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Differential expression of ferritin genes in response to abiotic stresses and hormones in pear (Pyrus pyrifolia)

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Abstract

In this study, the expression patterns of four ferritin genes (PpFer1, PpFer2, PpFer3, and PpFer4) in pear were investigated using quantitative real-time PCR. Analysis of tissue-specific expression revealed higher expression level of these genes in leaves than in other tested tissues. These ferritin genes were differentially expressed in response to various abiotic stresses and hormones treatments. The expression of ferritin wasn’t affected by Fe(III)-citrate treatment. Abscisic acid significantly enhanced the expression of all four ferritin genes, especially PpFer2, followed by N-benzylyminopurine, gibberellic acid, and indole-3-acetic acid. The expression peaks of PpFer1 and PpFer3 in leaves appeared at 6, 6, and 12 h, respectively, after pear plant was exposed to oxidative stress (5 mM H2O2), salt stress (200 mM NaCl), and heat stress (40°C). A significant increase in PpFer4 expression was detected at 6 h after salt stress or heat stress. The expression of ferritin genes was not altered by cold stress. These results suggested that ferritin genes might be functionally important in acclimation of pear to salt and oxidative stresses. Hormone treatments had no significant effect on expression of ferritin genes compared to abiotic stresses. This showed accumulation of ferritin genes could be operated by different transduction pathways under abiotic stresses and hormones treatments.

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References

  1. Theil EC (1987) Ferritin: structure, gene regulation, and cellular function in animals, plants, and microorganisms. Annu Rev Biochem 56:289–315

    Article  PubMed  CAS  Google Scholar 

  2. Cario G, Rappocciolo E, Tacchini L, Schiaffonati L (1991) Expression of the genes for the ferritin H and L subunits in rat liver and heart: evidence for tissue-specific regulations at pre- and post translational levels. Biochem J 275:813–816

    Google Scholar 

  3. Wilkinsonr J, Di X, Schonig K et al (2006) Tissue specific expression of ferritin H regulates cellular iron homeostasis in vivo. Biochem J 395:501–507

    Article  Google Scholar 

  4. Hentze MW, Kuhn LC (1996) Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron nitric oxide and oxidative stress. Proc Natl Acad Sci USA 93:8175–8182

    Article  PubMed  CAS  Google Scholar 

  5. Lescure AM, Proudhon D, Pesey H et al (1991) Ferritin gene transcription is regulated by iron in soybean cell cultures. Proc Natl Acad Sci USA 88:8222–8226

    Article  PubMed  CAS  Google Scholar 

  6. Wei JZ, Theil EC (2000) Identification and characterization of the iron regulatory element in the ferritin gene of a plant (soybean). J Biol Chem 275:17488–17493

    Article  PubMed  CAS  Google Scholar 

  7. Petit JM, van Wuytswinkel O, Briat JF, Lobreaux S (2001) Characterization of an iron-dependent regulatory sequence involved in the transcriptional control of AtFer1 and ZmFer1 plant ferritin genes by iron. J Biol Chem 276:5580–5590

    Google Scholar 

  8. Lobreèaux S, Massenet O, Brait JF (1992) Iron induces ferritin synthesis in maize plantlets. Plant Mol Biol 19:563–575

    Article  Google Scholar 

  9. Wicks RE, Entsch B (1993) Functional genes found for three different plant ferritin subunits in the legume, Vigna unguiculata. Biochem Biophys Res Commun 192:813–819

    Article  PubMed  CAS  Google Scholar 

  10. Wardrop AJ, Wicks RE, Entsch B (1999) Occurrence and expression of members of the ferritin gene family in cowpeas. Biochem J 337:523–530

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  12. Strozycki PM, Skapska A, Szczesniak K et al (2003) Differential expression and evolutionary analysis of the three ferritin genes in the legume plant Lupinus luteus. Physiol Plant 118:380–389

    Article  CAS  Google Scholar 

  13. Jiang TB (2005) Isolation and expression pattern analysis of two ferritin genes in tobacco. J Integr Plant Biol. doi: 10.1111/j.1744-7909.2005.00044.x

  14. Aziz N, Munro HN (1987) Iron regulates ferritin mRNA translation through a segment of its 5′ un-translation region. Proc Natl Acad Sci USA 84:8478–8482

    Article  PubMed  CAS  Google Scholar 

  15. Torti SV, Kwak EL, Miller SC et al (1988) The molecular cloning and characterization of murine ferritin heavy chain, a tumor necrosis factor inducible gene. J Biol Chem 263:12638–12644

