Skip to main content
SpringerLink
Log in

Mycotoxin Ochratoxin A-induced cell death and changes in oxidative metabolism of Arabidopsis thaliana

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

We evaluated the phytotoxicity of mycotoxin ochratoxin A (OTA) from Aspergillus and Penicillium strains on Arabidopsis thaliana. The results demonstrate that the growth of Arabidopsis thaliana on media containing OTA was inhibited significantly. Moreover, OTA induced necrotic lesions in detached leaves, which are reminiscent of hypersensitive response lesions that are activated during plant–pathogen interactions and other abiotic stress factors. From our study, we can see that OTA exposure stimulated a biphasic oxidative burst in the leaves, resulting in the generation of hydrogen peroxide (H2O2) and superoxide anion radicals (O ·−2 ) and in the concomitant down-regulation of antioxidant enzyme defense responses and up-regulation of lipid peroxidation. These results suggested that OTA damage might result from reactive oxygen species pathways. Our experiments provide a useful model plant system for research on OTA-induced plant cell death.

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
Fig. 7

Similar content being viewed by others

Abbreviations

APX:

Ascorbate peroxidases

CAT:

Catalases

DAB:

3,3′-Diaminobenzidine

DON:

Deoxynivalenol

FB1:

Fumonisin B1

H2DCFDA:

2′,7′-Dichlorodihydrofluorescein diacetate

H2O2 :

Hydrogen peroxide

HR:

Hypersensitive response

MDA:

Malondialdehyde

MES:

2-(N-morpholino) ethanesulphonic acid

MS:

Murashige and Skoog

NBT:

Nitroblue tetrazolium

O ·−2 :

Superoxide anion radicals

OTA:

Ochratoxin A

PCD:

Programmed cell death

POD:

Peroxidase

PR:

Pathogenesis related

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

References

  • Abarca ML, Bragulat MR, Sastella G, Cabanes FJ (1994) Ochratoxin A production by strains of Aspergillus niger var niger. Appl Environ Microbiol 60:2650–2652

    CAS  PubMed  Google Scholar 

  • Asai T, Stone JM, Heard JE, Kovtun Y, Yorgey P, Sheen J, Ausubel FM (2000) Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell 12:1823–1835

    Article  CAS  PubMed  Google Scholar 

  • Babior BM, Benna JE, Chanock SJ, Smith RM (1997) The NADPH oxidase of leukocytes: the respiratory burst oxidase. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbour Press, Plainview, pp 737–783

    Google Scholar 

  • Boesch-Saadatmandi C, Loboda A, Jozkowicz A, Huebbe P, Blank R, Wolffram S, Dulak J, Rimbach G (2008) Effect of ochratoxin A on redox-regulated transcription factors, antioxidant enzymes and glutathione-S-transferase in cultured kidney tubulus cells. Food Chem Toxicol 46:2665–2671

    Article  CAS  PubMed  Google Scholar 

  • Bowling SA, Clarke JD, Liu YD, Klessig DF, Dong XN (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9:1573–1584

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Breisegem FV, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390

    Article  Google Scholar 

  • Ciegler A, Fennell DJ, Mintzlaff HJ, Leistner L (1972) Ochratoxin synthesis by Penicillium species. Naturwissenschaften 59:365–366

    Article  CAS  PubMed  Google Scholar 

  • Clark HA, Snedeker SM (2006) Ochratoxin A: its cancer risk and potential for exposure. J Toxicol Environ Health B Crit Rev 9:265–296

    Article  CAS  PubMed  Google Scholar 

  • Costa S, Utan A, Cervellati R, Speroni E, Guerra MC (2007) Catechins: natural free-radical scavengers against ochratoxin A-induced cell damage in a pig kidney cell line (LLC-PK1). Food Chem Toxicol 45:1910–1917

    Article  CAS  PubMed  Google Scholar 

  • Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL (1997) A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88:685–694

