Journal of Forestry Research

, Volume 28, Issue 3, pp 453–463 | Cite as

Two novel eukaryotic translation initiation factor 5A genes from Populus simonii × P. nigra confer tolerance to abiotic stresses in Saccharomyces cerevisiae

Original Paper
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Abstract

The role of plant eIF5A proteins in multiple biological processes, such as protein synthesis regulation, translation elongation, mRNA turnover, programmed cell death and stress tolerance is well known. Toward using these powerful proteins to increase stress tolerance in agricultural plants, in the present study, we cloned and characterized PsneIF5A2 and PsneIF5A4 from young poplar (P. simonii × P. nigra) leaves. The deduced amino acid sequences of PsneIF5A2 and PsneIF5A4 were 98 % similar to each other, and they are orthologs of eIF5A1 in Arabidopsis. In a subcellular localization analysis, PsneIF5A2 and PsneIF5A4 proteins were localized in the nucleus and cytoplasm. qRT-PCR analysis showed that PsneIF5A2 and PsneIF5A4 were transcribed in poplar flowers, stem, leaves, and roots. In addition, they were also induced by abiotic stresses. Transgenic yeast expressing PsneIF5A2 and PsneIF5A4 had increased salt, heavy metal, osmotic, oxidative tolerance. Our results suggest that PsneIF5A2 and PsneIF5A4 are excellent candidates for genetic engineering to improve salt and heavy metal tolerance in agricultural plants.

Keywords

Abiotic tolerance eIF5A Populus simonii × P. nigra Subcellular localization Yeast 

