Skip to main content
SpringerLink
Log in

A New AP2/ERF Transcription Factor from the Oil Plant Jatropha curcas Confers Salt and Drought Tolerance to Transgenic Tobacco

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Jatropha curcas L. is a drought and salt-tolerant oil plant widely used for various purposes and has considerable potential as a diesel/kerosene substitute or extender. Understanding the molecular mechanisms underlie that the response to various biotic and abiotic stresses of this plant could be important to crop improvement efforts. Here, a new AP2/ERF-type transcription factor gene, named JcERF2, was isolated from the leaves of J. curcas. Sequence analysis showed that the JcERF2 gene contains a 759-bp open reading frame encoding a polypeptide of 252 amino acids. The predicted JcERF2 protein contained a conserved DNA-binding domain (the AP2/ERF domain) with 58 amino acids. The JcERF2 protein is highly homologous with other ERFs. JcERF2 was localized in the nucleus by analysis with a JcERF2-green fluorescent protein (GFP) fusion protein. Quantitative polymerase chain reaction (qPCR) analysis showed that JcERF2 was induced by drought, salt, abscisic acid, and ethylene. Overexpression of JcERF2 in transgenic tobacco plants enhanced the expression of biotic and abiotic stress-related genes, increased the accumulation of free proline and soluble carbohydrates, and conferred tolerance to drought and salt stresses compared to the wild type (WT). Taken together, the JcERF2 gene is a novel AP2/ERF transcription factor involved in plant response to environmental factors, which can be used as a potential candidate gene for genetic engineering of crops.

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

Similar content being viewed by others

References

  1. Abel, S., & Theologis, A. (1994). Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression. The Plant Journal, 5, 421–427.

    Article  CAS  Google Scholar 

  2. Archana, N. R., & Penna, S. (2013). Molecular evolution of plantP5CSgene involved in proline biosynthesis. Molecular Biology Reports, 40, 6429–6435.

    Article  Google Scholar 

  3. Ayarpadikannan, S., Chung, E., Kim, K., So, H., Schraufnaggle, K. R., & Lee, J. (2014). RsERF1 derived from wild radish (Raphanus sativus) confers salt stress tolerance in Arabidopsis. Acta Physiologiae Plantarum, 36, 993–1008.

    Article  CAS  Google Scholar 

  4. Boutilier, K., Offringa, R., Sharma, V. K., Kieft, H., Ouellet, T., Zhang, L. M., Hattori, J., Liu, C. M., van Lammeren, A. A., Miki, B. L. A., Custers, J. B. M., & van Lookeren Campagne, M. M. (2002). Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell, 14, 1737–1749.

    Article  CAS  Google Scholar 

  5. Cao, Y. F., Song, F. M., Goodman, R. M., & Zheng, Z. (2006). Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress. Journal of Plant Physiology, 163, 1167–1178.

    Article  CAS  Google Scholar 

  6. Cao, Y. F., Wu, Y. F., Zheng, Z., & Song, F. M. (2005). Overexpression of the rice EREBP-like gene OsBIERF3 enhances disease resistance and salt tolerance in transgenic tobacco. Physiological and Molecular Plant Pathology, 67, 202–211.

    Article  CAS  Google Scholar 

  7. Chen, M., Xu, Z., Xia, L., Li, L., Cheng, X., Dong, J., Wang, Q., & Ma, Y. (2009). Cold-induced modulation and functional analyses of the DRE-binding transcription factor gene, GmDREB3, in soybean (Glycine max L.). Journal of Experimental Botany, 60, 121–135.

    Article  CAS  Google Scholar 

  8. Chinnusamy, V., Schumaker, K., & Zhu, J. K. (2004). Molecular genetic perspectives on cross-talk and specificity in abiotic stress signaling in plants. Journal of Experimental Botany, 55, 225–236.

    Article  CAS  Google Scholar 

  9. Chuck, G., Meeley, R. B., & Hake, S. (1998). The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet l. Genes & Development, 12, 1145–1154.

    Article  CAS  Google Scholar 

  10. Clough, S. J., & Bent, A. F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal, 16, 735–743.

    Article  CAS  Google Scholar 

  11. Egawa, C., Kobayashi, F., Ishibashi, M., Nakamura, T., Nakamura, C., & Takumi, S. (2006). Differential regulation of transcript accumulation and alternative splicing of a DREB2 homolog under abiotic stress conditions in common wheat. Genes & Genetic Systems, 81, 77–91.

