Skip to main content

Advertisement

SpringerLink
Log in

RceIF5A, encoding an eukaryotic translation initiation factor 5A in Rosa chinensis, can enhance thermotolerance, oxidative and osmotic stress resistance of Arabidopsis thaliana

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Eukaryotic translation initiation factor 5A (eIF5A) is the only cellular protein known to contain the unusual amino acid hypusine. It is a highly conserved protein found in all eukaryotic organisms. Although originally identified as a translation initiation factor, recent studies suggest that eIF5A is mainly involved in translation elongation, mRNA turnover and decay, cell proliferation, and programmed cell death. However, the precise cellular function of eIF5A remains largely unknown, especially in plants. Here, we report the identification and characterization of RceIF5A from Rosa chinensis. RceIF5A expression is up-regulated in Rosa chinensis under high temperature, and oxidative and osmotic stress conditions. We produced transgenic Arabidopsis that constitutively enhanced or suppressed expression of RceIF5A. The RceIF5A over-expression plants exhibited increased resistance to heat, and oxidative and osmotic stresses, while the suppressed expression plants (three AteIF5A isoforms in Arabidopsis were down-regulated) showed more susceptibility to these stresses. These results reveal a new physiological role for eIF5A in plants and contribute to the elucidation of the molecular mechanisms involved in the stress response pathway.

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

References

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39 (0032-079X):205–207

    Google Scholar 

  • Bevec D, Hauber J (1997) Eukaryotic initiation factor 5a activity and hiv-1 rev function. Biol Signals 6(3):124–133

    Article  PubMed  CAS  Google Scholar 

  • Chamot D, Kuhlemeier C (1992) Differential expression of genes encoding the hypusine-containing translation initiation factor, eif-5a, in tobacco. Nucleic Acids Res 20(4):665–669

    Article  PubMed  CAS  Google Scholar 

  • Chan KL, New D, Ghandhi S, Wong F, Lam CM, Wong JT (2002) Transcript levels of the eukaryotic translation initiation factor 5a gene peak at early g(1) phase of the cell cycle in the dinoflagellate crypthecodinium cohnii. Appl Environ Microbiol 68(5):2278–2284

    Article  PubMed  CAS  Google Scholar 

  • Chou WC, Huang YW, Tsay WS, Chiang TY, Huang DD, Huang HJ (2004) Expression of genes encoding the rice translation initiation factor, eif5a, is involved in developmental and environmental responses. Physiol Plant 121(1):50–57

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743

    Article  PubMed  CAS  Google Scholar 

  • Cooper HL, Park MH, Folk JE, Safer B, Braverman R (1983) Identification of the hypusine-containing protein hy+ as translation initiation factor eif-4d. Proc Natl Acad Sci USA 80(7):1854–1857

    Article  PubMed  CAS  Google Scholar 

  • Dhindsa RA, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 126:93–101

    Article  Google Scholar 

  • Dresselhaus T, Cordts S, Lorz H (1999) A transcript encoding translation initiation factor eif-5a is stored in unfertilized egg cells of maize. Plant Mol Biol 39(5):1063–1071

    Article  PubMed  CAS  Google Scholar 

  • Duguay J, Jamal S, Liu Z, Wang TW, Thompson JE (2007) Leaf-specific suppression of deoxyhypusine synthase in Arabidopsis thaliana enhances growth without negative pleiotropic effects. J Plant Physiol 164(4):408–420

    Article  PubMed  CAS  Google Scholar 

  • Elfgang C, Rosorius O, Hofer L, Jaksche H, Hauber J, Bevec D (1999) Evidence for specific nucleocytoplasmic transport pathways used by leucine-rich nuclear export signals. Proc Natl Acad Sci USA 96(11):6229–6234

    Article  PubMed  CAS  Google Scholar 

  • Feng H, Chen Q, Feng J, Zhang J, Yang X, Zuo J (2007) Functional characterization of the Arabidopsis eukaryotic translation initiation factor 5a-2 that plays a crucial role in plant growth and development by regulating cell division, cell growth, and cell death. Plant Physiol 144(3):1531–1545

