadmium and nickel uptake and translocation in Halimione portulacoides. Chemosphere 69:836–840

    Article  CAS  PubMed  Google Scholar 

  20. Chen YX, Lin Q, Luo YM (2003) The role of citric acid on the phytoremediation of heavy metal contaminated soil. Chemosphere 50:807–811

    Article  CAS  PubMed  Google Scholar 

  21. Clemens S, Kim EJ, Neumann D, Schroeder JI (1999) Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J 18:3325–3333

    Article  CAS  PubMed  Google Scholar 

  22. Kupper H, Seib LO, Sivaguru M et al (2007) A method for cellular localization of gene expression via quantitative in situ hybridization in plants. Plant J 50:159–187

    Article  CAS  PubMed  Google Scholar 

  23. Pence NS, Larsen PB, Ebbs SD et al (2000) The molecular physiology of heavy metal transporter in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci U S A 97:4956–4960

    Article  CAS  PubMed  Google Scholar 

  24. Lee S, Moon JS, Ko TS et al (2003) Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiol 131:656–663

    Article  CAS  PubMed  Google Scholar 

  25. Courbot M, Willems G, Motte P (2007) A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol 144:1052–1065

    Article  CAS  PubMed  Google Scholar 

  26. Hanikenne M, Talke IN, Haydon MJ et al (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395

    Article  CAS  PubMed  Google Scholar 

  27. Alberts B, Johnson A, Lewis J et al (2001) Molecular Biology of the Cell. The Fourth Edition. NCBI Bookshelf, Phoenix, p 126

    Google Scholar 

  28. Ohno T, Nakahira S, Suzuki Y et al (2004) Molecular characterization of plasma membrane H+-ATPase in a carrot mutant cell line with enhanced citrate excretion. Physiol Plant 122:265–274

    Article  CAS  Google Scholar 

  29. Schwab AP, Zhu DS, Banks MK (2008) Influence of organic acids on the transport of heavy metals in soil. Chemosphere 72:986–994

    Article  CAS  PubMed  Google Scholar 

  30. Pollard AJ, Powell KD, Harper FA et al (2002) The genetic basis of metal hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566

    Article  CAS  Google Scholar 

  31. Ueno D, Iwashita T, Zhao FJ et al (2008) Characterization of Cd translocation and identification of the Cd form in xylem sap of the Cd-hyperaccumulator Arabidopsis halleri. Plant Cell Physiol 49:540–548

    Article  CAS  PubMed  Google Scholar 

  32. Lu LL, Tian SK, Yang XE et al (2008) Enhanced root-to-shoot translocation of cadmium in the hyperaccumulating ecotype of Sedum alfredii. J Exp Bot 59:3203–3213

    Article  CAS  PubMed  Google Scholar 

  33. Cataldo DA, Garland TR, Wildung RE (1983) Cadmium uptake kinetics in intact soybean plants. Plant Physiol 73:844–848

    Article  CAS  PubMed  Google Scholar 

  34. 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

    Article  CAS  PubMed  Google Scholar 

  35. Uraguchi S, Mori S, Kuramata M et al (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

    Article  CAS  PubMed  Google Scholar 

  36. Cosio C, Martinoia E, Keller C (2004) Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis halleri at the leaf cellular level. Plant Physiol 134:716–725

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported partially by the Opening Scientific Research Foundation of the Key State Lab of Soil and Sustainable Agriculture (grant no. 200505), the Opening Scientific Research Foundation of the Key Lab of Oil Crop Biology of the Ministry of Agriculture (grant no. 200705), National Natural Scientific Foundation of China (grant no. 30771294), and the International Foundation for Science (grant nos. C/3042–2, 3).

Author information

Authors and Affiliations

  1. Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Lingyan Hou & Weiming Shi

  2. College of Resources and Environment, South China Agricultural University, Guangzhou, 510642, China

    Lingyan Hou & Hong Shen

  3. Key Laboratory of Oil Crop Biology of the Ministry of Agriculture, Wuhan, 430062, China

    Wenhui Wei

Authors
  1. Lingyan Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weiming Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wenhui Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hong Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hong Shen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hou, L., Shi, W., Wei, W. et al. Cadmium Uptake, Translocation, and Tolerance in AHA1OX Arabidopsis thaliana . Biol Trace Elem Res 139, 228–240 (2011). https://doi.org/10.1007/s12011-010-8657-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-010-8657-6

Keywords

Search

Navigation