    Article  CAS  Google Scholar 

  12. Elliott, R. C., Betzner, A. S., Huttner, E., Oakes, M. P., Tucker, W. Q., Gerentes, D., Perez, P., & Smyth, D. R. (1996). AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell, 8, 155–168.

    Article  CAS  Google Scholar 

  13. Fischer, U., & Dröge-Laser, W. (2004). Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to tobacco mosaic virus. Molecular Plant-Microbe Interactions, 17, 1162–1171.

    Article  CAS  Google Scholar 

  14. Fukao, T., Yeung, E., & Bailey-Serres, J. (2011). The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell, 23, 412–427.

    Article  CAS  Google Scholar 

  15. Gibbs, D. J., Lee, S. C., Isa, N. M., Gramuglia, S., Fukao, T., Bassel, G. W., Correia, C. S., Corbineau, F., Theodoulou, F. L., Bailey-Serres, J., & Holdsworth, M. J. (2011). Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature, 479, 415–418.

    Article  CAS  Google Scholar 

  16. Gilmour, S. J., Sebolt, A. M., Salazar, M. P., Everard, J. D., & Thomashow, M. F. (2000). Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiology, 124, 1854–1865.

    Article  CAS  Google Scholar 

  17. Gu, Y. Q., Wildermuth, M. C., Chakravarthy, S., Loh, Y. T., Yang, C., He, X. H., Han, Y., & Martin, G. B. (2002). Tomato transcription factors pti4, pti5 and pti6 activate defense responses when expressed in Arabidopsis. Plant Cell, 14, 817–831.

    Article  CAS  Google Scholar 

  18. Gutterson, N., & Reuber, T. L. (2004). Regulation of disease resistance pathways by AP2/ERF transcription factors. Current Opinion in Plant Biology, 7, 465–471.

    Article  CAS  Google Scholar 

  19. Hao, D. Y., 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. The Journal of Biological Chemistry, 273, 26857–26861.

    Article  CAS  Google Scholar 

  20. Hinz, M., Wilson, I. W., Yang, J., Buerstenbinder, K., Llewellyn, D., Dennis, E. S., Sauter, M., & Dolferus, R. (2010). Arabidopsis RAP2.2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiology, 153, 757–772.

    Article  CAS  Google Scholar 

  21. Hirakawa, H., Tsuchimoto, S., Sakai, H., Nakayama, S., Fujishiro, T., Kishida, Y., Kohara, M., Watanabe, A., Yamada, M., Aizu, T., et al. (2012). Upgraded genomic information of Jatropha curcas L. Plant Biotechnology, 29, 123–130.

    Article  CAS  Google Scholar 

  22. Hongbo, S., Zongsuo, L., & Mingan, S. (2006). Osmotic regulation of 10 wheat (Triticum aestivum L.) genotypes at soil water deficits. Colloids and Surfaces. B, Biointerfaces, 47, 132–139.

    Article  Google Scholar 

  23. Hu, Y. X., Wang, Y. H., Liu, X. F., & Li, J. Y. (2004). Arabidopsis RAV1 is down-regulated by brassinosteroid and may act as a negative regulator during plant development. Cell Research, 14, 8–15.

    Article  CAS  Google Scholar 

  24. Jin, L., Huang, B., Li, H., & Liu, J. (2009). Expression profiles and transactivation analysis of a novel ethylene-responsive transcription factor gene GhERF5 from cotton. Progress in Natural Science, 19, 563–572.

    Article  CAS  Google Scholar 

  25. Jofuku, K. D., den Boer, B. G., Montagu, M. V., & Okamuro, J. K. (1994). Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell, 6, 1211–1225.

    Article  CAS  Google Scholar 

  26. Jung, J., Won, S. Y., Suh, S. C., Kim, H., Wing, R., Jeong, Y., Hwang, I., & Kim, M. (2007). The barley ERF-type transcription factor HvRAF confers enhanced pathogen resistance and salt tolerance in Arabidopsis. Planta, 225, 575–588.

    Article  CAS  Google Scholar 

  27. Kajikawa, M., Morikawa, K., Inoue, M., Widyastuti, U., Suharsono, S., Yokota, A., & Akashi, K. (2012). Establishment of bispyribac selection protocols for Agrobacterium tumefaciens- and Agrobacterium rhizogenes-mediated transformation of the oil seed plant Jatropha curcas L. Plant Biotechnology, 29, 145–153.

    Article  CAS  Google Scholar 

  28. Kim, W. K., Kim, J. H., Jeong, D. H., Chun, Y. H., Kim, S. H., Cho, K. J., & Chang, M. J. (2011). Radish (Raphanus sativus L. leaf) ethanol extract inhibits protein and mRNA expression of ErbB2 and ErbB3 in MDA-MB-231 human breast cancer cells. Nutrition Research Practice, 5, 288–293.