    Article  PubMed  CAS  Google Scholar 

  • Gao Y, Chen Y (2000) Advances in the study of the effects of danggui buxue decoction and its modified recipes on immunity and hematopoietic function. Zhong Yao Cai 23(3):177–180

    PubMed  CAS  Google Scholar 

  • Gordon ED, Mora R, Meredith SC, Lee C, Lindquist SL (1987) Eukaryotic initiation factor 4d, the hypusine-containing protein, is conserved among eukaryotes. J Biol Chem 262(34):16585–16589

    PubMed  CAS  Google Scholar 

  • Gregio AP, Cano VP, Avaca JS, Valentini SR, Zanelli CF (2009) Eif5a has a function in the elongation step of translation in yeast. Biochem Biophys Res Commun 380(4):785–790

    Article  PubMed  CAS  Google Scholar 

  • Hanauske-Abel HM, Park MH, Hanauske AR, Popowicz AM, Lalande M, Folk JE (1994) Inhibition of the g1-s transition of the cell cycle by inhibitors of deoxyhypusine hydroxylation. Biochim Biophys Acta 1221(2):115–124

    Article  PubMed  CAS  Google Scholar 

  • Hanawa-Suetsugu K, Sekine S, Sakai H, Hori-Takemoto C, Terada T, Unzai S, Tame JR, Kuramitsu S, Shirouzu M, Yokoyama S (2004) Crystal structure of elongation factor p from thermus thermophilus hb8. Proc Natl Acad Sci USA 101(26):9595–9600

    Article  PubMed  Google Scholar 

  • Hershey JW, Smit-McBride Z, Schnier J (1990) The role of mammalian initiation factor eif-4d and its hypusine modification in translation. Biochim Biophys Acta 1050(1–3):160–162

    PubMed  CAS  Google Scholar 

  • Hopkins MT, Lampi Y, Wang TW, Liu Z, Thompson JE (2008) Eif5a is involved in pathogen-induced cell death and development of disease symptoms in Arabidopsis thaliana. Plant Physiol 148(1):479–489

    Article  PubMed  CAS  Google Scholar 

  • Jao DL, Yu Chen K (2002) Subcellular localization of the hypusine-containing eukaryotic initiation factor 5a by immunofluorescent staining and green fluorescent protein tagging. J Cell Biochem 86(3):590–600

    Article  PubMed  CAS  Google Scholar 

  • Jiang R, Hu YH, Jiang CH, Zhao HW, Hu SL, Ming F (2006) 2d-page analysis of Chinese rose leaf protein under heat shock stress. China Biotechnol 26:91–94

    CAS  Google Scholar 

  • Kang HA, Hershey JW (1994) Effect of initiation factor eif-5a depletion on protein synthesis and proliferation of saccharomyces cerevisiae. J Biol Chem 269(6):3934–3940

    PubMed  CAS  Google Scholar 

  • Kang HA, Schwelberger HG, Hershey JW (1993) Translation initiation factor eif-5a, the hypusine-containing protein, is phosphorylated on serine in saccharomyces cerevisiae. J Biol Chem 268(20):14750–14756

    PubMed  CAS  Google Scholar 

  • Kemper WM, Berry KW, Merrick WC (1976) Purification and properties of rabbit reticulocyte protein synthesis initiation factors m2balpha and m2bbeta. J Biol Chem 251(18):5551–5557

    PubMed  CAS  Google Scholar 

  • Kyrpides NC, Woese CR (1998) Universally conserved translation initiation factors. Proc Natl Acad Sci USA 95(1):224–228

    Article  PubMed  CAS  Google Scholar 

  • Lebska M, Ciesielski A, Szymona L, Godecka L, Lewandowska-Gnatowska E, Szczegielniak J, Muszynska G (2010) Phosphorylation of maize eukaryotic translation initiation factor 5a (eif5a) by casein kinase 2: identification of phosphorylated residue and influence on intracellular localization of eif5a. J Biol Chem 285(9):6217–6226

    Article  PubMed  CAS  Google Scholar 

  • Liu Z, Duguay J, Ma F, Wang TW, Tshin R, Hopkins MT, McNamara L, Thompson JE (2008) Modulation of eif5a1 expression alters xylem abundance in Arabidopsis thaliana. J Exp Bot 59(4):939–950

