Skip to main content
SpringerLink
Log in

Effects of Terbium (III) on Signaling Molecules in Horseradish

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

Abstract

Rare earth elements, especially terbium (Tb), are high-valence heavy metal elements that accumulate in the environment, and they show toxic effects on plants. Signaling molecules regulate many physiological and biochemical processes in plants. How rare earth elements affect signaling molecules remains largely unknown. In the present study, the effects of Tb3+ on some extracellular and intracellular signaling molecules (gibberellic acid, abscisic acid, auxin, H2O2, and Ca2+) in horseradish leaves were investigated by using high-performance liquid chromatography, X-ray energy spectrometry, and transmission electron microscopy, and Tb3+ was sprayed on the surface of leaves. Tb3+ treatment decreased the auxin and gibberellic acid contents and increased the abscisic acid content. These changes in the contents of phytohormones (gibberellic acid, abscisic acid, and auxin) triggered excessive production of intracellular H2O2. Consequently, the increase in H2O2 content stimulated the influx of extracellular Ca2+ and the release of Ca2+ from Ca2+ stores, leading to Ca2+ overload and the resulting inhibition of physiological and biochemical processes. The effects outlined above were more evident with increasing the concentration of Tb3+ sprayed on horseradish leaves. Our data provide a possible underlying mechanism of Tb3+ action on plants.

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

Similar content being viewed by others

References

  1. Redling K (2006) Rare earth elements in agriculture with emphasis on animal husbandry. Ludwig-Maximilians-Universität München, LMU München

  2. Veitch NC (2004) Horseradish peroxidase: a modern view of a classic enzyme. Phytochemistry 65(3):249–259

    Article  CAS  PubMed  Google Scholar 

  3. Guo SF, Cao R, Lu AH, Zhou Q, Lu TH, Ding XL, Li CJ, Huang XH (2008) One of the possible mechanisms for the inhibition effect of Tb(III) on peroxidase activity in horseradish (Armoracia rusticana) treated with Tb(III). J Biol Inorg Chem 13(4):587–597

    Article  CAS  PubMed  Google Scholar 

  4. Wang LH, Zhou Q, Lu TH, Ding XL, Huang XH (2010) Molecular and cellular mechanism of effect of La(III) on horseradish peroxidase. J Biol Inorg Chem 15(7):1063–1069

    Article  CAS  PubMed  Google Scholar 

  5. Guo XS, Zhou Q, Lu TH, Fang M, Huang XH (2007) Distribution and translocation of 141Ce(III) in horseradish. Ann Bot 100(7):1459–1465

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Wang LH, Zhou Q, Huang XH (2009) Photosynthetic responses to heavy metal terbium stress in horseradish leaves. Chemosphere 77(7):1019–1025

    Article  CAS  PubMed  Google Scholar 

  7. DalCorso G, Farinati S, Furini A (2010) Regulatory networks of cadmium stress in plants. Plant Signal Behav 5:663–667

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Buchanan B, Gruissem W, Jones R (2000) Biochemistry & molecular biology of plants. Wiley, New York

  9. Wang LH, Huang XH, Zhou Q (2008) Effects of rare earth elements on the distribution of mineral elements and heavy metals in horseradish. Chemosphere 73(3):314–319

    Article  CAS  PubMed  Google Scholar 

  10. Hu ZY, Richter H, Sparovek G, Schnug E (2004) Physiological and biochemical effects of rare earth elements on plants and their agricultural significance: a review. J Plant Nutr 27:183–220

    Article  CAS  Google Scholar 

  11. Wang LH, Zhou Q, Huang XH (2010) Effects of heavy metal terbium on contents of cytosolic nutrient elements in horseradish cell. Ecotoxicol Environ Saf 73(5):1012–1017

    Article  CAS  PubMed  Google Scholar 

  12. Lichtenthaler H (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148(2):350–382

    Article  CAS  Google Scholar 

  13. Shah K, Kumar R, Verma S, Dubey R (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144

    Article  CAS  Google Scholar 

  14. Hammerschmidt R, Nuckles E, Kug J (1982) Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium. Physiol Plant Pathol 20:77–82

    Google Scholar 

  15. Ma Z, Ge L, Lee ASY, Yong JWH, Tan SN, Ong ES (2008) Simultaneous analysis of different classes of phytohormones in coconut (Cocos nucifera L.) water using high-performance liquid chromatography and liquid chromatography–tandem mass spectrometry after solid-phase extraction. Anal Chim Acta 610(2):274–281

    Article  CAS  PubMed  Google Scholar 

  16. Bóka K, Orbán N, Kristóf Z (2007) Dynamics and localization of H2O2 production in elicited plant cells. Protoplasma 230:89–97

    Article  PubMed  Google Scholar 

  17. Pellinen R, Palva T, Kangasjarvi J (1999) Subcellular localization of ozone-induced hydrogen peroxide production in birch (Betula pendula) leaf cells. Plant J 20:349–356

    Article  CAS  PubMed  Google Scholar 

  18. Bestwick CS, Brown IR, Bennett MHR, Mansfield JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 9(2):209–221

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Slezak J, Tribulova N, Pristacova J, Uhrik B, Thomas T, Khaper N, Kaul N, Singal P (1995) Hydrogen peroxide changes in ischemic and reperfused heart. Cytochemistry and biochemical and X-ray microanalysis. Am J Pathol 147(3):772–781

