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ERF transcription factors involved in salt response in tomato

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Abstract

ERF transcription factors are important regulatory components of ethylene signaling, known to be involved in plant development and stress responses by regulating the expression of ethylene responsive genes. However, relatively less is known about the function of ERF gene family in wild tomato response to salt stress. Previously, we have carried out a microarray analysis on the salt-responsive genes in salt tolerant wild tomato Solanum pimpinellifolium ‘PI365967’. Five ERF genes (SpERFs) with induced expression upon salt treatment were subsequently selected for further characterization. Sequence analysis revealed that the seven amino acid residues in ERF proteins which are critical for their binding to the GCC-box in the promoter of ethylene responsive genes were conserved in five SpERFs. Two of five SpERFs (SpERF.B7 and SpERF.C11) belong to B3 sub-group as predicted by phylogenetic analysis. Expression analysis indicated that two SpERFs of B3 sub-group were more strongly induced in salt-tolerant genotypes than in salt-sensitive genotypes, in the order of PI365967 > LA2711 > Moneymaker, suggesting a positive role of B3 sub-group SpERFs in salt stress in tomato. To further confirm the function of B3 SpERFs in salt response, SpERF.B7 (one of two B3 SpERFs) was over-expressed in Arabidopsis. Consistent with our expectation, transgenic lines exhibited enhanced salt tolerance. These results will provide useful information for improving salt tolerance in tomato breeding in the future.

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References

  • Abeles FB, Morgan PW, Saltveit MEJ (1992) Ethylene in plant biology. Academic Press, San Diego

    Google Scholar 

  • Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol 123:1047–1056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren JY, Li WW, Noble WS (2009) MEME Suite: tools for motif discovery and searching. Nucleic Acids Res 37:206–208

    Article  Google Scholar 

  • Cao Y, Wu Y, Zheng Z, Song F (2005) Overexpression of the rice EREBP-like gene OsBIERF3 enhances disease resistance and salt tolerance in transgenic tobacco. Physiol Mol Plant Pathol 67:202–211

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fischer U, Droge-Laser W (2004) Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to tobacco mosaic virus. Mol Plant-Microbe Interact J 17:1162–1171

    Article  CAS  Google Scholar 

  • Huang Z, Zhang Z, Zhang X, Zhang H, Huang D, Huang R (2004) Tomato TERF1 modulates ethylene response and enhances osmotic stress tolerance by activating expression of downstream genes. FEBS Lett 573:110–116

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Zhang BL, Sun S, Xing GM, Wang F, Li MY, Tian YS, Xiong AS (2016) AP2/ERF transcription factors involved in response to tomato yellow leaf curly virus in tomato. Plant Genome. https://doi.org/10.3835/plantgenome2015.09.0082

    Google Scholar 

  • Ji AJ, Luo HM, Xu ZC, Zhang X, Zhu YJ, Liao BS, Yao H, Song JY, Chen SL (2016) Genome-wide identification of the AP2/ERF gene family involved in active constituent biosynthesis in Salvia miltiorrhiza. Plant Genome. https://doi.org/10.3835/plantgenome2015.08.0077

    PubMed  Google Scholar 

  • Kagaya Y, Ohmiya K, Hattori T (1999) RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic Acids Res 27:470–478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Licausi F, Giorgi FM, Zenoni S, Osti F, Pezzotti M, Perata P (2010) Genomic and transcriptomic analysis of the AP2/ERF superfamily in Vitis vinifera. BMC Genom 11:719–734

    Article  CAS  Google Scholar 

  • Licausi F, Ohme-Takagi M, Perata P (2013) APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199:639–649

    Article  CAS  PubMed  Google Scholar 

  • Liu M, Gomes BL, Mila I, Purgatto E, Peres LE, Frasse P, Maza E, Zouine M, Roustan JP, Bouzayen M, Pirrello J (2016) Comprehensive profiling of ethylene response factor expression identifies ripening-associated ERF genes and their link to key regulators of fruit ripening in tomato. Plant Physiol 170:1732–1744

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • 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 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narasimhulu SB, Deng X, Sarria R, Gelvin SB (1996) Early transcription of agrobacterium T-DNA genes in tobacco and maize. Plant Cell 8:873–886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ouyang Z, Liu S, Huang L, Hong Y, Li X, Zhang Y, Zhang H, Li D, Song F (2016) Tomato SlERF.A1, SlERF.B4, SlERF.C3 and SlERF.A3, members of B3 group of ERF family, are required for resistance to Botrytis cinerea. Front Plant Sci 7:1964