    Article  PubMed  CAS  Google Scholar 

  • Mehta AM, Saftner RA, Mehta RA, Davies PJ (1994) Identification of posttranslationally modified 18-kilodalton protein from rice as eukaryotic translation initiation factor 5a. Plant Physiol 106(4):1413–1419

    PubMed  CAS  Google Scholar 

  • Mendoza I, Rubio F, Rodriguez-Navarro A, Pardo JM (1994) The protein phosphatase calcineurin is essential for nacl tolerance of saccharomyces cerevisiae. J Biol Chem 269(12):8792–8796

    PubMed  CAS  Google Scholar 

  • Park MH (1989) The essential role of hypusine in eukaryotic translation initiation factor 4d (eif-4d). Purification of eif-4d and its precursors and comparison of their activities. J Biol Chem 264(31):18531–18535

    PubMed  CAS  Google Scholar 

  • Park MH, Chung SI, Cooper HL, Folk JE (1984) The mammalian hypusine-containing protein, eukaryotic initiation factor 4d. Structural homology of this protein from several species. J Biol Chem 259(7):4563–4565

    PubMed  CAS  Google Scholar 

  • Park MH, Wolff EC, Folk JE (1993a) Hypusine: its post-translational formation in eukaryotic initiation factor 5a and its potential role in cellular regulation. Biofactors 4(2):95–104

    PubMed  CAS  Google Scholar 

  • Park MH, Wolff EC, Folk JE (1993b) Is hypusine essential for eukaryotic cell proliferation? Trends Biochem Sci 18(12):475–479

    Article  PubMed  CAS  Google Scholar 

  • Park MH, Lee YB, Joe YA (1997) Hypusine is essential for eukaryotic cell proliferation. Biol Signals 6(3):115–123

    Article  PubMed  CAS  Google Scholar 

  • Pay A, Heberle-Bors E, Hirt H (1991) Isolation and sequence determination of the plant homologue of the eukaryotic initiation factor 4d cdna from alfalfa, medicago sativa. Plant Mol Biol 17(4):927–929

    Article  PubMed  CAS  Google Scholar 

  • Requejo R, Tena M (2006) Maize response to acute arsenic toxicity as revealed by proteome analysis of plant shoots. Proteomics 6(Suppl 1):S156–S162

    Article  PubMed  Google Scholar 

  • Rosorius O, Reichart B, Kratzer F, Heger P, Dabauvalle MC, Hauber J (1999) Nuclear pore localization and nucleocytoplasmic transport of eif-5a: Evidence for direct interaction with the export receptor crm1. J Cell Sci 112(Pt 14):2369–2380

    PubMed  CAS  Google Scholar 

  • Saini P, Eyler DE, Green R, Dever TE (2009) Hypusine-containing protein eif5a promotes translation elongation. Nature 459(7243):118–121

    Article  PubMed  CAS  Google Scholar 

  • Schrader R, Young C, Kozian D, Hoffmann R, Lottspeich F (2006) Temperature-sensitive eif5a mutant accumulates transcripts targeted to the nonsense-mediated decay pathway. J Biol Chem 281(46):35336–35346

    Article  PubMed  CAS  Google Scholar 

  • Sharom M, Willemot C, Thompson JE (1994) Chilling injury induces lipid phase changes in membranes of tomato fruit. Plant Physiol 105(1):305–308

    PubMed  CAS  Google Scholar 

  • Shi XP, Yin KC, Ahern J, Davis LJ, Stern AM, Waxman L (1996) Effects of n1-guanyl-1, 7-diaminoheptane, an inhibitor of deoxyhypusine synthase, on the growth of tumorigenic cell lines in culture. Biochim Biophys Acta 1310(1):119–126

    Article  PubMed  Google Scholar 

  • Tang W, Charles TM, Newton RJ (2005) Overexpression of the pepper transcription factor capf1 in transgenic virginia pine (pinus virginiana mill.) confers multiple stress tolerance and enhances organ growth. Plant Mol Biol 59(4):603–617

