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Expression of the Apx gene family during leaf senescence of Arabidopsis thaliana

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Abstract

Oxygen-free radicals are thought to play an essential role in senescence. Therefore, the expression patterns of the small gene family encoding the H2O2 scavenging enzymes ascorbate peroxidase (APX; EC 1.11.1.11) were analyzed during senescence of Arabidopsis thaliana (L.) Heinh. Applying real-time RT-PCR, the mRNA levels were quantified for three cytosolic (APX1, APX2, APX6), two chloroplastic types (stromal sAPX, thylakoid tAPX), and three microsomal (APX3, APX4, APX5) isoforms identified in the genome of Arabidopsis. The genes of chloroplastic thylakoid-bound tAPX and the microsomal APX4 exhibit a strong age-related decrease of mRNA level in leaves derived from one rosette as well as in leaves derived from plants of different ages. In contrast to the tAPX, the mRNA of sAPX was only reduced in old leaves of old plants. The microsomal APX3 and APX5, and the cytosolic APX1, APX2, and APX6 did not show remarkable age-related changes in mRNA levels. The data show that expression of the individual APX genes is differentially regulated during senescence indicating possible functional specialization of respective isoenzymes. The hydrogen peroxide levels seem to be controlled very precisely in different cell compartments during plant development.

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Abbreviations

APX:

Ascorbate peroxides

CAT:

Catalase

SAG:

Senescence-associated gene

SDG:

Senescence-downregulated gene

ROS:

Reactive oxygen species

REU:

Relative expression units

References

  • Asada K (1997) The role of ascorbate peroxidase and monodehydroascorbate reductase in H2O2 scavenging in plants. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory Press, New York, pp 715–735

    Google Scholar 

  • Bowler C, Fluhr R (2000) The role of calcium and activated oxygen as signals for controlling cross-tolerance. Trends Plant Sci 5:241–246

    Article  PubMed  CAS  Google Scholar 

  • Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 307:181–199

    Article  Google Scholar 

  • Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D (2003) The molecular analysis of leaf senescence – a genomics approach. Plant Biotechnol J 1:3–22

    Article  PubMed  CAS  Google Scholar 

  • Bunkelmann JR, Trelease RN (1996) Ascorbate peroxidase: a prominent membrane protein in oilseed glyoxysomes. Plant Physiol 110:589–598

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signalling. New Phytol 146:359–388

    Article  CAS  Google Scholar 

  • Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33:691–705

    Article  PubMed  CAS  Google Scholar 

  • Gepstein S (1988) Photosynthesis. In: Nooden KD, Leopold AC (eds) Senescence and aging in plants. Academic Press Inc, San Diego, pp 85–109

    Google Scholar 

  • Hensel LL, Grbic V, Baumgarten DA, Bleeker AD (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. Plant Cell 5:553–564

    Article  PubMed  CAS  Google Scholar 

  • Jespersen HM, Kjærsgaard VH, Østergaard L, Welinder KG (1997) From sequence analysis of three novel ascorbate peroxidases from Arabidopsis thaliana to structure, function and evolution of seven types of ascorbate peroxidase. Biochem J 326:305–310

    PubMed  CAS  Google Scholar 

  • Jimenez A, Hernandez JA, Pastori G, del Rio LA, Sevilla F (1998) Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 118:1327–1335

    Article  PubMed  CAS  Google Scholar 

  • Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9:627–640

    Article  PubMed  CAS  Google Scholar 

  • Kubo A, Hikaru S, Tanaka K, Tanaka K, Kondo N (1992) Cloning and sequencing of a cDNA encoding ascorbate peroxidase from Arabidopsis thaliana. Plant Mol Biol 18:691–701

    Article  PubMed  CAS  Google Scholar 

  • Kubo A, Saji H, Tanaka K, Kondo N (1995) Expression of Arabidopsis cytosolic ascorbate peroxidase gene in response to ozone or sulfur dioxide. Plant Mol Biol 29:479–489

    Article  PubMed  CAS  Google Scholar 

  • Kurepa J, Smalle J, Van Montagu M, Inzé D (1998) Oxidative stress tolerance and longevity in Arabidopsis: the late flowering mutant gigantea is tolerant to paraquat. Plant J 14:759–764

    Article  PubMed  CAS  Google Scholar 

  • Lohmann KN, Gan S, John MC, Amasino RM (1994) Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol Plant 92:322–328

    Article  Google Scholar 

  • Lopez F, Vansuyt G, Casse-Delbart F, Fourcroy P (1996) Ascorbate peroxidase activity, not the mRNA level, is enhanced in salt-stressed Raphanus sativus plants. Physiol Plantarum 97:13–20

    Article  CAS  Google Scholar 

  • McKersie BD, Thompson JE (1978) Phase behaviour of chloroplast and microsomal membranes during leaf senescence. Plant Physiol 61:639–643