    Article  Google Scholar 

  29. Kumar, N., Reddy, M., & Sujatha, M. (2013). Genetic transformation of Jatropha curcas: Current status and future prospects. In B. Bahadur, M. Sujatha, & N. Carels (Eds.), Jatropha, Challenges for a New Energy Crop. Volume 2 (pp. 535–546). New York: Springer.

    Chapter  Google Scholar 

  30. Li, M. R., Li, H. Q., Jiang, H. W., Pan, X. P., & Wu, G. J. (2008). Establishment of an Agrobacteriuim-mediated cotyledon disc transformation method for Jatropha curcas. Plant Cell Tissue and Organ Culture, 92, 173–181.

    Article  CAS  Google Scholar 

  31. Licausi, F., van Dongen, J. T., Giuntoli, B., Novi, G., Santaniello, A., Geigenberger, P., & Perata, P. (2010). HRE1 and HRE2, two hypoxiainducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. The Plant Journal, 62, 302–315.

    Article  CAS  Google Scholar 

  32. Matsukura, S., Mizoi, J., Yoshida, T., Todaka, D., Ito, Y., Maruyama, K., Shinozaki, K., & Yamaguchi-Shinozaki, K. (2010). Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Molecular Genetics and Genomics, 283, 185–196.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  34. 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  Google Scholar 

  35. Oñate-Sánchez, L., & Singh, K. B. (2002). Identification of Arabidopsis ethylene-responsive element binding factors with distinct induction kinetics after pathogen infection. Plant Physiology, 128, 1313–1322.

    Article  Google Scholar 

  36. Openshaw, K. (2000). A review of Jatropha curcas: an oil plant of unfulfilled promise. Biomass and Bioenergy, 19, 1–15.

    Article  Google Scholar 

  37. Pan, J. L., Fu, Q. T., & Xu, Z. F. (2010). Agrobacterium tumefaciens-mediated transformation of biofuel plant Jatropha curcas using kanamycin selection. African Journal of Biotechnology, 9, 6477–6481.

    CAS  Google Scholar 

  38. Park, J. M., Park, C. J., Lee, S. B., Ham, B. K., Shin, R., & Paek, K. H. (2001). Overexpression of the tobaccoTsi1gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. The Plant Cell, 13, 1035–1046.

    Article  CAS  Google Scholar 

  39. Paz-Ares, J., Ghosal, D., Wienand, U., Peterson, P. A., & Saedler, H. (1987). The regulatory C1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. The EMBO Journal, 6, 3553–3558.

    CAS  Google Scholar 

  40. Roosens, N. H., al Bitar, F. A., Loenders, K., Angenon, G., & Jacobs, M. (2002). Overexpression of ornithine-d-aminotransferase increases pro biosynthesis and confers osmotolerance in transgenic plants. Molecular Breeding, 9, 73–80.

    Article  CAS  Google Scholar 

  41. 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 

  42. Sato, S., Hirakawa, H., Isobe, S., Fukai, E., Watanabe, A., Kato, M., Kawashima, K., Minami, C., Muraki, A., Nakazaki, N., et al. (2011). Sequence analysis of the genome of an oil-bearing tree, Jatropha curcas L. DNA Research, 18, 65–76.

    Article  CAS  Google Scholar 

  43. Schmook, B., & Serralta-Peraza, L. (1997). J. curcas: distribution and uses in the Yucatán Peninsula of Mexico. In G. M. Gübitz, M. Mittelbach, & M. Trabi (Eds.), Biofuels and industrial products from Jatropha curcas (pp. 53–57). Graz: DVB.

    Google Scholar 

  44. Shan, D. P., Huang, J. G., Yang, Y. T., Guo, Y. H., Wu, C. A., Yang, G. D., Gao, Z., & Zheng, C. C. (2007). Cotton GhDREB1 increases plant tolerance to low temperature and is negatively regulated by gibberellic acid. The New Phytologist, 176, 70–81.

    Article  CAS  Google Scholar 

  45. Singh, K. B., Foley, R. C., & Oñate-Sánchez, L. (2002). Transcription factors in plant defense and stress responses. Current Opinion in Plant Biology, 5(5), 430–436.

    Article  CAS  Google Scholar 

  46. Song, C., Agarwal, M., Ohta, M., Guo, Y., Halfter, U., Wang, P., & Zhu, J. (2005). Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell, 17, 2384–2396.