Abbreviations

ABA

Abscisic acid

eIF5A

Eukaryotic translation initiation factor 5A

EV

Empty vector

Gal

Galactose

Glu

Glucose

NLS

Nuclear localization signal

ORF

Open reading frame

qRT-PCR

Quantitative real time polymerase chain reaction

RT-PCR

Reverse transcriptase polymerase chain reaction

SC

Synthetic complete medium

Ura

Uracil

References

  1. An Y, Wang YC, Lou LL, Zheng TC, Qu GZ (2011) A novel zinc-finger-like gene from Tamarix hispida is involved in salt and osmotic tolerance. J Plant Res 124:689–697CrossRefPubMedGoogle Scholar
  2. Benne R, Brown-Luedi ML, Hershey JW (1978) Purification and characterization of protein synthesis initiation factors eIF-1 eIF-4C eIF-4D and eIF-5 from rabbit reticulocytes. J Biol Chem 253:3070–3077PubMedGoogle Scholar
  3. Chamot D, Kuhlemeier C (1992) Differential expression of genes encoding the hypusine-containing translation initiation factor eIF-5A in tobacco. Nucleic Acids Res 20:665–669CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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 121:50–57CrossRefPubMedGoogle Scholar
  5. 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 144:1531–1545CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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 380:785–790CrossRefPubMedGoogle Scholar
  7. 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 101:9595–9600CrossRefPubMedPubMedCentralGoogle Scholar
  8. Hopkins MT, Lampi Y, Wang TW, Liu Z, Thompson JE (2008) Eukaryotic translation initiation factor 5A is involved in pathogen-induced cell death and development of disease symptoms in Arabidopsis. Plant Physiol 148:479–489CrossRefPubMedPubMedCentralGoogle Scholar
  9. Jenkins ZA, Hååg PG, Johansson HE (2001) Human eIF5A2 on chromosome 3q25-q27 is a phylogenetically conserved vertebrate variant of eukaryotic translation initiation factor 5A with tissue-specific expression. Genomics 71:101–109CrossRefPubMedGoogle Scholar
  10. Kang HA, Hershey JWB (1994) Effect of initiation factor eIF-5A depletion on protein synthesis and proliferation of Saccharomyces cerevisiae. J Biol Chem 269:3934–3940PubMedGoogle Scholar
  11. Kang HA, Schwelberger HG, Hershey JWB (1993) Translation initiation factor eIF-5A the hypusine-containing protein is phosphorylated on serine in Saccharomyces cerevisiae. J Biol Chem 268:14750–14756PubMedGoogle Scholar
  12. Kemper WM, Berry KW, Merrick WC (1976) Purification and properties of rabbit reticulocyte protein synthesis initiation factors M2Balpha and M2Bbeta. J Biol Chem 251:5551–5557PubMedGoogle Scholar
  13. Kim KK, Hung LW, Yokota H, Kim R, Kim SH (1998) Crystal structures of eukaryotic translation initiation factor 5A from Methanococcus jannaschii at 1.8 A resolution. Proc Natl Acad Sci USA 95:10419–10424CrossRefPubMedPubMedCentralGoogle Scholar
  14. Klier H, Wohl T, Eckerskorn C, Magdolen V, Lottspeich F (1993) Determination and mutational analysis of the phosphorylation site in the hypusine-containing protein Hyp2p. FEBS Lett 334:360–364CrossRefPubMedGoogle Scholar
  15. Kyrpides NC, Woese CR (1998) Universally conserved translation initiation factors. Proc Natl Acad Sci USA 95:224–228CrossRefPubMedPubMedCentralGoogle Scholar
  16. Lee EH, Hyun DH, Park EH, Lim CJ (2010) A second protein disulfide isomerase plays a protective role against nitrosative and nutritional stresses in Schizosaccharomyces pombe. Mol Biol Rep 37:3663–3671CrossRefPubMedGoogle Scholar
  17. 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 59:939–950CrossRefPubMedGoogle Scholar
  18. 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 25:402–408CrossRefPubMedGoogle Scholar
  19. Ma F, Liu Z, Wang TW, Hopkins MT, Peterson CA, Thompson JE (2010) Arabidopsis eIF5A3 influences growth and the response to osmotic and nutrient stress. Plant Cell Environ 33:1682–1696CrossRefPubMedGoogle Scholar
  20. Niwa Y (2003) A synthetic green fluorescent protein gene for plant biotechnology. Plant Biotechnol 20:1–11CrossRefGoogle Scholar
  21. Okay S, Derelli E, Unver T (2014) Transcriptome-wide identification of bread wheat WRKY transcription factors in response to drought stress. Mol Genet Genomics 289:765–781CrossRefPubMedGoogle Scholar
  22. 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 17:927–929CrossRefPubMedGoogle Scholar
  23. Pollard VW, Malim MH (1998) The HIV-1 Rev protein. Annu Rev Microbiol 52:491–532CrossRefPubMedGoogle Scholar
  24. Requejo R, Tena M (2006) Maize response to acute arsenic toxicity as revealed by proteome analysis of plant shoots. Proteomics 6:S156–S162CrossRefPubMedGoogle Scholar
  25. Rosorius O, Reichart B, Krätzer 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 112:2369–2380PubMedGoogle Scholar
  26. Saini P, Eyler DE, Green R, Dever TE (2009) Hypusine-containing protein eIF5A promotes translation elongation. Nature 459:118–121CrossRefPubMedPubMedCentralGoogle Scholar
  27. Tamura K, Dudley J, Ne M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  28. Teng YB, Ma XX, He YX, Jiang YL, Du J, Xiang C, Chen Y, Zhou CZ (2009) Crystal structure of Arabidopsis translation initiation factor eIF-5A2. Proteins 77:736–740CrossRefPubMedGoogle Scholar
  29. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins D (1997) The ClustalX windows interface: exible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882CrossRefPubMedPubMedCentralGoogle Scholar
  30. 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 9:174–179CrossRefPubMedGoogle Scholar
  31. 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 276:17541–17549CrossRefPubMedGoogle Scholar
  32. Wang TW, Lu L, Zhang CG, Taylor C, Thompson JE (2003) Pleiotropic effects of suppressing deoxyhypusine synthase expression in Arabidopsis thaliana. Plant Mol Biol 52:1223–1235CrossRefPubMedGoogle Scholar
  33. Wang L, Xu C, Wang C, Wang Y (2012) Characterization of a eukaryotic translation initiation factor 5A homolog from Tamarix androssowii involved in plant abiotic stress tolerance. BMC Plant Biol 12:118CrossRefPubMedPubMedCentralGoogle Scholar
  34. Wang C, Deng P, Chen L, Wang X, Ma H, Hu W, Yao N, Feng Y, Chai R, Yang G, He G (2013) A wheat WRKY transcription factor TaWRKY10 confers tolerance to multiple abiotic stresses in transgenic tobacco. PLoS One 8:e65120CrossRefPubMedPubMedCentralGoogle Scholar
  35. Xu A, Chen KY (2001) Hypusine is required for a sequence-specific interaction of eukaryotic initiation factor 5A with postsystematic evolution of ligands by exponential enrichment RNA. J Biol Chem 276:2555–2561CrossRefPubMedGoogle Scholar
  36. Xu J, Zhang B, Jiang C, Ming F (2011) 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 75:167–178CrossRefPubMedGoogle Scholar
  37. Yang G, Wang Y, Xia D, Gao C, Wang C, Yang C (2014) Overexpression of a GST gene (ThGSTZ1) from Tamarix hispida improves drought and salinity tolerance by enhancing the ability to scavenge reactive oxygen species. Plant Cell Tissue Organ Cult 117:99–112CrossRefGoogle Scholar
  38. Yao M, Ohsawa A, Kikukawa S, Tanaka I, Kimura M (2003) Crystal structure of hyperthermophilic archaeal initiation factor 5A: a homologue of eukaryotic initiation factor 5A (eIF-5A). J Biochem 133:75–81CrossRefPubMedGoogle Scholar
  39. 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 348:1358–1366CrossRefPubMedGoogle Scholar
  40. Zhao Y, Sun J, Xu P, Zhang R, Li L (2014) Intron-mediated alternative splicing of wood-associated NAC transcription factor1B regulates cell wall thickening during fiber development in Populus species. Plant Physiol 164:765–776CrossRefPubMedPubMedCentralGoogle Scholar
  41. Zhou JP, Yang ZJ, Feng J, Chi SH, Liu C, Ren ZL (2006) Cloning and analysis of gene encoding wheat translation initiation factor eIF5A. Yi Chuan 28:571–577PubMedGoogle Scholar
  42. Zuk D, Jacobson A (1998) A single amino acid substitution in yeast eIF-5A results in mRNA stabilization. EMBO J 17:2914–2925CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Northeast Forestry University and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.State Key Laboratory of Tree Genetics and BreedingNortheast Forestry UniversityHarbinChina

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