    PubMed  CAS  Google Scholar 

  16. Colucci-D’Amato LG, Ursini MV, Colletta G et al (1989) Thyrotropin stimulates transcription from the ferritin heavy chain promoter. Biochem Biophys Res Commun 165:506–511

    Article  PubMed  Google Scholar 

  17. Yokomori N, Iwasa Y, Aida K et al (1991) Transcriptional regulation of ferritin messenger ribonucleic acid levels by insulin in cultured rat glioma cells. Endocrinology 128:1474–1480

    Article  PubMed  CAS  Google Scholar 

  18. Bevilacqua MA, Faniello MC, Russo T, Cimino F, Costanzo F (1994) Transcriptional regulation of the human H-ferritin encoding gene (FERH) in G418-treated cells: role of the B-box-binding factor. Gene 141:287–291

    Article  PubMed  CAS  Google Scholar 

  19. Tsolova V, Atanassov A (1994) Plant regeneration of Vitis sp. via repetitive embryogenesis. Biotechnol Biotechnol Equip 10:32–36

    Google Scholar 

  20. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  21. Cataldo DA, Mc Fadden KM, Garland TR, Wildung RE (1998) Organic constituents and complexation of nickel, iron, cadmium and plutonium in soybean exudates. Plant Physiol 86:734–739

    Article  Google Scholar 

  22. Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Reptr 11:113–116

    Article  CAS  Google Scholar 

  23. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  24. Wittwer CT, Herrmann MG, Moss AA, Rasmussen RP (1997) Continuous fluorescence monitoring of rapid cycle DNA amplification. Biotechniques 22:130–138

    PubMed  CAS  Google Scholar 

  25. Morrison TB, Weis JJ, and Wittwer CT (1998) Quantification of low-copy transcripts by continuous SYBR Green I monitoring during amplification. Biotechniques 24:954–958, 960, 962

    Google Scholar 

  26. Kampfenkel K, Van Montagu M, Inzè D (1995) Effects of iron excess on Nicotiana plumbaginifolia plants (implications to oxidative stress. Plant Physiol 107:725–735

    PubMed  CAS  Google Scholar 

  27. Durand JP, Goudard F, Pieri J et al (2004) Crassostrea gigas ferritin: cDNA sequence analysis for two heavy chain type subunits and protein purification. Gene 338:187–195

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  29. Lobreèaux S, Thoiron S, Briat JF (1995) Induction of ferritin synthesis in maize leaves by an iron-mediated oxidative stress. Plant J 8:443–449

    Article  Google Scholar 

  30. 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

    PubMed  CAS  Google Scholar 

  31. Klausner RD, Rouault TA, Harford JB (1993) Regulating the fate of mRNA: the control of cellular iron metabolism. Cell 72:19–28

    Article  PubMed  CAS  Google Scholar 

  32. Georgieva T, Dunkov BC, Dimov S et al (2002) Drosophila melanogaster ferritin: cDNA encoding a light chain homologue, temporal and tissue specific expression of both subunit types. Insect Biochem Mol Biol 32:295–302

    Article  PubMed  CAS  Google Scholar 

  33. Geiser DL, Mayo JJ, Winzerling JJ (2007) The unique regulation of Aedes aegypti larval cell ferritin by iron. Insect Biochem Mol Biol 37:418–429

    Article  PubMed  CAS  Google Scholar 

  34. Ong DS, Wang L, Zhu Y et al (2005) The response of ferritin to LPS and acute phase of pseudomonas infection. J Endotoxin Res 11:267–280

    PubMed  CAS  Google Scholar 

  35. Kopáček P, Ždychová J, Yoshiga T et al (2003) Molecular cloning, expression and isolation of ferritins from two tick species Ornithodoros moubata and Ixodes ricinus. Insect Biochem Mol Biol 33:103–113

    Article  PubMed  Google Scholar 

  36. Savino G, Briat JF, Lobreaux S (1997) Inhibition of the iron-induced ZmFer1 maize ferritin gene expression by antioxidants and serine/threonine phosphatase inhibitors. J Biol Chem 272:33319–33326

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  38. Lobreèaux S, Hardy T, Briat JF (1993) Abscisic acid is involved in the iron-induced synthesis of maize ferritin. EMBO J 12:651–657

    Google Scholar 

  39. Fobis-Loisy I, Loridon K, Lebrun M, Briat JF (1995) Structure and differential expression of two maize ferritin genes in response to iron and abscisic acid. Eur J Biochem 231:609–619