    Article  CAS  PubMed  Google Scholar 

  • Gechev TS, Gadjev IZ, Hille J (2004) An extensive microarray analysis of AAL-toxin-induced cell death in Arabidopsis thaliana brings new insights into the complexity of programmed cell death in plants. Cell Mol Life Sci 61:1185–1197

    Article  CAS  PubMed  Google Scholar 

  • Gechev TS, Breusegem FV, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101

    Article  CAS  PubMed  Google Scholar 

  • Greenberg JT, Guo A, Klessig DF, Ausubel FM (1994) Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77:551–563

    Article  CAS  PubMed  Google Scholar 

  • Hoeberichts FA, Woltering EJ (2002) Multiple mediators of plant programmed cell death: interplay of conserved cell death mechanisms and plant-specific regulators. BioEssays 25:47–57

    Article  CAS  Google Scholar 

  • Horie Y (1995) Productivity of ochratoxin A of Aspergillus carbonarius in Aspergillus section Nigri. Nippon King-akukai Kaiho 36:73–76

    CAS  Google Scholar 

  • Jabs T, Dietrich RA, Dang JL (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273:1853–1856

    Article  CAS  PubMed  Google Scholar 

  • Kamp HG, Eisenbrand G, Schlatter J, Würth K, Janzowski C (2005) Ochratoxin A: induction of (oxidative) DNA damage, cytotoxicity and apoptosis in mammalian cell lines and primary cells. Toxicology 206:413–425

    Article  CAS  PubMed  Google Scholar 

  • Liang ZH (2008) Detection of ochratoxin A and analysis of ochratoxingenic-fungi in foodstuff. Dissertation, China Agriculture University

  • Mahalingam R, Jambunathan N, Gunjan SK, Faustin E, Weng H, Ayoubi P (2006) Analysis of oxidative signaling induced by ozone in Arabidopsis thaliana. Plant Cell Environ 29:1357–1371

    Article  CAS  PubMed  Google Scholar 

  • Maksymiec W, Krupa Z (2006) The effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ Exp Bot 57:187–194

    Article  CAS  Google Scholar 

  • Masuda D, Ishida M, Yamaguchi K, Yamaguchi I, Kimura M, Nishiuchi T (2007) Phytotoxic effects of trichothecenes on the growth and morphology of Arabidopsis thaliana. J Exp Bot 58:1617–1626

    Article  CAS  PubMed  Google Scholar 

  • Mitterbauer R, Adam G (2002) Saccharomyces cerevisae and Arabidopsis thaliana: useful model systems for the identification of molecular mechanisms involved in resistance of plants to toxins. Eur J Plant Pathol 108:699–703

    Article  CAS  Google Scholar 

  • Nagy NE, Dalen LS, Jones DL, Swensen B, Fossdal CG, Eldhuset TD (2004) Cytological and enzymatic responses to aluminium stress in root tips of Norway spruce seedlings. New Phytol 163:595–607

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Overmyer K, Brosché M, Pellinen R, Kuittinen T, Tuominen H, Ahlfors R, Keinänen M, Saarma M, Scheel D, Kangasjärvi J (2005) Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1 mutant. Plant Physiol 137:1092–1104

    Article  CAS  PubMed  Google Scholar 

  • Paciolla C, Dipierro N, Mulè G, Logrieco A, Dipierro S (2004) The mycotoxins beauvericin and T-2 induce cell death and alteration to the ascorbate metabolism in tomato protoplasts. Physiol Mol Plant Pathol 65:49–56

    Article  CAS  Google Scholar 

  • Petrik J, Žanić-Grubišić T, Barišić K, Pepeljnjak S, Radić B, Ferenčić Ž, Čepelak I (2003) Apoptosis and oxidatice stress induced by ochratoxin A in rat kidney. Arch Toxicol 77:585–693

    Article  Google Scholar 

  • Romero-Puertas MC, Rodríguez-serrano M, Corpas FJ, Gómez M, Del Río LA, Sandalio LM (2004) Cadmium-induced subcellular accumulation of O ·−2 and H2O2 in pea leaves. Plant Cell Environ 27:1122–1134

