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Differential involvement of the IDRS cis-element in the developmental and environmental regulation of the AtFer1 ferritin gene from Arabidopsis

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Abstract

Four different ferritin genes have been identified in Arabidopsis thaliana, namely AtFer1, 2, 3 and 4. AtFer1, which strongly accumulates in leaves treated with excess iron, contains in its promoter an Iron-Dependent Regulatory Sequence (IDRS). The IDRS sequence is responsible for repression of AtFer1 transcription under conditions of low iron supply. Arabidopsis plants transformed with a 1,400-bp AtFer1 promoter, with either a wild-type or a mutated IDRS fused to the β-glucuronidase (GUS) reporter gene, enabled us to analyze the activity of the AtFer1 promoter in different tissues as well as during age-dependent or dark-induced senescence. Our results show that IDRS mediates AtFer1 expression during dark-induced senescence while it does not affect AtFer1 expression during age-dependent senescence or in young seedlings. Photoinhibition promoted either by high light or chilling temperature, or wounding, does not activate the AtFer1 promoter. In contrast, AtFer2, AtFer3, AtFer4 transcript abundances are increased in response to photoinhibition and AtFer3 transcript abundance is increased upon wounding. Taken together, our results indicate that other cis-elements, different from the IDRS, regulate the territory-specific or developmental expression of AtFer1 gene. Expression of this gene appears insensitive to some of the environmental stresses tested, which instead up-regulate other members of the Arabidopsis ferritin gene family.

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Abbreviations

At1400IDRS line:

Arabidopsis line transformed with a construct containing the wild-type AtFer1 1,400-bp promoter upstream of the GUS reporter gene

At1400m*IDRS line:

Arabidopsis line transformed with a construct containing the AtFer1 1,400-bp promoter with the mutated IDRS sequence

F 0 :

initial fluorescence of dark-adapted leaves

F m :

maximal fluorescence of dark-adapted leaves

F v :

variable fluorescence (F m−F 0) of dark-adapted leaves

GUS:

β-glucuronidase

JA:

jasmonic acid

IDRS:

iron dependent regulatory sequence

RT–PCR:

reverse transcription–polymerase chain reaction

WT:

wild type

References

  • Andrews SC, Smith JMA, Yewdall JR, Guest JR, Harrison PM (1991) Bacterioferritins and ferritins are distantly related in evolution. FEBS Lett 293:164–168

    Article  CAS  PubMed  Google Scholar 

  • Becker W, Apel K (1993) Differences in gene expression between natural and artificially induced leaf senescence. Planta 189:74–79

    CAS  Google Scholar 

  • Bowler C, van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    CAS  Google Scholar 

  • Briat JF, Lobreaux S (1997) Iron transport and storage in plants. Trends Plant Sci 2:187–192

    Article  Google Scholar 

  • Buchanan BB, Gruissen W, Jones RL (2000) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, MD

  • Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48:181–199

    Google Scholar 

  • Buchanan-Wollaston V, Ainsworth C (1997) Leaf senescence in Brassica napus: cloning of senescence related genes by subtractive hybridization. Plant Mol Biol 33:821–834

    Article  CAS  PubMed  Google Scholar 

  • Cairo G, Pietrangelo A (2000) Iron regulatory proteins in pathobiology. Biochem J 352:241–250

    Article  CAS  PubMed  Google Scholar 

  • Epple P, Apel K, Bohlmann H (1995) An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol 109:813–820

    CAS  PubMed  Google Scholar 

  • Gaymard F, Boucherez J, Briat JF (1996) Characterization of a ferritin mRNA from Arabidopsis thaliana accumulated in response to iron through an oxidative pathway independent of abscisic acid. Biochem J 318:67–73

    CAS  PubMed  Google Scholar 

  • Guerinot ML, Yi Y (1994) Iron: nutritious, noxious and not ready available. Plant Physiol 104:815–820

    CAS  PubMed  Google Scholar 

  • Harrison PM, Arosio P (1996) The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1275:161–203

    CAS  PubMed  Google Scholar 

  • Hinderhofer K, Zentgraf U (2001) Identification of a transcription factor specifically expressed at the onset of leaf senescence. Planta 213:469–473

    CAS  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed  Google Scholar 

  • Kim GT, Tsukaya H, Uchimiya H (1998) The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells (1998) Genes Devel 12:2381–2391