    Article  PubMed  CAS  Google Scholar 

  40. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  PubMed  CAS  Google Scholar 

  41. Viswanathan C, Zhu JK (2002) Molecular genetic analysis of cold-regulated gene transcription. Philos Trans R Soc Lond B 357:877–886

    Article  CAS  Google Scholar 

  42. Tsuji Y, Ayaki H, Whitman SP et al (2000) Coordinate transcriptional and translational regulation of ferritin in response to oxidative stress. Mol Cell Biol 20:5818–5827

    Article  PubMed  CAS  Google Scholar 

  43. Hintze KJ, Theil EC (2005) DNA and mRNA elements with complementary responses to hemin, antioxidant inducers, and iron control ferritin-L expression. Proc Natl Acad Sci USA 102:15048–15052

    Article  PubMed  CAS  Google Scholar 

  44. Iwasaki K, Mackenzie EL, Hailemariam K et al (2006) Hemin-mediated regulation of an antioxidant-responsive element of the human ferritin H gene and role of Ref-1 during erythroid differentiation of K562 cells. Mol Cell Biol 26:2845–2856

    Article  PubMed  CAS  Google Scholar 

  45. Bowler C, Alliotte T, De Loose M et al (1989) The induction of manganese superoxide dismutase in response to stress in Nicotiana plumbaginifolia. EMBO J 8:31–38

    PubMed  CAS  Google Scholar 

  46. Yang R, Deng C, Ouyang B, Ye Z (2010) Molecular analysis of two salt-responsive NAC-family genes and their expression analysis in tomato. Mol Biol Rep. doi: 10.1007/s11033-010-0177-0

  47. Gao JJ, Zhang Z, Peng RH et al. (2010) Forced expression of Mdmyb10, a myb transcription factor gene from apple, enhances tolerance to osmotic stress in transgenic Arabidopsis. Mol Biol Rep. doi: 10.1007/s11033-010-0096-0

  48. Epsztejn S, Glickstein H, Picard V et al (1999) H-ferritin subunit overexpression in erythroid cells reduces the oxidative stress response and induces multidrug resistance properties. Blood 94:3593–3603

    PubMed  CAS  Google Scholar 

  49. Orino K, Lehman L, Tsuji Y et al (2001) Ferritin and the response to oxidative stress. Biochem J 357:241–247

    Article  PubMed  CAS  Google Scholar 

  50. Goto F, Yoshihara T, Saiki H (1998) Iron accumulation in tobacco plants expressing soya bean ferritin gene. Transgenic Res 7:173–180

    Article  CAS  Google Scholar 

  51. Deák M, Horváth GV, Devletova S et al (1999) Plants ectopically expressing the iron-binding protein, ferritin, are tolerant to oxidative damage and pathogens. Nat Biotechnol 17:192–196

    Article  PubMed  Google Scholar 

  52. Van Wuytswinkel O, Vansuyt G, Grignon N et al (1999) Iron homeostasis alternation in transgenic tobacco overexpressing ferritin. Plant J 17:93–97

    Article  PubMed  Google Scholar 

  53. Vasconcelos M, Datta K, Oliva N et al (2003) Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. Plant Sci 164:371–378

    Article  CAS  Google Scholar 

  54. Lin F, Girotti AW (1998) Hemin-enhanced resistance of human leukemia cells to oxidative killing: antisense determination of ferritin involvement. Arch Biochem Biophys 352:51–58

    Article  PubMed  CAS  Google Scholar 

  55. Hekimi S, Guarente L (2003) Genetics and the specificity of the aging process. Science 299:1351–1354

    Article  PubMed  CAS  Google Scholar 

  56. Liu DJ, Chen JY, Lu WJ (2010) Expression and regulation of the early auxin-responsive Aux/IAA genes during strawberry fruit development. Mol Biol Rep. doi:10.1007/s11033-010-0216-x

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Acknowledgments

The authors thank all lab members, particularly, Zhaoguo Tong, for their assistance and suggestions when they were conducting the research. They are highly grateful to Dr. Xia Ye for her critical comments when they were preparing this manuscript. This work was supported by National and Jiangsu Provincial Program for High Technology Research and Development in China (Nos.: 2006AA100108, BG2006313).

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Correspondence to Zhen Zhang.

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Xi, L., Xu, K., Qiao, Y. et al. Differential expression of ferritin genes in response to abiotic stresses and hormones in pear (Pyrus pyrifolia). Mol Biol Rep 38, 4405–4413 (2011). https://doi.org/10.1007/s11033-010-0568-2

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