Abstract
The plant-specific NAC (for NAM, ATAF1,2 and CUC2) proteins have been found to play important roles in plant development and stress responses. In this study, a NAC gene CarNAC1 (for Cicer arietinum L. NAC gene 1) was isolated from a cDNA library constructed with chickpea seedling leaves treated by polyethylene glycol. CarNAC1 encoded a putative protein with 239 amino acids and contained 3 exons and 2 introns within genomic DNA sequence. CarNAC1 had a conserved NAC domain in the N-terminus and the CarNAC1:GFP (green fluorescent protein) fusion protein was localized in the nucleus of onion epidermal cells. Additionally, CarNAC1 exhibited the trans-activation activity which was mapped to the C-terminus. The CarNAC1 transcript was detected in many chickpea organs including seedling leaves, stems, roots, flowers, and young pods, but less accumulated in young seeds. CarNAC1 was induced by leaf age and showed changes in expression during seed development and germination. Furthermore, the expression of CarNAC1 was strongly induced by drought, salt, cold, wounding, H2O2, ethephon, salicylic acid, indole-3-acetic acid, and gibberellin. Our results suggest that CarNAC1 encodes a novel NAC-domain protein and may be a transcriptional activator involved in plant development and various stress responses.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- 6-BA:
-
N-6-benzyl-adenine
- CUC:
-
Up-shaped cotyledon
- DAF:
-
Days after flowering
- EST:
-
Expressed sequence tag
- ET:
-
Ethephon
- GA3:
-
Gibberellin
- GFP:
-
Green fluorescent protein
- IAA:
-
Indole-3-acetic acid
- MeJA:
-
Methyl jasmonate
- NAC:
-
NAM, ATAF1,2 and CUC2
- NST:
-
NAC secondary wall thickening promoting factor
- ORF:
-
Open reading frame
- PEG:
-
Polyethylene glycol
- RACE:
-
Rapid amplification of cDNA end
- RT-PCR:
-
Reverse transcription polymerase chain reaction
- SA:
-
Salicylic acid
- SD:
-
Synthetic defined medium
- SENU5:
-
Senescence up-regulated 5
References
Ooka, H., Satoh, K., Doi, K., Nagata, T., Otomo, Y., Murakami, K., et al. (2003). Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Research, 10, 239–247.
Olsen, A. N., Ernst, H. A., Leggio, L. L., & Skriver, K. (2005). NAC transcription factors: structurally distinct, functionally diverse. Trends in Plant Science, 10, 79–87.
Souer, E., van Houwelingen, A., Kloos, D., Mol, J., & Koes, R. (1996). The No Apical Meristem gene of petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell, 85, 159–170.
He, X. J., Mu, R. L., Cao, W. H., Zhang, Z. G., Zhang, J. S., & Chen, S. Y. (2005). AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant Journal, 44, 903–916.
Uauy, C., Distelfeld, A., Fahima, T., Blechl, A., & Dubcovsky, J. (2006). A NAC gene regulating senescence improves grain protein, zinc, and iron content in Wheat. Science, 314, 1298–1301.
Guo, Y. F., & Gan, S. S. (2006). AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant Journal, 46, 601–612.
Yoo, S. Y., Kim, Y., Kim, S. Y., Lee, J. S., & Ahn, J. H. (2007). Control of flowering time and cold response by a NAC-domain protein in Arabidopsis. PLoS ONE, 7, e642.
Mitsuda, N., Iwase, A., Yamamoto, H., Yoshida, M., Seki, M., Shinozaki, K., et al. (2007). NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell, 19, 270–280.
Nakashima, K., Tran, L. P., Nguyen, D. V., Fujita, M., Maruyama, K., Todaka, D., et al. (2007). Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. The Plant Journal, 51, 617–630.
FAOSTAT Database. (2006). http://www.faostat.fao.org/.
Arumuganathan, K., & Earle, E. D. (1991). Nuclear DNA content of some important plant species. Plant Molecular Biology, 9, 208–218.
Rajesh, P. N., O’Bleness, M., Roe, B. A., & Muehlbauer, F. J. (2008). Analysis of genome organization, composition and microsynteny using 500 kb BAC sequences in chickpea. Theoretical and Applied Genetics, 177, 449–458.
Singh, K. B., Ocampo, B., & Robertson, L. D. (1998). Diversity for abiotic and biotic stress resistance in the wild annual Cicer species. Genetic Resources and Crop Evolution, 45, 9–17.
Gao, W. R., Wang, X. S., Liu, Q. Y., Peng, H., Chen, C., Li, J. G., et al. (2008). Comparative analysis of ESTs in response to drought stress in chickpea (C. arietinum L.). Biochemical and Biophysical Research Communications, 376, 578–583.
