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Catalase and alternative oxidase cooperatively regulate programmed cell death induced by β-glucan elicitor in potato suspension cultures

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Abstract

In potato (Solanum tuberosum L.) suspension cells, the expression of the gene encoding alternative oxidase (AOX) and H2O2 accumulation were induced by treatment with β-glucan elicitor. The inhibition of catalase activity enhanced both AOX mRNA expression and the production of H2O2, whereas the ascorbate peroxidase inhibitor did not have any effect on these responses. Simultaneous inhibition of catalase and AOX activities in elicited cells dramatically increased H2O2 accumulation, leading to the disruption of mitochondrial membrane potential (ΔΨm) and programmed cell death (PCD). The results demonstrate, for the first time, that not only AOX but also catalase plays a central role in the suppression of mitochondrial ΔΨm breakdown and PCD induced by β-glucan elicitor.

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Abbreviations

AOX :

Alternative oxidase

APX :

Ascorbate peroxidase

AT :

3-Amino-1,2,4-triazole

CAT :

Catalase

H 2 DCF-DA :

Dichlorofluorescein diacetate

p-HMB :

p-Hydroxymercuribenzoate

JC-1 :

5,5′,6,6′-Tetrachloro-1,1′,3,3′-tetraethylbenzimidazolycarbocyanine iodide

PCD :

Programmed cell death

ROS :

Reactive oxygen species

SHAM :

Salicylhydroxamic acid

ΔΨ m :

Membrane potential

Reference

  • Abe F, Kitashiba H, Kishitani S, Toriyama K (1997) Isolation of a cDNA clone encoding the alternative oxidase expressed in rice anthers. Sex Plant Reprod 10:374–375

    Google Scholar 

  • Axel M, Andrea D, Dina FT, Jurgen E (1997) Involvement of an NAD(P)H oxidase in the elicitor-inducible oxidative burst of soybean. Phytochemistry 45:1101–1107

    Google Scholar 

  • Doke N (1997) The oxidative burst: roles in signal transduction and plant stress. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory Press, New York, pp 785–813

  • Fath A, Bethke PC, Jones RL (2001) Enzymes that scavenge reactive oxygen species are down-regulated prior to gibberellic acid-induced programmed cell death in barley aleurone. Plant Physiol 126:156–166

    Google Scholar 

  • Greenberg JT (1997) Programmed cell death in plant–pathogen interactions. Annu Rev Plant Physiol Plant Mol Biol 48:525–545

    Google Scholar 

  • Lam E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411:848–853

    Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Google Scholar 

  • Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96:8271–8276

    Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Google Scholar 

  • Mittler R, Feng X, Cohen M (1998) Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco. Plant Cell 10:461–473

    Google Scholar 

  • Parsons HL, Yip JYH, Vanlerberghe GC (1999) Increased respiratory restriction during phosphate-limited growth in transgenic tobacco cells lacking alternative oxidase. Plant Physiol 121:1309–1320

    Google Scholar 

  • Pennell RI, Lamb C (1997) Programmed cell death in plants. Plant Cell 9:1157–1168

    Google Scholar 

  • Petit PX, Lecoeur H, Zorn E, Dauguet C, Mignotte B, Gougeon ML (1995) Alterations of mitochondrial membrane structure and function are early events of dexamethasone-induced thymocyte apoptosis. J Cell Biol 130:157–167

    Google Scholar 

  • Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Barr JE, Rodermel S, Inzé D, Mittler R (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J 32:329–342

    Google Scholar 

  • Robson CA, Vanlerberghe GC (2002) Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and -independent pathways of programmed cell death. Plant Physiol 129:1908–1920

    Google Scholar 

  • Shirasu K, Nakajima H, Rajasekhar VK, Dixon RA, Lamb C (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9:261–270

    Google Scholar 

  • Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, Steele GD, Chen LB (1991) Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming cation JC-1. Proc Natl Acad Sci USA 88:3671–3675

    Google Scholar 

  • Vanlerberghe GC, McIntosh L (1996) Signals regulating the expression of the nuclear gene encoding alternative oxidase of plant mitochondria. Plant Physiol 111:589–595

    Google Scholar 

  • Vanlerberghe GC, Robson CA, Yip JYH (2002) Induction of mitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death. Plant Physiol 129:1829–1842

    Google Scholar 

  • Wagner AM (1995) A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells. FEBS Lett 368:339–342

    Google Scholar 

  • Yamaguchi T, Yamada A, Hong N, Ogawa T, Ishii T, Shibuya N (2000) Differences in the recognition of glucan elicitor signals between rice and soybean: beta-glucan fragments from the rice blast disease fungus Pyricularia oryzae that elicit phytoalexin biosynthesis in suspension-cultured rice cells. Plant Cell 12:817–826

    Google Scholar 

  • Yao N, Tada Y, Sakamoto M, Nakayashiki H, Park P, Tosa Y, Mayama S (2002) Mitochondrial oxidative burst involved in apoptotic response in oats. Plant J 30:567–579

    Google Scholar 

  • Yip JYH, Vanlerberghe GC (2001) Mitochondrial alternative oxidase acts to dampen the generation of active oxygen species during a period of rapid respiration induced to support a high rate of nutrient uptake. Physiol Plant 112:327–333

    Google Scholar 

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Authors and Affiliations

  1. Faculty of Agriculture, Kobe University, Nada-ku, Kobe 657-8501, Japan

    Masashi Mizuno, Yasuomi Tada, Kimitaka Uchii, Sachiko Kawakami & Shigeyuki Mayama

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  1. Masashi Mizuno
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  2. Yasuomi Tada
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  3. Kimitaka Uchii
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  4. Sachiko Kawakami
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  5. Shigeyuki Mayama
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Correspondence to Masashi Mizuno.

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Mizuno, M., Tada, Y., Uchii, K. et al. Catalase and alternative oxidase cooperatively regulate programmed cell death induced by β-glucan elicitor in potato suspension cultures. Planta 220, 849–853 (2005). https://doi.org/10.1007/s00425-004-1402-7

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