    Article  CAS  Google Scholar 

  • Schraudner M, Moeder W, Wiese C, Camp WV, Inzé D, Langebartels C, Sandermann H Jr (1998) Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3. Plant J 16:235–245

    Article  CAS  Google Scholar 

  • Schwerdt G, Freudinger R, Mildenberger S, Silbernagl S, Gekle M (1999) The nephrotoxin ochratoxin A induces apoptosis in cultured human proximal tubule cells. Cell Biol Toxicol 15:405–415

    Article  CAS  PubMed  Google Scholar 

  • Schwerdt G, Holzinger H, Sauvant C, Königs M, Humpf HU, Gekle M (2007) Long-term effects of ochratoxin A on fibrosis and cell death in human proximal tubule or fibroblast cells in primary culture. Toxicology 232:57–67

    Article  CAS  PubMed  Google Scholar 

  • Schwerdt G, Holzinger H, Königs M, Humpf HU, Gekle M (2009) Effect of ochratoxin A on cell survival and collagen homeostasis in human mesangial cells in primary culture. Food Chem Toxicol 27:209–213

    Google Scholar 

  • Stone JM, Heard JE, Asai T, Ausubel FM (2000) Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutants. Plant Cell 12:1811–1822

    Article  CAS  PubMed  Google Scholar 

  • Van Der Merwe KJ, Steyne PS, Fourie L, Scott DB, Theron JJ (1965) Ochratoxin A, a toxic metabolite produced by Aspergillus ochraceus. Nature 205:1112–1113

    Article  PubMed  Google Scholar 

  • WHO (2001) Safety evaluation of certain mycotoxins in food, fifty-sixth meeting of the joint FAO/WHO expert committee on food additives. WHO Food Addit Ser 47:706

    Google Scholar 

  • Wohlgemuth H, Mittelstrass K, Kschieschan S, Bender J, Weigel HJ, Overmyer K, Kangasjärvi J, Sandermann H, Langebartels C (2002) Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. Plant Cell Environ 25:717–726

    Article  CAS  Google Scholar 

  • Xu WT, Peng XL, Luo YB, Wang JA, Guo X, Huang KL (2009) Physiological and biochemical responses of gragefruit seed extract dip on ‘Redglobe’ grape. LWT-Food Sci Technol 42:471–476

    Article  CAS  Google Scholar 

  • Zhang X, Boesch-Saadatmandi C, Lou Y, Wolffram S, Huebbe P, Rimbach G (2009) Ochratoxin A induces apoptosis in neuronal cells. Genes Nutr 4:41–48

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Ministry of Agriculture and the Ministry of Science and Technology of China.

Author information

Authors and Affiliations

  1. Laboratory of Fruit Physiology and Molecular Biology, College of Food Science and Nutritional Engineering, China Agricultural University, 100083, Beijing, China

    Xiao-Li Peng, Wen-Tao Xu, Yan Wang, Kun-Lun Huang, Wei-wei Zhao & Yun-Bo Luo

  2. Supervision and Testing Center of Agricultural Products Quality, Ministry of Agriculture, 100083, Beijing, China

    Wen-Tao Xu, Kun-Lun Huang & Zhi-hong Liang

Authors
  1. Xiao-Li Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wen-Tao Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kun-Lun Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhi-hong Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wei-wei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yun-Bo Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Kun-Lun Huang or Yun-Bo Luo.

Additional information

Communicated by K. Chong.

X.-L. Peng and W.-T. Xu contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 149 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peng, XL., Xu, WT., Wang, Y. et al. Mycotoxin Ochratoxin A-induced cell death and changes in oxidative metabolism of Arabidopsis thaliana . Plant Cell Rep 29, 153–161 (2010). https://doi.org/10.1007/s00299-009-0808-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-009-0808-x

Keywords

Search

Navigation