Abstract
The JcERF1 gene, which is related to the ERF family (ethylene responsive factor coding genes), was isolated and characterized from the oil tree Jatropha curcas. The JcERF1 protein contains conserved an AP2/EREBP DNA-binding domain of 58 amino acid residues. The JcERF1 gene could be induced by abscisic acid, high salinity, hormones, and osmotic stress, suggesting that JcERF1 is regulated by certain components of the stress-signaling pathway. The full-length and C-terminus of JcERF1 driven by the GAL4 promoter functioned effectively as a transactivator in yeast, while its N-terminus was completely inactive. Transient expression analysis using a JcERF1-mGFP fusion gene in onion epidermal cells revealed that the JcERF1 protein is targeted to the nucleus. Transgenic tobacco plants carrying CaMV35S::JcERF1 fragments were shown to be much more salt tolerant compared to wild-type plants. Our results indicate that JcERF1 is a new member of the ERF transcription factors family that may play an important role in tolerance to environmental stress.
Similar content being viewed by others
Abbreviations
- ABA:
-
abscisic acid
- 3-AT:
-
3-amino-1,2,4-aminotriazole
- CaMV:
-
cauliflower mosaic virus
- DREB:
-
dehydrationresponsive element-binding factor
- EREBP:
-
ethylene-responsive element-binding protein
- ERF:
-
ethylene-responsive factor
- LB:
-
Luria-Bertani medium
- MDA:
-
malondialdehyde
- mGFP:
-
modified green fluorescent protein
- MS:
-
Murashige-Skoog medium
- NLS:
-
nuclear localization signal
- OE:
-
overexpression of JcERF1 in tobacco
- ORF:
-
open reading frame
- PEG:
-
polyethylene glycol
- RACE:
-
rapid amplification of cDNA end
- RT-PCR:
-
reverse transcription polymerase chain reaction
- SD:
-
synthetic dropout
- TF:
-
transcription factor
- WT:
-
wild-type
References
Singh, K., Foley, R. C., and Onate-Sanchez, L. (2002) Transcription factors in plant defense and stress responses, Curr. Opin. Plant Biol., 5, 430–436.
Sakuma, Y., Liu, Q., Dubouzet, J. G., Abe, H., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and coldinducible gene expression, Biochem. Biophys. Res. Commun., 290, 998–1009.
Boutilier, K., Offringa, R., Sharma, V. K., Kieft, H., Ouellet, T., Zhang, L., Hattori, J., Liu, C. M., van Lammeren, A. A., Miki, B. L., Custers, J. B., and van Lookeren Campagne, M. M. (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth, Plant Cell, 14, 1737–1749.
Chuck, G., Meeley, R. B., and Hake, S. (1998) The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet 1, Genes Devel., 12, 1145–1154.
Elliott, R. C., Betzner, A. S., Huttner, E., Oakes, M. P., Tucker, W. Q., Gerentes, D., Perez, P., and 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.
Alonso, A., Queiroz, C. S., and Magalhaes, A. C. (1997) Chilling stress leads to increased cell membrane rigidity in roots of coffee (Coffea arabica L.) seedlings, Biochim. Biophys. Acta (BBA)-Biomembranes, 1323, 75–84.
Hu, Y. X., Wang, Y. H., Liu, X. F., and Li, J. Y. (2004) Arabidopsis RAV1 is down-regulated by brassinosteroid and may act as a negative regulator during plant development, Cell Res., 14, 8–15.
Sohn, K. H., Lee, S. C., Jung, H. W., Hong, J. K., and Hwang, B. K. (2006) Expression and functional roles of the pepper pathogen-induced transcription factor RAV1 in bacterial disease resistance, and drought and salt stress tolerance, Plant Mol. Biol., 61, 897–915.
Lee, T. I., and Young, R. A. (2000) Transcription of eukaryotic protein-coding genes, Ann. Rev. Genet., 34, 77–137.
Xu, D., Duan, X., Wang, B., Hong, B., Ho, T., and Wu, R. (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice, Plant Physiol., 110, 249–257.
Buttner, M., and Singh, K. B. (1997) Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an ocs element binding protein, Proc. Natl. Acad. Sci. USA, 94, 5961–5966.
Cao, Y., Song, F., Goodman, R. M., and Zheng, Z. (2006) Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress, J. Plant Physiol., 163, 1167–1178.
Jung, J., Won, S. Y., Suh, S. C., Kim, H., Wing, R., Jeong, Y., Hwang, I., and Kim, M. (2007) The barley ERF-type transcription factor HvRAF confers enhanced pathogen resistance and salt tolerance in Arabidopsis, Planta, 225, 575–588.
Tang, M., Sun, J., Liu, Y., Chen, F., and 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.