    Article  PubMed  CAS  Google Scholar 

  • Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55:853–867

    PubMed  CAS  Google Scholar 

  • Miller JD, Arteca RN, Pell EJ (1999) Senescence-associated gene expression during ozone-induced leaf senescence. Plant Physiol 120:1015–1023

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Zilinskas A (1993) Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazolium. Anal Biochem 212:540–546

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Zilinskas B (1994) Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. Plant J 5:397–405

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mullineaux P, Ball L, Escorbar C, Karpinska B, Creissen G, Karpinski S (2000) Are diverse signalling pathways integrated in the regulation of Arabidopsis antioxidant defence gene expression in response to excess excitation energy? Phil Trans Roy Soc Lond B 355:1531–1540

    Article  CAS  Google Scholar 

  • Navabpour S, Morris K, Allen R, Harrison E, Mackerness SAH, Buchanan-Wollaston V (2003) Expression of senescence-enhanced genes in response to oxidative stress. J Exp Bot 54:2285–2292

    Article  PubMed  CAS  Google Scholar 

  • Orendi G, Zimmermann P, Baar C, Zentgraf U (2001) Loss of stress-induced expression of catalase3 during leaf senescence in Arabidopsis thaliana is restricted to oxidative stress. Plant Sci 161:301–314

    Article  PubMed  CAS  Google Scholar 

  • Panchuk II, Volkov RA, Schöffl F (2002) Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129:838–853

    Article  PubMed  CAS  Google Scholar 

  • Quirino BF, Normanly J, Amasino RM (1999) Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Mol Biol 40:267–278

    Article  PubMed  CAS  Google Scholar 

  • Santos M, Gouisseau H, Lister C, Foyer C, Creissen G, Mullineaux P (1996) Cytosolic ascorbate peroxidase from Arabidopsis thaliana L. is encoded by a small multigenen family. Planta 198:64–69

    Article  PubMed  CAS  Google Scholar 

  • Scandalios JG, Guan L, Polidoros AN (1997) Catalases in plants: gene structure, properties, regulation and expression. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defense. Cold Spring Harbor Press, New York, pp 343–406

    Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  PubMed  CAS  Google Scholar 

  • Thomas H (1977) Ultrastructure, polypeptide composition and photochemical activity of chloroplasts during foliar senescence of a non-yellowing mutant genotype of Festuca pratensis Huds. Planta 137:53–60

    Article  CAS  Google Scholar 

  • Thompson JE (1988) The molecular basis for membrane deterioration during senescence. In: Nooden KD, Leopold AC (eds) Senescence and aging in plants. Academic Press Inc, San Diego, pp 52–83

    Google Scholar 

  • Vansuyt G, Lopez F, Inze D, Briat JF, Fourcroy P (1997) Iron triggers a rapid induction of ascorbate peroxidase gene expression in Brassica napus. FEBS Lett 410:195–200

    Article  PubMed  CAS  Google Scholar 

  • Volkov RA, Panchuk II, Schöffl F (2003) Heat-stress dependent and developmental modulation of gene expression: the potential of house-keeping genes as internal standards in mRNA expression profiling using real-time RT-PCR. J Exp Bot 54:2343–2349

    Article  PubMed  CAS  Google Scholar 

  • Weaver LM, Gan S, Quirino BF, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37:455–469

    Article  PubMed  CAS  Google Scholar 

  • Willekens H, Inzé D, Van Montagu M (1995) Catalases in plants. Mol Breed 1:207–228

    Article  CAS  Google Scholar 

  • Yamaguchi K, Mori H, Nishimura M (1995) A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in Pumpkin. Plant Cell Physiol 36:1157–1162

    PubMed  CAS  Google Scholar 

  • Ye ZZ, Rodriguez R, Tran A, Hoang H, de los Santos D, Brown S, Vellanoweth RL (2000) The developmental transition to flowering represses ascorbate peroxidase activity and induces enzymatic lipid peroxidation in leaf tissue in Arabidopsis thaliana. Plant Sci 158:115–127

    Article  Google Scholar 

  • Zentgraf U, Jobst J, Kolb D, Rentsch D (2004) Senescence related gene expression profiles of rosette leaves of Arabidopsis thaliana: leaf age versus plant age. Plant Biol 6:178–183

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Prof. Dr. Friedrich Schöffl, ZMBP, University of Tübingen for support and critical discussion and Heike Spiekermann for technical help. We also thank the NASC (Nottingham Arabidopsis Stock Centre, University of Nottingham, UK) for supply of Arabidopsis thaliana, ecotype Col0 seeds. This work was supported by Sonderforschungsbereich 446 of the Deutsche Forschungsgemeinschaft.

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Correspondence to Ulrike Zentgraf.

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Panchuk, I.I., Zentgraf, U. & Volkov, R.A. Expression of the Apx gene family during leaf senescence of Arabidopsis thaliana . Planta 222, 926–932 (2005). https://doi.org/10.1007/s00425-005-0028-8

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  • DOI: https://doi.org/10.1007/s00425-005-0028-8

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