Journal of Plant Biology

, Volume 61, Issue 2, pp 61–71 | Cite as

PsnERF75 Transcription Factor from Populus simonii × P. nigra Confers Salt Tolerance in Transgenic Arabidopsis

  • Shengji Wang
  • Boru Zhou
  • Wenjing Yao
  • Tingbo Jiang
Original Article


ERF transcription factor involves in many aspects of plant development and response to both biotic and abiotic environmental stimuli. In this study, we provided evidence that PsnERF75 can improve the salt tolerance ability of transgenic Arabidopsis. RT-qPCR analysis described the spatio-temporal expression patterns of PsnERF75 in different poplar tissues. Under salt stress condition, root and leaf tissues were more sensitive than stem tissue. In addition, seed germination rates of PsnERF75 transgenic Arabidopsis were significantly enhanced. Growth status of PsnERF75 transgenic Arabidopsis seedlings was much better than that of the controls. Physiological and histochemical assays indicated PsnERF75 transgenic Arabidopsis have a greater capacity to eliminate reactive oxygen species and lighten the damages to plants than the controls. Using RNA-seq analysis, 100 DEGs that were significant differentially expressed between PsnERF75 transgenic Arabidopsis and the controls under salt stress conditions were identified. Seventeen upregulated and 10 down-regulated DEGs participate in plant salt stress response process. In addition, subcellular localization showed that PsnERF75 is a nuclear-localized protein. All of the results will provide novel insights into the functions of ERF75 in plants under abiotic stress condition.


Abiotc stress ERF Populus simonii × P. nigra Plant physiology 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

12374_2017_450_MOESM1_ESM.xlsx (29 kb)
Supplementary material, approximately 29 KB.