    PubMed Central  CAS  PubMed  Google Scholar 

  20. Tian HQ, Kuang A, Musgrave ME, Russell SD (1998) Calcium distribution in fertile and sterile anthers of a photoperiod-sensitive genic male-sterile rice. Planta 204(2):183–192

    Article  CAS  Google Scholar 

  21. Wang S, Tiwari S, Hagen G, Guilfoyle T (2005) Auxin response factor 7 restores the expression of auxin-responsive genes in mutant Arabidopsis leaf mesophyll protoplasts. Plant Cell 17(7):1979

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Kovtun Y, Chiu WL, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci U S A 97:2940–2945

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Minamiguchi K, Kumagai H, Masuda T, Kawada M, Ishizuka M, Takeuchi T (2001) Thiolutin, an inhibitor of HUVEC adhesion to vitronectin, reduces paxillin in HUVECs and suppresses tumor cell induced angiogenesis. Int J Cancer 93:307–316

    Article  CAS  PubMed  Google Scholar 

  24. Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Biol 49:199–222

    Article  CAS  Google Scholar 

  25. Fan L, Feng X, Wang Y, Deng X (2007) Gibberellin signal transduction in rice. J Integr Plant Biol 49:731

    Article  CAS  Google Scholar 

  26. Macdonald H (1997) Auxin perception and signal transduction. Physiol Planta 100:423–430

    Article  CAS  Google Scholar 

  27. Raven P, Evert R, Eichhorn S (2004) Biology of plants. WH Freeman, New York

  28. He H, Serraj R, Yang Q (2009) Changes in OsXTH gene expression, ABA content, and peduncle elongation in rice subjected to drought at the reproductive stage. Acta Physiol Plant 31:749–756

    Article  CAS  Google Scholar 

  29. Kutlu N, Terzi R, Tekeli C, Senel G, Battal P, Kadioglu A (2009) Changes in anatomical structure and levels of endogenous phytohormones during leaf rolling in Ctenanthe setosa under drought stress. Turk J Biol 33:115–122

    CAS  Google Scholar 

  30. Guan L, Zhao J, Scandalios J (2000) Cis-elements and trans-factors that regulate expression of the maize Cat 1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J 22:87–95

    Article  CAS  PubMed  Google Scholar 

  31. Joo J, Bae Y, Lee J (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 126(3):1055–1060

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Kwak JM, Nguyen V, Schroeder JI (2006) The role of reactive oxygen species in hormonal responses. Plant Physiol 141(2):323–329

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406(6797):731–734

    Article  CAS  PubMed  Google Scholar 

  34. Peters SC, Piper HM (2007) Reoxygenation-induced Ca2+ rise is mediated via Ca2+ influx and Ca2+ release from the endoplasmic reticulum in cardiac endothelial cells. Cardiovasc Res 73(1):164–171

    Article  CAS  PubMed  Google Scholar 

  35. Chen WP, Li PH (2001) Chilling-induced Ca2+ overload enhances production of active oxygen species in maize (Zea mays L.) cultured cells: the effect of abscisic acid treatment. Plant Cell Environ 24(8):791–800

    Article  CAS  Google Scholar 

  36. Gasbarrini A, Borle AB, Farghali H, Bender C, Francavilla A, Vanthiel D (1992) Effect of anoxia on intracellular ATP, Na+(I), Ca2+(I), Mg2+(I), and cytotoxicity in rat hepatocytes. J Biol Chem 267(10):6654–6663

    CAS  PubMed  Google Scholar 

  37. Hall KE, Browning MD, Dudek EM, Macdonald RL (1995) Enhancement of high-threshold calcium currents in rat primary afferent neurons by constitutively active protein-kinase-C. J Neurosci 15(9):6069–6076

    CAS  PubMed  Google Scholar 

  38. Janeczek AH, Vanalten PJ, Reyes HM, Walter RJ (1993) Modulation of the cytoskeleton and intracellular calcium in leukocytes exhibiting a cancer-associated chemotaxis defect. J Leukoc Biol 54(4):351–359

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful for the financial support of the National Natural Science Foundation of China (31170477, 21371100), the Foundation of the State Development and Reforming Committee (GFZ2071609), the Natural Science Foundation of Jiangsu Province (BK2011160, BK2009401), and Research and Innovation Project for Postgraduate of Higher Education Institutions of Jiangsu Province in 2012 (CXZZ12_0760).

Author information

Authors and Affiliations

  1. State Key Laboratory of Food Science and Technology, School of Environmental and Civil Engineering, Jiangnan University, Wuxi, 214122, China

    Lihong Wang, Xuanbo Zhang & Qing Zhou

  2. Jiangsu Collaborative Innovation Center of Biomedical Functional Materials, Jiangsu Key Laboratory of Biomedical Materials, College of Chemistry and Materials Science, Nanjing Normal University, Nanjing, 210046, China

    Xiaohua Huang

Authors
  1. Lihong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xuanbo Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qing Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaohua Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Qing Zhou or Xiaohua Huang.

Additional information

Lihong Wang and Xianbo Zhang contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, L., Zhang, X., Zhou, Q. et al. Effects of Terbium (III) on Signaling Molecules in Horseradish. Biol Trace Elem Res 164, 122–129 (2015). https://doi.org/10.1007/s12011-014-0209-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-014-0209-z

Keywords

Search

Navigation