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Genome-Wide Analysis and Expression Profiling of the ERF Transcription Factor Family in Potato (Solanum tuberosum L.)

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Abstract

The ERF transcription factors belong to the AP2/ERF superfamily, one of the largest transcription factor families in plants. They play important roles in plant development processes, as well as in the response to biotic, abiotic, and hormone signaling. In the present study, 155 putative ERF transcription factor genes were identified from the potato (Solanum tuberosum) genome database, and compared with those from Arabidopsis thaliana. The StERF proteins are divided into ten phylogenetic groups. Expression analyses of five StERFs were carried out by semi-quantitative RT-PCR and compared with published RNA-seq data. These latter analyses were used to distinguish tissue-specific, biotic, and abiotic stress genes as well as hormone-responsive StERF genes. The results are of interest to better understand the role of the AP2/ERF genes in response to diverse types of stress in potatoes. A comprehensive analysis of the physiological functions and biological roles of the ERF family genes in S. tuberosum is required to understand crop stress tolerance mechanisms.

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References

  1. 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  Google Scholar 

  2. Xu, Z. S., Chen, M., Li, L. C., & Ma, Y. Z. (2011). Functions and application of the AP2/ERF transcription factor family in crop improvement. Journal of Integrative Plant Biology, 53, 570–585.

    Article  CAS  Google Scholar 

  3. Wessler, S. R. (2005). Homing into the origin of the AP2 DNA binding domain. Trends in Plant Science, 10, 54–56.

    Article  CAS  Google Scholar 

  4. Zhou, M. L., Ma, J. T., Pang, J. F., Zhang, Z. L., Tang, Y. X., & Wu, Y. M. (2010). Regulation of plant stress response by dehydration responsive element binding (DREB) transcription factors. African Journal of Biotechnology, 9, 9255–9269.

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  6. Licausi, F., Giorgi, F. M., Zenoni, S., Osti, F., Pezzotti, M., & Perata, P. (2010). Genomic and transcriptomic analysis of the AP2/ERF superfamily in Vitis vinifera. BMC Genomics, 11, 719.

    Article  CAS  Google Scholar 

  7. Hu, L. F., & Liu, S. Q. (2011). Genome-wide identification and phylogenetic analysis of the ERF gene family in cucumbers. Genetics and Molecular Biology, 34, 624–633.

    Article  CAS  Google Scholar 

  8. Sakuma, Y., Liu, Q., Dubouzet, J. G., Abe, H., Shinozaki, K., & Yamaguchi-Shinozaki, K. (2002). DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochemical and Biophysical Research Communications, 290, 998–1009.

    Article  CAS  Google Scholar 

  9. Lin, R. C., Park, H. J., & Wang, H. Y. (2008). Role of Arabidopsis RAP2.4 in regulating light- and ethylene-mediated developmental processes and drought stress tolerance. Molecular Plant, 1, 42–57.

    Article  CAS  Google Scholar 

  10. Liu, N., Zhong, N. Q., Wang, G. L., Li, L. J., Liu, X. L., He, Y. K., & Xia, G. X. (2007). Cloning and functional characterization of PpDBF1 gene encoding a DRE-binding transcription factor from Physcomitrella patens. Planta, 226, 827–838.

    Article  CAS  Google Scholar 

  11. Qin, F., Kakimoto, M., Sakuma, Y., Maruyama, K., Osakabe, Y., Tran, L. S. P., et al. (2007). Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J, 50, 54–69.

    Article  CAS  Google Scholar 

  12. Wang, X. M., Chen, X. F., Liu, Y., Gao, H. W., Wang, Z., & Sun, G. Z. (2011). CkDREB gene in Caragana korshinskii is involved in the regulation of stress response to multiple abiotic stresses as an AP2/EREBP transcription factor. Molecular Biology Reports, 38, 2801–2811.

    Article  CAS  Google Scholar 

  13. Yamaguchi-Shinozaki, K., & Shinozaki, K. (1993). Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Molecular & General Genetics: MGG, 236, 331–340.

    Article  CAS  Google Scholar 

  14. Zhang, G. Y., Chen, M., Chen, X. P., Xu, Z. S., Guan, S., Li, L. C., et al. (2008). Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). Journal of Experimental Botany, 59, 4095–4107.

    Article  CAS  Google Scholar 

  15. Kim, Y. H., Jeong, J. C., Park, S., Lee, H. S., & Kwak, S. S. (2012). Molecular characterization of two ethylene response factor genes in sweetpotato that respond to stress and activate the expression of defense genes in tobacco leaves. Journal of Plant Physiology, 169, 1112–1120.

    Article  CAS  Google Scholar 

  16. Rae, L., Lao, N. T., & Kavanagh, T. A. (2011). Regulation of multiple aquaporin genes in Arabidopsis by a pair of recently duplicated DREB transcription factors. Planta, 234, 429–444.