  1. Abogadallah GM, Nada RM, Malinowski R, Quick P (2011) Overexpression of HARDY, an AP2/ERF gene from Arabidopsis, improves drought and salt tolerance by reducing transpiration and sodium uptake in transgenic Trifolium alexandrinum L. Planta 233: 1265−1276CrossRefGoogle Scholar
  2. Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24: 1337−1344CrossRefGoogle Scholar
  3. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373−399CrossRefGoogle Scholar
  4. Bari R, Jones JDG, Leyser O, Sun TP, Kakimoto T (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69: 473−488CrossRefGoogle Scholar
  5. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65: 1229−1240CrossRefGoogle Scholar
  6. Benamor M, Flores B, Latché A, Bouzayen M, Pech J C, Romojaro F (1999) Inhibition of ethylene biosynthesis by antisense acc oxidase rna prevents chilling injury in charentais cantaloupe melons. Plant Cell Environ 22: 1579−1586Google Scholar
  7. Cela J, Chang C, Munne-Bosch S (2011) Accumulation of gammarather than alpha-tocopherol alters ethylene signaling gene expression in the vte4 mutant of Arabidopsis thaliana. Plant Cell Physiol 52: 1389−1400CrossRefPubMedCentralGoogle Scholar
  8. Chen J, Song L, Dai J, Gan N, Liu Z (2004) Effects of microcystins on the growth and the activity of superoxide dismutase and peroxidase of rape (Brassica napus L.) and rice (Oryza sativa L.). Toxicon 43: 393−400CrossRefPubMedGoogle Scholar
  9. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743CrossRefPubMedGoogle Scholar
  10. Cole Trapnell AR, Loyal Goff, Geo Pertea, Daehwan Kim, David R Kelley, Harold Pimentel, Steven L Salzberg, John L Rinn, Lior Pachter (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562−578PubMedCentralGoogle Scholar
  11. Gao C, Wang Y, Jiang B, Liu G, Yu L, Wei Z, Yang C (2011a) A novel vacuolar membrane H+-ATPase c subunit gene (ThVHAc1) from Tamarix hispida confers tolerance to several abiotic stresses in Saccharomyces cerevisiae. Mol Biol Rep 38: 957−963Google Scholar
  12. Gao S, Yuan L, Zhai H, Liu CL, He SZ, Liu QC (2011b) Transgenic sweetpotato plants expressing an LOS5 gene are tolerant to salt stress. Plant Cell Tissue Organ Cult 107: 205−213CrossRefGoogle Scholar
  13. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28: 1091−1101CrossRefGoogle Scholar
  14. Guo ZJ, Chen XJ, Wu XL, Ling JQ, Xu P (2004) Overexpression of the AP2/EREBP transcription factor OPBP1 enhances disease resistance and salt tolerance in tobacco. Plant Mol Biol 55: 607−618CrossRefGoogle Scholar
  15. Hao D, Ohme-Takagi M, Sarai A (1998) Unique Mode of GCC Box Recognition by the DNA-binding Domain of Ethylene-responsive Element-binding Factor (ERF Domain) in Plant. J Biol Chem 273: 26857−26861CrossRefGoogle Scholar
  16. Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61: 1041−1052CrossRefGoogle Scholar
  17. Huang Y, Li H, Gupta R, Morris PC, Luan S, Kieber JJ (2000) ATMPK4, an Arabidopsis homolog of mitogen-activated protein kinase, is activated in vitro by AtMEK1 through threonine phosphorylation. Plant Physiol 122: 1301−1310PubMedCentralGoogle Scholar
  18. Jofuku KD, den Boer BG, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6: 1211−1225CrossRefPubMedCentralGoogle Scholar
  19. Kumar D, Yusuf MA, Singh P, Sardar M, Sarin NB (2013) Modulation of antioxidant machinery in alpha-tocopherol-enriched transgenic Brassica juncea plants tolerant to abiotic stress conditions. Protoplasma 250: 1079−1089Google Scholar
  20. Lichtenthaler HK (1990) Applications of Chlorophyll Fluorescene: in Photosynthesis Research, Stress Physiology, Hydrobiology and Remote Sensing. J Appl Ecol 27: 764Google Scholar
  21. Liu Z, Han B, Jin C, Han J, Zhou L (2013) A Novel Thylakoid Ascorbate Peroxidase from Jatrophacurcas Enhances Salt Tolerance in Transgenic Tobacco. Int J Mol Sci 15: 171−185CrossRefPubMedCentralGoogle Scholar
  22. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T Method. Methods 25: 402−408CrossRefGoogle Scholar
  23. Lurie S, Fallik E, Handros A, Shapira R (1997) The possible involvement of peroxidase in resistance to Botrytis cinereain heat treated tomato fruit. Physiol Mol Plant Pathol 50: 141−149CrossRefGoogle Scholar
  24. Mao G, Seebeck T, Schrenker D, Yu O (2013) CYP709B3, a cytochrome P450 monooxygenase gene involved in salt tolerance in Arabidopsis thaliana. BMC Plant Biol 13: 1−13CrossRefGoogle Scholar
  25. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33: 453−467CrossRefGoogle Scholar
  26. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490−498CrossRefGoogle Scholar
  27. Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta 1819: 86CrossRefPubMedGoogle Scholar
  28. Neill SJ (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53: 1237−1247CrossRefGoogle Scholar
  29. Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7: 173−182CrossRefPubMedCentralGoogle Scholar