    CAS  PubMed  Google Scholar 

  • Kim S, Ponka P (2000) Effects of interferon-γ and lipopolysaccharide on macrophage iron metabolism are mediated by nitric oxide induced degradation of iron-regulatory protein-2. J Biol Chem 275:6220–6226

    Article  CAS  PubMed  Google Scholar 

  • Laulhere JP, Briat JF (1993) Iron release and uptake by plant ferritin: effects of pH, reduction and chelation. Biochem J 290:693–699

    CAS  PubMed  Google Scholar 

  • Lohman KN, Gan S, Manorama CJ, Amasino R (1994) Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol Plant 92:322–328

    Article  Google Scholar 

  • Marks MD, West J, Weeks DP (1987) The relatively large beta-tubulin gene family of Arabidopsis contains a member with an unusual transcribed 5′ noncoding sequence. Plant Mol Biol 10:91–104

    CAS  Google Scholar 

  • Matile P (2001) Senescence and cell death in plant development: chloroplast senescence and its regulation. In: Aro EM, Andersson B (eds) Regulation of photosynthesis. Kluwer, Dordrecht, The Netherlands, pp 277–296

  • Murgia I, Briat JF, Tarantino D, Soave C (2001) Plant ferritin accumulates in response to photoinhibition but its ectopic overexpression does not protect against photoinhibition. Plant Physiol Biochem 39:1–10

    Article  Google Scholar 

  • Murgia I, Delledonne M, Soave C (2002) Nitric oxide mediates iron-induced ferritin accumulation in Arabidopsis. Plant J 30:521–528

    Article  CAS  PubMed  Google Scholar 

  • Oh SA, Park JH, Lee GI, Paek SK, Park SK, Nam HG (1997) Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J 12:527–535

    CAS  PubMed  Google Scholar 

  • Petit JM, Briat JF, Lobreaux S (2001a) Structure and differential expression of the four members of the Arabidopsis thaliana ferritin gene family. Biochem J 359:575–582

    Article  CAS  PubMed  Google Scholar 

  • Petit JM, van Wuytswinkel O, Briat JF, Lobreaux S (2001b) Characterization of an iron-dependent regulatory sequence involved in the transcriptional control of AtFer1 and ZmFer1 plant ferritin genes by iron. J Biol Chem 276:5584–5590

    Article  CAS  PubMed  Google Scholar 

  • Tarantino D, Vianelli A, Carraro L, Soave C (1999) A nuclear mutant of Arabidopsis thaliana selected for enhanced sensitivity to light-chill stress is altered in PSII electron transport activity. Physiol Plant 107:361–371

    Article  CAS  Google Scholar 

  • Vignutelli A, Wasternack C, Apel K, Bohlmann H (1998) Systemic and local induction of an Arabidopsis thionin gene by wounding and pathogens. Plant J 14:285–295

    CAS  PubMed  Google Scholar 

  • Wasternack C, Parthier B (1997) Jasmonate-signalled plant gene expression. Trends Plant Sci 2:302–307

    Article  Google Scholar 

  • Wei J, Theil E (2000) Identification and characterization of a plant regulatory element in the ferritin gene of a plant (soybean). J Biol Chem 275:17488–17943

    Article  CAS  PubMed  Google Scholar 

  • Woo HR, Chung KM, Park JH, Oh SA, Ahn T, Hong SH, Jang SK, Nam HG (2001) ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13:1779–1790

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by MURST 2000 in the framework of the program "Nitric oxide and plant resistance to pathogens" and by the Centre National de la Recherche Scientifique (France).

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Authors and Affiliations

  1. Sezione di Fisiologia e Biochimica delle Piante, Dipartimento di Biologia, , via Celoria 26, 20133, Milano, Italy

    Delia Tarantino, Carlo Soave & Irene Murgia

  2. Laboratoire de Biochimie et Physiologie Moleculaire des Plantes, CNRS UMR 5004, Agro-M/INRA, 34060, Montpellier, Cedex 1, France

    Jean-Michel Petit, Stephane Lobreaux & Jean-François Briat

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  1. Delia Tarantino
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  2. Jean-Michel Petit
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  3. Stephane Lobreaux
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  4. Jean-François Briat
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  5. Carlo Soave
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  6. Irene Murgia
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Correspondence to Irene Murgia.

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Tarantino, D., Petit, JM., Lobreaux, S. et al. Differential involvement of the IDRS cis-element in the developmental and environmental regulation of the AtFer1 ferritin gene from Arabidopsis . Planta 217, 709–716 (2003). https://doi.org/10.1007/s00425-003-1038-z

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