    Article  CAS  Google Scholar 

  17. Sharoni, A. M., Nuruzzaman, M., Satoh, K., Shimizu, T., Kondoh, H., Sasaya, T., et al. (2011). Gene structures, classification and expression models of the AP2/EREBP transcription factor family in rice. Plant and Cell Physiology, 52, 344–360.

    Article  CAS  Google Scholar 

  18. Zarei, A., Korbes, A. P., Younessi, P., Montiel, G., Champion, A., & Memelink, J. (2011). Two GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-mediated activation of the PDF1.2 promoter in Arabidopsis. Plant Molecular Biology, 75, 321–331.

    Article  CAS  Google Scholar 

  19. Park, J. M., Park, C. J., Lee, S. B., Ham, B. K., Shin, R., & Paek, K. H. (2001). Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell, 13, 1035–1046.

    Article  CAS  Google Scholar 

  20. Wei, G., Pan, Y., Lei, J., & Zhu, Y. X. (2005). Molecular cloning, phylogenetic analysis, expressional profiling and in vitro studies of TINY2 from Arabidopsis thaliana. Journal of Biochemistry and Molecular Biology, 38, 440–446.

    Article  CAS  Google Scholar 

  21. Liu, Y., Zhao, T. J., Liu, J. M., Liu, W. Q., Liu, Q., Yan, Y. B., & Zhou, H. M. (2006). The conserved Ala37 in the ERF/AP2 domain is essential for, binding with the DRE element and the GCC box. FEBS Letters, 580, 1303–1308.

    Article  CAS  Google Scholar 

  22. Zhuang, J., Cai, B., Peng, R. H., Zhu, B., Jin, X. F., Xue, Y., et al. (2008). Genome-wide analysis of the AP2/ERF gene family in Populus trichocarpa. Biochemical and Biophysical Research Communications, 371, 468–474.

    Article  CAS  Google Scholar 

  23. Song, X. M., Li, Y., & Hou, X. L. (2013). Genome-wide analysis of the AP2/ERF transcription factor superfamily in Chinese cabbage (Brassica rapa ssp. pekinensis). BMC Genomics, 14, 573.

    Article  CAS  Google Scholar 

  24. Gil-Humanes, J., Piston, F., Martin, A., & Barro, F. (2009). Comparative genomic analysis and expression of the APETALA2-like genes from barley, wheat, and barley-wheat amphiploids. BMC Plant Biology, 9, 66.

    Article  Google Scholar 

  25. Girardi, C. L., Rombaldi, C. V., Dal Cero, J., Nobile, P. M., Laurens, F., Bouzayen, M., & Quecini, V. (2013). Genome-wide analysis of the AP2/ERF superfamily in apple and transcriptional evidence of ERF involvement in scab pathogenesis. Scientia Horticulturae-Amsterdam, 151, 112–121.

    Article  CAS  Google Scholar 

  26. Pirrello, J., Prasad, B. C. N., Zhang, W. S., Chen, K. S., Mila, I., Zouine, M., et al. (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 Biology, 12, 190.

    Article  CAS  Google Scholar 

  27. Massa, A. N., Childs, K. L., Lin, H., Bryan, G. J., Giuliano, G., & Buell, C. R. (2011). The transcriptome of the reference potato genome Solanum tuberosum Group Phureja clone DM1-3 516R44. PLoS One, 6, e26801.

    Article  CAS  Google Scholar 

  28. Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum, 15, 473–497.

    Article  CAS  Google Scholar 

  29. Morel, G., & Wetmore, R. H. (1951). Fern callus tissue culture. American Journal of Botany, 38, 141–143.

    Article  CAS  Google Scholar 

  30. Hassairi, A., Masmoudi, K., Albouy, J., Robaglia, C., Jullien, M., & Ellouz, R. (1998). Transformation of two potato cultivars ‘Spunta’ and ‘Claustar’ (Solanum tuberosum) with lettuce mosaic virus coat protein gene and heterologous immunity to potato virus Y. Plant Science, 136, 31–42.

    Article  CAS  Google Scholar 

  31. Verwoerd, T. C., Dekker, B. M., & Hoekema, A. (1989). A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Research, 17, 2362.

    Article  CAS  Google Scholar 

  32. Degenhardt, J., Al-Masri, A. N., Kurkcuoglu, S., Szankowski, I., & Gau, A. E. (2005). Characterization by suppression subtractive hybridization of transcripts that are differentially expressed in leaves of apple scab-resistant and susceptible cultivars of Malus domestica. Molecular Genetics and Genomics, 273, 326–335.

    Article  CAS  Google Scholar 

  33. 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. Molecular Biology and Evolution, 28, 2731–2739.

    Article  CAS  Google Scholar 

  34. Voorrips, R. E. (2002). MapChart: Software for the graphical presentation of linkage maps and QTLs. The Journal of Heredity, 93, 77–78.