Yang, Z., Tian, L., Latoszek-Green, M., Brown, D., and Wu, K. (2005) Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses, Plant Mol. Biol., 58, 585–596.
Liu, H. Y., Feng, D. R., Liu B., He, Y. M., Wang, H. B., and Wang, J. F. (2009) Studies on subcellular localization of MpASR in onion epidermal cells mediated by Agrobacterium, J. Tropic. Subtrop. Bot., 17, 218–222.
Hoekema, A., Hirsch, P., Hooykaas, P., and Schilperoort, R. (1983) A binary plant vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Tiplasmid, Nature, 303, 179–180.
Murashige, T., and Skoog, F. (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures, Physiol. Plant., 15, 47373–47497.
Xiang, Y., Huang, Y., and Xiong, L. (2007) Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement, Plant Physiol., 144, 1416–1428.
Fryer, M. J., Andrews, J. R., Oxborough, K., Blowers, D. A., and Baker, N. R. (1998) Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature, Plant Physiol., 116, 571–580.
Zhang, D. Z., Wang, P. H., and Zhao, H. X. (1990) Determination of the content of free proline in wheat leaves, Plant Physiol. Commun., 4, 62–65.
Raikhel, N. (1992) Nuclear targeting in plants, Plant Physiol., 100, 1627–1632.
Okamuro, J. K., Caster, B., Villarroel, R., Van Montagu, M., and Jofuku, K. D. (1997) The AP2 domain of APETA-LA2 defines a large new family of DNA binding proteins in Arabidopsis, Proc. Natl. Acad. Sci. USA, 94, 7076–7081.
Riechmann, J., Heard, J., Martin, G., Reuber, L., Keddie, J., Adam, L., Pineda, O., Ratcliffe, O., Samaha, R., and Creelman, R. (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes, Science, 290, 2105–2110.
Hao, D., Ohme-Takagi, M., and 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, 26857–26861.
Tanimoto, M., Roberts, K., and Dolan, L. (1995) Ethylene is a positive regulator of root hair development in Arabidopsis thaliana, Plant J., 8, 943–948.
Fujimoto, S. Y., Ohta, M., Usui, A., Shinshi, H., and Ohme Takagi, M. (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression, Plant Cell Online, 12, 393–404.
Tournier, B., Sanchez-Ballesta, M. T., Jones, B., Pesquet, E., Regad, F., Latche, A., Pech, J.-C., and Bouzayen, M. (2003) New members of the tomato ERF family show specific expression pattern and diverse DNA-binding capacity to the GCC box element, FEBS Lett., 550, 149–154.
Igarashi, D., Ishida, S., Fukazawa, J., and Takahashi, Y. (2001) 14-3-3 proteins regulate intracellular localization of the bZIP transcriptional activator RSG, Plant Cell, 13, 2483–2497.
Gu, Y.-Q., Yang, C., Thara, V. K., Zhou, J., and Martin, G. B. (2000) Pti4 is induced by ethylene and salicylic acid, and its product is phosphorylated by the Pto kinase, Plant Cell Online, 12, 771–785.
Park, J. M., Park, C. J., Lee, S. B., Ham, B. K., Shin, R., and 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.
Ohta, M., Ohme-Takagi, M., and Shinshi, H. (2000) Three ethylene-responsive transcription factors in tobacco with distinct transactivation functions, Plant J. Cell Mol. Biol., 22, 29–38.
Van der Fits, L., and Memelink, J. (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism, Science, 289, 295–297.
Yi, S. Y., Kim, J.-H., Joung, Y. H., Lee, S., Kim, W. T., Yu, S. H., and Choi, D. (2004) The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in Arabidopsis, Plant Physiol., 136, 2862–2874.
Tang, W., Charles, T. M., and 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 Mol. Biol., 59, 603–617.
Wang, H., Huang, Z., Chen, Q., Zhang, Z., Zhang, H., Wu, Y., Huang, D., and Huang, R. (2004) Ectopic overexpression of tomato JERF3 in tobacco activates downstream gene expression and enhances salt tolerance, Plant Mol. Biol., 55, 183–192.
Author information
Authors and Affiliations
Corresponding author
Additional information
Published in Russian in Biokhimiya, 2014, Vol. 79, No. 11, pp. 1505–1517.
Rights and permissions
About this article
Cite this article
Yang, H., Yu, C., Yan, J. et al. Overexpression of the Jatropha curcas JcERF1 gene coding an AP2/ERF-Type transcription factor increases tolerance to salt in transgenic tobacco. Biochemistry Moscow 79, 1226–1236 (2014). https://doi.org/10.1134/S0006297914110108
Received:
Revised:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0006297914110108