Abstract
Key message
DgNAC1, a transcription factor of chrysanthemum, was functionally verified to confer salt stress responses by regulating stress-responsive genes.
Abstract
NAC transcription factors play effective roles in resistance to different abiotic stresses, and overexpressions of NAC TFs in Arabidopsis have been proved to be conducive in improving salinity tolerance. However, functions of NAC genes in chrysanthemum continue to be poorly understood. Here, we performed physiology and molecular experiments to evaluate roles of DgNAC1 in chrysanthemum salt stress responses. In this study, DgNAC1-overexpressed chrysanthemum was obviously more resistant to salt over the WT (wild type). Specifically, the transgenic chrysanthemum showed a higher survival rate and lower EC (electrolyte conductivity) than WT under salt stress. The transgenic chrysanthemum also showed fewer accumulations of MDA (malondialdehyde) and reactive oxygen species (H2O2 and O2 −), greater activities of SOD (superoxide dismutase), POD (peroxidase) and CAT (catalase), as well as more proline content than WT under salt stress. Furthermore, stress-responsive genes in transgenic chrysanthemum were greater up-regulated than in WT under salinity stress. Thus, all results revealed that DgNAC1 worked as a positive regulator in responses to salt stress and it may be an essential gene for molecular breeding of salt-tolerant plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274. doi:10.1007/s00299-006-0204-8
An G, Watson BD, Chiang CC (1988) Transformation of tobacco, tomato, potato, and Arabidopsis thaliana using a binary Ti vector system. Plant Physiol 81:301–305. doi:10.1104/pp.81.1.301
An J, Song A, Guan Z, Jiang J, Chen F, Lou W, Liu Z, Chen S (2014) The over-expression of Chrysanthemum crassum CcSOS1 improves the salinity tolerance of chrysanthemum. Mol Biol Rep 41:4155–4162. doi:10.1007/s11033-014-3287-2
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. doi:10.1146/annurev.arplant.55.031903.141701
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. doi:10.1016/0003-2697(71)90370-8
Chen S, Cui X, Chen Y, Gu C, Miao H, Gao H, Chen F, Liu Z, Guan Z, Fang W (2011) CgDREBa transgenic chrysanthemum confers drought and salinity tolerance. Environ Exp Bot 74:255–260. doi:10.1016/j.envexpbot.2011.06.007
Chen L, Chen Y, Jiang J, Chen S, Chen F, Guan Z, Fang W (2012a) The constitutive expression of Chrysanthemum dichrum ICE1 in Chrysanthemum grandiflorum improves the level of low temperature, salinity and drought tolerance. Plant Cell Rep 31:1747–1758. doi:10.1007/s00299-012-1288-y
Chen LG, Song Y, Li SJ, Zhang L, Zou C, Yu D (2012b) The role of WRKY transcription factors in plant abiotic stresses. Biochim Biophys Acta 1819:120–128. doi:10.1016/j.bbagrm.2011.09.002
Chinnusamy V, Zhu J, Zhu JK (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126:52–61. doi:10.1111/j.1399-3054.2006.00596.x
Farmer EE, Mueller MJ (2013) ROS-mediated lipid peroxidation and RES-activated signaling. Annu Rev Plant Biol 64:429–450. doi:10.1146/annurev-arplant-050312-120132
Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC(NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992. doi:10.1073/pnas.0604882103
Irigoyen JJ, Emerich DW, Sanchez-Diaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60. doi:10.1111/j.1399-3054.1992.tb08764.x
Jaleel CA, Riadh K, Gopi R, Manivannan P, Ines J, Al-Juburi HJ, Zho CX, Shao HB, Panneerselvam R (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant 31:427–436. doi:10.1007/s11738-009-0275-6
Li P, Song A, Gao C, Wang L, Sun J, Jiang J, Chen F, Chen S (2015) Chrysanthemum WRKY gene CmWRKY17 negatively regulates salt stress tolerance in transgenic chrysanthemum and Arabidopsis plants. Plant Cell Rep 34:1365–1378. doi:10.1007/s00299-015-1793-x
Lindemose S, O’Shea C, Jensen MK, Skriver K (2013) Structure, function and networks of transcription factors involved in abiotic stress responses. Int J Mol Sci 14:5842–5878. doi:10.3390/ijms14035842
Liu K, Wang L, Xu Y, Chen N, Ma Q, Li F, Chong K (2007) Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice. Planta 226:007–1016. doi:10.1007/s00425-007-0548-5
Liu QL, Xu KD, Zhao LJ, Pan YZ, Jiang BB, Zhang HQ, Liu GL (2011) Overexpression of a novel chrysanthemum NAC transcription factor gene enhances salt tolerance in tobacco. Biotechnol Lett 33:2073–2082. doi:10.1007/s10529-011-0659-8
Liu QL, Zhong M, Li S, Pan YZ, Jiang BB, Jia Y, Zhang HQ (2013) Overexpression of a chrysanthemum transcription factor gene, DgWRKY3, in tobacco enhances tolerance to salt stress. Plant Physiol Biochem 69:27–33. doi:10.1016/j.plaphy.2013.04.016
Mao X, Zhang H, Qian X, Li A, Zhao G, Jing R (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 63:2933–2946. doi:10.1093/jxb/err462
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–457. doi:10.1111/j.1365-3040.2009.02041.x