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876–4882.
Saitou, N., & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology Evolution, 13, 964–969.
Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning, a laboratory manual. NY: Cold Spring Harbor.
Horsch, R. B., Fry, J., Hoffmann, N., Neidermeyer, J., Rogers, S. G., & Fraley, R. T. (1988). Leaf disc transformation plant molecular biology manual (pp. 1–9). Dordrecht: Kluwer.
Hu, H., Dai, M., Yao, J., Xiao, B., Li, X., Zhang, Q., et al. (2006). Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proceedings of the National Academy of Sciences of the United States of America, 103, 12987–12992.
Lu, P. L., Chen, N. Z., An, R., Su, Z., Qi, B. S., Ren, F., et al. (2007). A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Molecular Biology, 63, 289–305.
Liu, X. A., & Baird, W. V. (2003). Differential expression of genes regulated in response to drought or salinity stress in sunflower. Crop Science, 43, 678–687.
Tran, L. P., Quach, T. N., Guttikonda, S. K., Aldrich, D. L., Kumar, R., Neelakandan, A., et al. (2009). Molecular characterization of stress-inducible GmNAC genes in soybean. Molecular Genetics and Genomics. [Epub ahead of print]. doi:10.1007/s00438-009-0436-8.
Guilfoyle, T. J., & Hagen, G. (2007). Auxin response factors. Current Opinion in Plant Biology, 10, 453–460.
Schwechheimer, C. (2008). Understanding gibberellic acid signaling are we there yet? Current Opinion Plant Biology, 11, 9–15.
John, I., Hackett, R., Cooper, W., Drake, R., Farrell, A., & Grierson, D. (1997). Cloning and characterization of tomato leaf senescence-related cDNAs. Plant Molecular Biology, 33, 641–651.
Zhong, R., Demura, T., & Ye, Z. H. (2006). SND1, A NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell, 18, 3158–3170.
Kubo, M., Udagawa, M., Nishikubo, N., Horiguchi, G., Yamaguchi, M., Ito, J., et al. (2005). Transcription switches for protoxylem and metaxylem vessel formation. Genes Development, 19, 1855–1860.
Fujita, M., Fujita, Y., Maruyama, K., Seki, M., Hiratsu, K., Ohme-Takagi, M., et al. (2004). A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant Journal, 39, 863–876.
Tran, L. P., Nakashima, K., Sakuma, Y., Simpson, S. D., Fujita, Y., Maruyama, K., et al. (2004). Isolation and functional analysis of Arabidopsis stress inducible NAC transcription factors that bind to a drought responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell, 16, 2481–2498.
Glazebrook, J. (2001). Genes controlling expression of defense responses in Arabidopsis. Current Opinion Plant Biology, 4, 301–308.
Mengiste, T., Chen, X., Salmeron, J., & Dietrich, R. (2003). The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell, 15, 2551–2565.
Binyamin, L., Falah, M., Portnoy, V., Soudry, E., & Gepstein, S. (2001). The early light-induced protein is also produced during leaf senescence of Nicotiana tabacum. Planta, 212, 591–597.
Weaver, L. M., Gan, S., Quirino, B., & Amasino, R. M. (1998). A comparison of the expression patterns of several senescence associated genes in response to stress and hormone treatment. Plant Molecular Biology, 37, 455–469.
Peng, H., Cheng, H. Y., Chen, C., Yu, X. W., Yang, J. N., Gao, W. R., et al. (2009). A NAC transcription factor gene of Chickpea (Cicer arietinum), CarNAC3, is involved in drought stress response and various developmental processes. Journal of Plant Physiology. doi:10.1016/j.jplph.2009.05.013.
Acknowledgments
We gratefully acknowledge the financial support from the 111 Project supported by the Ministry of Education of China, from projects supported by the National Science and Technology Ministry of China (2007BAC15B06, 2006BAD09A04, 2006BAD09A08), from a project supported by the National Natural Science Foundation of China (30860152), from a project supported by the Xinjiang Science and Technology Department of China (200991254), and from a project supported by the Key Teacher Foundation of Guangxi Normal University, China, for this research. We also thank Prof. Lizhong Xiong from Huazhong Agricultural University, China, for kindly supplying the trans-activation system.
Author information
Authors and Affiliations
Corresponding author
Additional information
H. Peng and X. Yu contributed equally to this study.
An erratum to this article is available at http://dx.doi.org/10.1007/s12033-016-9916-3.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Peng, H., Yu, X., Cheng, H. et al. Cloning and Characterization of a Novel NAC Family Gene CarNAC1 from Chickpea (Cicer arietinum L.). Mol Biotechnol 44, 30–40 (2010). https://doi.org/10.1007/s12033-009-9202-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12033-009-9202-8