    PubMed  PubMed Central  Google Scholar 

  • Pan YJ, Liu L, Lin YC, Zu YG, Li LP, Tang ZH (2016) Ethylene antagonizes salt-induced growth retardation and cell death process via transcriptional controlling of ethylene-, BAG- and senescence-associated genes in Arabidopsis. Front Plant Sci 7:696

    PubMed  PubMed Central  Google Scholar 

  • Pirrello J, Prasad BN, Zhang W, Chen K, Mila I, Zouine M, Latché A, Pech JC, Ohme-Takagi M, Regad F, Bouzayen M (2012) Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differential responses to ethylene. BMC Plant Biol 12:190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi S, Lin Q, Zhu H, Gao F, Zhang W, Hua X (2016) The RING finger E3 ligase SpRing is a positive regulator of salt stress signaling in salt-tolerant wild tomato species. Plant Cell Physiol 57:528–539

    Article  CAS  PubMed  Google Scholar 

  • Rong W, Qi L, Wang A, Ye X, Du L, Liang H, Xin Z, Zhang Z (2014) The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat. Plant Biotechnol J 12:468–479

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Xu X, Zhu H, Liu A, Liu L, Li J, Hua X (2010) Comparative transcriptomic profiling of a salt-tolerant wild tomato species and a salt-sensitive tomato cultivar. Plant Cell Physiol 51:997–1006

    Article  CAS  PubMed  Google Scholar 

  • Tang M, Sun J, Liu Y, Chen F, Shen S (2007) Isolation and functional characterization of the JcERF gene, a putative AP2/EREBP domain-containing transcription factor, in the woody oil plant Jatropha curcas. Plant Mol Biol 63:419–428

    Article  CAS  PubMed  Google Scholar 

  • Tao JJ, Chen HW, Ma B, Zhang WK, Chen SY, Zhang JS (2015) The role of ethylene in plants under salinity stress. Front Plant Sci 6:1059

    Article  PubMed  PubMed Central  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Upadhyay RK, Soni DK, Singh R, Dwivedi UN, Pathre UV, Nath P, Sane AP (2013) SlERF36, an EAR-motif-containing ERF gene from tomato, alters stomatal density and modulates photosynthesis and growth. J Exp Bot 64:3237–3247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  CAS  PubMed  Google Scholar 

  • Wu D, Ji J, Wang G, Guan C, Jin C (2014) LchERF, a novel ethylene-responsive transcription factor from Lycium chinense, confers salt tolerance in transgenic tobacco. Plant Cell Rep 33:2033–2045

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki K, Kigawa T, Seki M, Shinozaki K, Yokoyama S (2013) DNA-binding domains of plant-specific transcription factors: structure, function, and evolution. Trends Plant Sci 18:267–276

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Wang C, Lin Q, Gao F, Ma Y, Zhang M, Lin Y, Ma Q, Hua X (2015) Genome-wide analysis of phylogeny, expression profile and sub-cellular localization of SKP1-Like genes in wild tomato. Plant Sci 238:105–114

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Yang G, Mu D, Li H, Zang D, Xu H, Zou X, Wang Y (2016) An ethylene-responsive factor BpERF11 negatively modulates salt and osmotic tolerance in Betula platyphylla. Sci Rep 6:23085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Wei T, Yin KQ, Chen Z, Gu H, Qu LJ, Qin G (2012) Arabidopsis RAP2.2 plays an important role in plant resistance to Botrytis cinerea and ethylene responses. New Phytol 195:450–460

    Article  CAS  PubMed  Google Scholar 

  • Zhu T, Deng X, Zhou X, Zhu L, Zou L, Li P, Zhang D, Lin H (2016) Ethylene and hydrogen peroxide are involved in brassinosteroid-induced salt tolerance in tomato. Sci Rep 6:35392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhuang J, Jiang H-H, Wang F, Peng R-H, Yao Q-H, Xiong A-S (2013) A rice OsAP23, functioning as an AP2/ERF transcription factor, reduces salt tolerance in transgenic Arabidopsis. Plant Mol Biol Rep 31:1336–1345

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Professor Xuejun Hua from the Institute of Botany, Chinese Academy of Science for his valuable advices during the revision of the manuscript. This work was supported by Youth Talent Research Start-Up Funds of Guangdong Ocean University.

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Correspondence to Hanqiao Hu or Yueqin Zhang.

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Yang, R., Liu, J., Lin, Z. et al. ERF transcription factors involved in salt response in tomato. Plant Growth Regul 84, 573–582 (2018). https://doi.org/10.1007/s10725-017-0362-4

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