Mittler R, Vanderauwera S, Gollery M, Breusegem FV (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. doi:10.1016/j.tplants.2004.08.009
Morran S, Eini O, Pyvovarenko T, Parent B, Singh R, Ismagul A, Eliby S, Shirley N, Langridge P, Lopato S (2011) Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol J 9:50–63. doi:10.1111/j.1467-7652.2010.00547.x
Nakashima K, Tran LS, Dong VN, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630. doi:10.1111/j.1365-313X.2007.03168.x
Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95. doi:10.1104/pp.108.129791
Nuruzzaman M, Sharoni AM, Kikuchi S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol 4:248. doi:10.3389/fmicb.2013.00248
Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, Hayashizaki Y, Suzuki K, Kojima K, Takahara Y, Yamamoto K, Kikuchi S (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247. doi:10.1093/dnares/10.6.239
Pan Y, Wu LJ, Yu ZL (2006) Effect of salt and drought stress on antioxidant enzymes activities and SOD isoenzymes of liquorice (Glycyrrhiza uralensis fisch). Plant Growth Regul 49:157–165. doi:10.1007/s10725-006-9101-y
Puhakainen T, Hess MW, Makela P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–753. doi:10.1023/B:PLAN.0000040903.66496.a4
Ranieri A, Petacco F, Castagna A, Soldatini GF (2000) Redox state and peroxidase system in sunflower plants exposed to ozone. Plant Sci 159:159–167. doi:10.1016/S0168-9452(00)00352-6
Shi J, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH (2010) Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol 30:914–922. doi:10.1093/treephys/tpq030
Shibuya K, Shimizu K, Niki T, Ichimura K (2014) Identification of a NAC transcription factor, EPHEMERAL1, that controls petal senescence in Japanese morning glory. Plant J 79:1044–1051. doi:10.1111/tpj.12605
Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223. doi:10.1016/S1369-5266(00)80068-0
Singh SK, Sharma HC, Goswami AM, Datta SP, Singh SP (2000) In vitro growth and leaf composition of grapevine cultivars as affected by sodium chloride. Biol Plant 43:283–286. doi:10.1023/A:1002720714781
Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (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. doi:10.1105/tpc.104.022699
Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132. doi:10.1016/j.copbio.2005.02.001
Wu Y, Deng Z, Lai J, Zhang Y, Yang C, Yin B, Zhao Q, Zhang L, Li Y, Yang C, Xie Q (2009) Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res 19:1279–1290. doi:10.1038/cr.2009.108
Xing X, Liu YK, Kong XP, Liu Y, Li DQ (2011) Overexpression of a maize dehydrin gene, ZmDHN2b, in tobacco enhances tolerance to low temperature. Plant Growth Regul 65:109–118. doi:10.1007/s10725-011-9580-3
Yang Y, Zhu K, Wu J, Liu L, Sun G, He Y, Chen F, Yu D (2016) Identification and characterization of a novel NAC-like gene in chrysanthemum (Dendranthema lavandulifolium). Plant Cell Rep 35:1783–1798. doi:10.1007/s00299-016-1996-9
Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2009) Tolerance to various environmental stresses conferred by the salt-responsive rice gene ONAC063 in transgenic Arabidopsis. Planta 229:1065–1075. doi:10.1007/s00425-009-0895-5
Yokotani N, Tsuchida-Mayama T, Ichikawa H, Mitsuda N, Ohme-Takagi M, Kaku H, Minami E, Nishizawa Y (2014) OsNAC111, a blast disease-responsive transcription factor in rice, positively regulates the expression of defense-related genes. Mol Plant-Microbe Interact 27:1027–1034. doi:10.1094/MPMI-03-14-0065-R
Zhang J, Kirkham MB (1996) Antioxidant responses to drought in sunflower and sorghum seedlings. New Phytol 132:361–373. doi:10.1111/j.1469-8137.1996.tb01856.x
Zhang L, Tian LH, Zhao JF, Song Y, Zhang CJ, Guo Y (2009) Identification of an apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol 149:916–928. doi:10.1104/pp.108.131144
Zhang L, Xi D, Luo L, Meng F, Li Y, Wu CA, Guo X (2011) Cotton GhMPK2 is involved in multiple signaling pathways and mediates defense responses to pathogen infection and oxidative stress. FEBS J 278:1367–1378. doi:10.1111/j.1742-4658.2011.08056.x
Zheng X, Chen B, Lu G, Han B (2009) Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem Biophys Res Commun 379:985–989. doi:10.1016/j.bbrc.2008.12.163
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. doi:10.1146/annurev.arplant.53.091401.143329
Acknowledgements
This research was supported by National Natural Science Foundation of China (31201649).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interests.
Additional information
Communicated by Hiroyasu Ebinuma.
Rights and permissions
About this article
Cite this article
Wang, K., Zhong, M., Wu, Yh. et al. Overexpression of a chrysanthemum transcription factor gene DgNAC1 improves the salinity tolerance in chrysanthemum. Plant Cell Rep 36, 571–581 (2017). https://doi.org/10.1007/s00299-017-2103-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-017-2103-6