    Article  CAS  Google Scholar 

  35. Saeed, A. I., Hagabati, N. K., Braisted, J. C., Liang, W., Sharov, V., Howe, E. A., et al. (2006). TM4 microarray software suite. Methods in Enzymology, 411, 134–193.

    Article  CAS  Google Scholar 

  36. Bailey, T. L., & Elkan, C. (1994). Fitting a mixture model by expectation maximization to discover motifs in biopolymers (Vol. 2). In Proceedings/… International Conference on Intelligent Systems for Molecular Biology, ISMB. International Conference on Intelligent Systems for Molecular Biology (pp. 28–36).

  37. Guo, A. Y., Zhu, Q. H., Chen, X., & Luo, J. C. (2007). GSDS: A gene structure display server. Yi chuan = Hereditas/Zhongguo yi chuan xue hui bian ji, 29, 1023–1026.

    Article  CAS  Google Scholar 

  38. Bouaziz, D., Pirrello, J., BenAmor, H., Hammami, A., Charfeddine, M., Dhieb, A., et al. (2012). Ectopic expression of dehydration responsive element binding proteins (StDREB2) confers higher tolerance to salt stress in potato. Plant Physiology and Biochemistry, 60, 98–108.

    Article  CAS  Google Scholar 

  39. Bouaziz, D., Pirrello, J., Charfeddine, M., Hammami, A., Jbir, R., Dhieb, A., et al. (2013). Overexpression of StDREB1 transcription factor increases tolerance to salt in transgenic potato plants. Molecular Biotechnology, 54, 803–817.

    Article  CAS  Google Scholar 

  40. Hanada, K., Zou, C., Lehti-Shiu, M. D., Shinozaki, K., & Shiu, S. H. (2008). Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiology, 148, 993–1003.

    Article  CAS  Google Scholar 

  41. Liu, L. S., White, M. J., & MacRae, T. H. (1999). Transcription factors and their genes in higher plants—Functional domains, evolution and regulation. European Journal of Biochemistry, 262, 247–257.

    Article  CAS  Google Scholar 

  42. Sharma, M. K., Kumar, R., Solanke, A. U., Sharma, R., Tyagi, A. K., & Sharma, A. K. (2010). Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. Molecular Genetics and Genomics, 284, 455–475.

    Article  CAS  Google Scholar 

  43. Bouaziz, D. (2013). Isolement, caractérisation, étude fonctionelle de facteurs de transcription de la famille des ERF et surexpression de deux membres chez la pomme de terre. Thesis at University of Sfax.

  44. Pandey, G. K., Grant, J. J., Cheong, Y. H., Kim, B. G., Li, L. G., & Luan, S. (2005). ABR1, an APETALA2-domain transcription factor that functions as a repressor of ABA response in Arabidopsis. Plant Physiology, 139, 1185–1193.

    Article  CAS  Google Scholar 

  45. Gutha, L. R., & Reddy, A. R. (2008). Rice DREB1B promoter shows distinct stress-specific responses, and the overexpression of cDNA in tobacco confers improved abiotic and biotic stress tolerance. Plant Molecular Biology, 68, 533–555.

    Article  CAS  Google Scholar 

  46. Zhu, Q., Zhang, J. T., Gao, X. S., Tong, J. H., Xiao, L. T., Li, W. B., & Zhang, H. X. (2010). The Arabidopsis AP2/ERF transcription factor RAP2.6 participates in ABA, salt and osmotic stress responses. Gene, 457, 1–12.

    Article  CAS  Google Scholar 

  47. Fujimoto, S. Y., Ohta, M., Usui, A., Shinshi, H., & Ohme-Takagi, M. (2000). Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell, 12, 393–404.

    Article  CAS  Google Scholar 

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Acknowledgments

This study was financed by the Tunisian Ministry of High Education and Scientific Research. The authors are grateful to Anne-Lise Haenni from Institute Jacques Monod (CNRS-France) for her kind help with the English language.

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Authors and Affiliations

  1. Unité d’Enzymes et Bioconversion, Ecole Nationale d’Ingénieurs de Sfax, Route Soukra Km 4, BP 1173, 3038, Sfax, Tunisia

    Mariam Charfeddine, Safa Charfeddine, Asma Hammami & Radhia Gargouri Bouzid

  2. Laboratoire de protection et amélioration des plantes, Centre de Biotechnologie de Sfax (CBS), BP 1177, 3018, Sfax, Tunisia

    Mohamed Najib Saïdi

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  1. Mariam Charfeddine
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  2. Mohamed Najib Saïdi
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  3. Safa Charfeddine
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  4. Asma Hammami
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  5. Radhia Gargouri Bouzid
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Correspondence to Mariam Charfeddine.

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Charfeddine, M., Saïdi, M.N., Charfeddine, S. et al. Genome-Wide Analysis and Expression Profiling of the ERF Transcription Factor Family in Potato (Solanum tuberosum L.). Mol Biotechnol 57, 348–358 (2015). https://doi.org/10.1007/s12033-014-9828-z

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