  30. Onate-Sanchez L, Anderson JP, Young J, Singh KB (2007) AtERF14, a member of the ERF family of transcription factors, plays a nonredundant role in plant defense. Plant Physiol 143: 400−409PubMedCentralGoogle Scholar
  31. Parida AK, Das AB, Mohanty P (2004) Defense potentials to NaCl in a mangrove, Bruguiera parviflora: differential changes of isoforms of some antioxidative enzymes. J Plant Physiol 161: 531−542Google Scholar
  32. Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14: 290−295CrossRefGoogle Scholar
  33. Qiang X, Fu HH, Gupta R, Luan S, Xu Q, Fu HH (1998) Molecular characterization of a tyrosine-specific protein phosphatase encoded by a stress-responsive gene in Arabidopsis. Plant Cell 10: 849−857Google Scholar
  34. Regier N, Frey B (2010) Experimental comparison of relative RTqPCR quantification approaches for gene expression studies in poplar. BMC Molecular Biol 11: 1−8CrossRefGoogle Scholar
  35. Robinson MD, Mccarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139−140CrossRefGoogle Scholar
  36. Sairam RK, Rao KV, Srivastava GC (2002) Differential Response of Wheat Genotypes to Long Term Salinity Stress in Relation to Oxidative Stress, Antioxidant Activity and Osmolyte Concentration. Plant Sci 163: 1037−1046CrossRefGoogle Scholar
  37. Sakuma Y, Maruyama K, Osakabe Y, Feng Q, Seki M, Shinozaki K, Yamaguchishinozaki K (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in droughtresponsive gene expression. Plant Cell 18: 1292−1309CrossRefPubMedCentralGoogle Scholar
  38. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28: 2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  39. Thomashow MF (1999) PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms. Annu Rev Plant Biol 50: 571−599Google Scholar
  40. Wang F, Tong W, Zhu H, Kong W, Peng R, Liu Q, Yao Q (2016a) A novel Cys2/His2 zinc finger protein gene from sweetpotato, IbZFP1, is involved in salt and drought tolerance in transgenic Arabidopsis. Planta 243: 783−797Google Scholar
  41. Wang F, Zhu H, Chen D, Li Z, Peng R, Yao Q (2016b) A grape bHLH transcription factor gene, VvbHLH1, increases the accumulation of flavonoids and enhances salt and drought tolerance in transgenic Arabidopsis thaliana. Plant Cell, Tissue and Organ Culture (PCTOC)Google Scholar
  42. Wang F, Zhu H, Kong W, Peng R, Liu Q, Yao Q (2016c) The Antirrhinum AmDEL gene enhances flavonoids accumulation and salt and drought tolerance in transgenic Arabidopsis. PlantaGoogle Scholar
  43. Wang S, Yao W, Wei H, Jiang T, Zhou B (2014) Expression patterns of ERF genes underlying abiotic stresses in di-haploid Populus simonii x P. nigra. Sci World J 2014: 745091Google Scholar
  44. Wang X, Liu S, Tian H, Wang S, Chen JG (2015) The Small Ethylene Response Factor ERF96 is Involved in the Regulation of the Abscisic Acid Response in Arabidopsis. Front Plant Sci 6: 1064 doi:10.3389/fpls.2015.01064PubMedPubMedCentralGoogle Scholar
  45. Whatley FR, Arnon DI (1963) Separation of the light and dark reactions in electron transfer during photosynthesis. Proc Natl Acad Sci USA 49: 266−270CrossRefPubMedCentralGoogle Scholar
  46. Xie Z, Duan L, Tian X, Wang B, Eneji AE, Li Z (2008) Coronatine alleviates salinity stress in cotton by improving the antioxidative defense system and radical-scavenging activity. J Plant Physiol 165: 375−384CrossRefGoogle Scholar
  47. Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6: 251−264CrossRefPubMedCentralGoogle Scholar
  48. Yao W, Wang S, Zhou B, Jiang T, Li C (2016) Transgenic poplar overexpressing the endogenous transcription factor ERF76 gene improves salinity tolerance. Tree Physiol 36: 896−908CrossRefPubMedGoogle Scholar
  49. Yong-Qiang G, Mary CW, Suma C, Ying-Tsu L, Caimei Y, Xiaohua H, Yu H, Gregory BM (2002) Tomato transcription factors pti4, pti5, and pti6 activate defense responses when expressed in Arabidopsis. Plant Cell 14: 817−831Google Scholar
  50. Zhai H, Wang F, Si Z, Huo J, Xing L, An Y, He S, Liu Q (2016) A myoinositol-1-phosphate synthase gene, IbMIPS1, enhances salt and drought tolerance and stem nematode resistance in transgenic sweet potato. Plant Biotechnol J 14: 592−602CrossRefPubMedGoogle Scholar
  51. Zhang G, Chen M, Chen X, Xu Z, Guan S, Li LC, Li A, Guo J, Mao L, Ma Y (2008) Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J Exp Bot 59: 4095−4107PubMedCentralGoogle Scholar
  52. Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 60: 3781−3796PubMedCentralGoogle Scholar

Copyright information

© Korean Society of Plant Biologists and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Shengji Wang
    • 1
    • 2
  • Boru Zhou
    • 2
  • Wenjing Yao
    • 2
  • Tingbo Jiang
    • 2
  1. 1.College of ForestryShanxi Agricultural UniversityTaigu, ShanxiChina
  2. 2.State Key Laboratory of Tree Genetics and BreedingNortheast Forestry UniversityHarbinChina

Personalised recommendations