    Article  PubMed  CAS  Google Scholar 

  • Thompson JE, Hopkins MT, Taylor C, Wang TW (2004) Regulation of senescence by eukaryotic translation initiation factor 5a: implications for plant growth and development. Trends Plant Sci 9(4):174–179

    Article  PubMed  CAS  Google Scholar 

  • Wang TW, Lu L, Wang D, Thompson JE (2001) Isolation and characterization of senescence-induced cdnas encoding deoxyhypusine synthase and eucaryotic translation initiation factor 5a from tomato. J Biol Chem 276(20):17541–17549

    Article  PubMed  CAS  Google Scholar 

  • Wang TW, Lu L, Zhang CG, Taylor C, Thompson JE (2003) Pleiotropic effects of suppressing deoxyhypusine synthase expression in Arabidopsis thaliana. Plant Mol Biol 52(6):1223–1235

    Article  PubMed  CAS  Google Scholar 

  • Wang TW, Zhang CG, Wu W, Nowack LM, Madey E, Thompson JE (2005) Antisense suppression of deoxyhypusine synthase in tomato delays fruit softening and alters growth and development. Plant Physiol 138(3):1372–1382

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Xiao Y, Chen W, Tang K, Zhang L (2009) Functional expression of vitreoscilla hemoglobin (vhb) in Arabidopsis relieves submergence, nitrosative, photo-oxidative stress and enhances antioxidants metabolism. Plant Sci 176:66–77

    Article  CAS  Google Scholar 

  • Wolff EC, Park MH, Folk JE (1990) Cleavage of spermidine as the first step in deoxyhypusine synthesis. The role of nad. J Biol Chem 265(9):4793–4799

    PubMed  CAS  Google Scholar 

  • Yang X, Wen X, Gong H, Lu Q, Yang Z, Tang Y, Liang Z, Lu C (2007) Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem ii in tobacco plants. Planta 225(3):719–733

    Article  PubMed  CAS  Google Scholar 

  • Zanelli CF, Valentini SR (2005) Pkc1 acts through zds1 and gic1 to suppress growth and cell polarity defects of a yeast eif5a mutant. Genetics 171(4):1571–1581

    Article  PubMed  CAS  Google Scholar 

  • Zanelli CF, Maragno AL, Gregio AP, Komili S, Pandolfi JR, Mestriner CA, Lustri WR, Valentini SR (2006) Eif5a binds to translational machinery components and affects translation in yeast. Biochem Biophys Res Commun 348(4):1358–1366

    Article  PubMed  CAS  Google Scholar 

  • Zuk D, Jacobson A (1998) A single amino acid substitution in yeast eif-5a results in mrna stabilization. EMBO J 17(10):2914–2925

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The study was supported by the Ministry of Agriculture of China (2008ZX08009-001), National High Technology Research and Development Program of China (2008AA10Z116), Youth Science and Technology Phosphor Foundation of Shanghai (08QH14003), and the Science and Technology Foundation of Shanghai (083391910400) for Feng Ming.

Author information

Authors and Affiliations

  1. State Key Laboratory of Genetic Engineering, Institute of Genetics, Fudan University, 220 Handan Road, Shanghai, 200433, People’s Republic of China

    Jianyao Xu, Bailong Zhang, Changhua Jiang & Feng Ming

  2. School of Life Science, Institute of Plant Biology, Fudan University, 220 Handan Road, Shanghai, 200433, People’s Republic of China

    Jianyao Xu, Bailong Zhang, Changhua Jiang & Feng Ming

Authors
  1. Jianyao Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bailong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Changhua Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Feng Ming
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Feng Ming.

Additional information

Jianyao Xu and Bailong Zhang contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xu, J., Zhang, B., Jiang, C. et al. RceIF5A, encoding an eukaryotic translation initiation factor 5A in Rosa chinensis, can enhance thermotolerance, oxidative and osmotic stress resistance of Arabidopsis thaliana . Plant Mol Biol 75, 167–178 (2011). https://doi.org/10.1007/s11103-010-9716-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-010-9716-2

Keywords

Search

Navigation