    Article  CAS  Google Scholar 

  47. Tang, M. J., Sun, J. W., Liu, Y., Chen, F., & Shen, S. H. (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 Molecular Biology, 63, 419–428.

    Article  CAS  Google Scholar 

  48. Tang, M. J., Liu, X. F., Deng, H. P., & Shen, S. H. (2011). Over-expression of JcDREB, a putative AP2/EREBP domain-containing transcription factor gene in woody biodiesel plant Jatropha curcas, enhances salt and freezing tolerance in transgenic Arabidopsis thaliana. Plant Science, 181, 623–631.

    Article  CAS  Google Scholar 

  49. Tang, W., Charles, T. M., & Newton, R. J. (2005). Overexpression of the pepper transcription factor CaPF1 in transgenic Virginia pine (Pinus virginiana Mill.) confers multiple stress tolerance and enhances organ growth. Plant Molecular Biology, 59, 603–617.

    Article  CAS  Google Scholar 

  50. Xiang, Y., Huang, Y., & Xiong, L. (2007). Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant Physiology, 144, 1416–1428.

    Article  CAS  Google Scholar 

  51. 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 

  52. Yang, H. J., Shen, H., Chen, L., Xing, Y. Y., Wang, Z. Y., Zhang, J. L., & Hong, M. M. (2002). The OsEBP-89 gene of rice encodes a putative EREBP transcription factor and is temporally expressed in developing endosperm and intercalary meristem. Plant Molecular Biology, 50, 379–391.

    Article  CAS  Google Scholar 

  53. Yi, S. Y., Kim, J. H., Joung, Y. H., Lee, S., Kim, W. T., Yu, S. H., & Choi, D. (2004). The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in Arabidopsis. Plant Physiology, 136, 2862–2874.

    Article  CAS  Google Scholar 

  54. Zhang, G. Y., Chen, M., Li, L. C., Xu, Z. S., Chen, X. P., Guo, J. M., & Ma, Y. Z. (2009). Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. Journal of Experimental Botany, 60, 3781–3796.

    Article  CAS  Google Scholar 

  55. Zhang, H., Zhang, D., Chen, J., Yang, Y., Huang, Z., Huang, D., Wang, X. C., & Huang, R. (2004). Tomato stress-responsive factor TSRF1 interacts with ethylene-responsive element GCC box and regulates pathogen resistance to Ralstonia solanacearum. Plant Molecular Biology, 55, 825–834.

    Article  CAS  Google Scholar 

  56. Zhang, X. L., Zhang, Z. J., Chen, J., Chen, Q., Wang, X. C., & Huang, R. F. (2005). Expressing TERF1 in tobacco enhances drought tolerance and abscisic acid sensitivity during seedling development. Planta, 222, 494–501.

    Article  CAS  Google Scholar 

  57. Wang, S., Yao, W., Wei, H., Jiang, T., & Zhou, B. (2014). Expression Patterns of ERF Genes Underlying Abiotic Stresses in Di-Haploid Populus simonii × P. Nigra. The Scientific World Journal, 2014, 1–10.

    Google Scholar 

  58. Himmelbach, A., Yang, Y., & Grill, E. (2003). Relay and control of abscisic acid signaling. Current Opinion in Plant Biology, 6, 470–479.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Natural Science Foundation of China (no. 31071448) and the Basic Research for Application project of Sichuan province (no. 2014JY0051).

Author information

Authors and Affiliations

  1. School of Life Sciences and Key Laboratory of Bio-Resources and Eco-Environment, Ministry of Education, Sichuan University, Chengdu, China

    Xuehua Wang, Haiyang Han, Jun Yan, Fang Chen & Wei Wei

Authors
  1. Xuehua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haiyang Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jun Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wei Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wei Wei.

Additional information

Novelty Statement

• A new AP2/ERF-type transcription factor gene, JcERF2, was isolated from the leaves of Jatropha curcas.

• Experiments using a binary expression vector, pBI121-JcERF2, in tobacco suggested that JcERF2 plays a role in plant defense reactions.

• The overexpression of JcERF2 in tobacco enhanced the expression of some biotic and abiotic stress-related genes, increased the accumulation of free proline and soluble carbohydrates, and conferred tolerance to drought and salt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Han, H., Yan, J. et al. A New AP2/ERF Transcription Factor from the Oil Plant Jatropha curcas Confers Salt and Drought Tolerance to Transgenic Tobacco. Appl Biochem Biotechnol 176, 582–597 (2015). https://doi.org/10.1007/s12010-015-1597-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-015-1597-z

Keywords

Search

Navigation