Abstract
Identification of the upstream regulators of a gene is important to characterize the transcriptional pathway and the function of the gene. Previously, we found that a zinc finger protein (ThZFP1) is involved in abiotic stress tolerance of Tamarix hispida. In the present study, we further investigated the transcriptional pathway of ThZFP1. Dof motifs are abundant in the ThZFP1 promoter; therefore, we used them to screen for transcriptional regulators of ThZFP1. A Dof protein, ThDof1.4, binds to the Dof motif specifically, and was hypothesized as the upstream regulator of ThZFP1. Further study showed that overexpression of ThDof1.4 in T. hispida activated the expression of GUS controlled by the ThZFP1 promoter. In T. hispida, transient overexpression of ThDof1.4 increased the transcripts of ThZFP1; conversely, transient RNAi-silencing of ThDof1.4 reduced the expression of ThZFP1. Chromatin immunoprecipitation indicated that ThDof1.4 binds to the ThZFP1 promoter. Additionally, ThDof1.4 and ThZFP1 share similar expression patterns in response to salt or drought stress. Furthermore, like ThZFP1, ThDof1.4 could increase the proline level and enhance ROS scavenging capability to improve salt and osmotic stress tolerance. Together, these results suggested that ThDof1.4 and ThZFP1 form a transcriptional regulatory cascade involved in abiotic stress resistance in T. hispida.
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References
Abdallah H, Bauer P (2016) Quantitative reverse transcription-qPCR-based gene expression analysis in plants. Plant Signal Transduct 9–24
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Broghammer A, Krusell L, Blaise M, Sauer J, Sullivan JT, Maolanon N, Vinther M, Lorentzen A, Madsen EB, Jensen KJ, Roepstorff P, Thirup S, Ronson CW, Thygesen MB, Stougaard J (2012) Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc Natl Acad Sci USA 109:13859–13864
Budak H, Akpinar BA, Unver T, Turktas M (2013) Proteome changes in wild and modern wheat leaves upon drought stress by two-dimensional electrophoresis and nanoLC-ESI–MS/MS. Plant Mol Biol 83:89–103
Chai G, Hu R, Zhang D, Qi G, Zuo R, Cao Y, Zhou G (2012) Comprehensive analysis of CCCH zinc finger family in poplar (Populus trichocarpa). BMC Genom 13:253
Corrales AR, Nebauer SG, Carrillo L, Fernández-Nohales P, Marqués J, Renau-Morata B, Granell A, Pollmann S, Vicete-Carbajosa J, Molina PV, Medina J (2014) Characterization of tomato Cycling Dof Factors reveals conserved and new functions in the control of flowering time and abiotic stress responses. J Exp Bot 65:995–1012
Ergen NZ, Budak H (2009) Sequencing over 13 000 expressed sequence tags from six subtractive cDNA libraries of wild and modern wheats following slow drought stress. Plant Cell Environ 32:220–236
Ergen NZ, Thimmapuram J, Bohnert HJ, Budak H (2009) Transcriptome pathways unique to dehydration tolerant relatives of modern wheat. Funct Integr Genom 9:377–396
Feng B, Han Y, Xiao Y, Kuang J, Fan Z, Chen J, Lu W (2016) The banana fruit Dof transcription factor MaDof23 acts as a repressor and interacts with MaERF9 in regulating ripening-related genes. J Exp Bot 67:2263–2275
Figueiredo DD, Barros PM, Cordeiro AM, Serra TS, Lourenço T, Chander S, Margarida Oliveira, Saibo NJ (2012) Seven zinc-finger transcription factors are novel regulators of the stress responsive gene OsDREB1B. J Exp Bot 63:3643–3656
Gao Y, Nishikawa H, Badejo AA, Shibata H, Sawa Y, Nakagawa T, Ishikawa T (2011) Expression of aspartyl protease and C3HC4-type RING zinc finger genes are responsive to ascorbic acid in Arabidopsis thaliana. J Exp Bot 62:3647–3657
Gupta S, Malviya N, Kushwaha H, Nasim J, Bish NC, Singh VK, Yadav D (2015) Insights into structural and functional diversity of Dof (DNA binding with one finger) transcription factor. Planta 241:549–562
Jefferson R, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901
Ji XY, Zheng L, Liu Yj, Nie XG, Liu SN, Wang YC (2014) A transient transformation system for the functional characterization of genes involved in stress response. Plant Mol Biol Rep 32:732–739
Jung YJ, Lee IH, Nou IS, Lee KD, Rashotte AM, Kang KK (2013) BrRZFP1 a Brassica rapa C3HC4-type RING zinc finger protein involved in cold, salt and dehydration stress. Plant Biol 15:274–283
Kim WC, Ko JH, Kim JY, Kim J, Bae HJ, Han KH (2013) MYB46 directly regulates the gene expression of secondary wall-associated cellulose synthases in Arabidopsis. Plant J 73:26–36
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408
Lucas S, Durmaz E, Akpınar BA, Budak H (2011) The drought response displayed by a DRE-binding protein from Triticum dicoccoides. Plant Physiol Biochem 49:346–351
Lucas-Reina E, Romero-Campero FJ, Romero JM, Valverde F (2015) An evolutionarily conserved DOF-CONSTANS module controls plant photoperiodic signaling. Plant Physiol 168:561–574
Noguero M, Atif RM, Ochatt S, Thompson RD (2013) The role of the DNA-binding one zinc finger (DOF) transcription factor family in plants. Plant Sci 209:32–45
Peng X, Zhao Y, Cao J, Zhang W, Jiang H, Li X, Cheng B (2012) CCCH-type zinc finger family in maize: genome-wide identification, classification and expression profiling under abscisic acid and drought treatments. PLoS ONE 7:e40120
Prestele J, Hierl G, Scherling C, Hetkamp S, Schwechheimer C, Isono E, Gietl C (2010) Different functions of the C3HC4 zinc RING finger peroxins PEX10, PEX2, and PEX12 in peroxisome formation and matrix protein import. Proc Natl Acad Sci 107:14915–14920
Santopolo S, Boccaccini A, Lorrai R, Ruta V, Capauto D, Minutello E, Serino G, Costantino P, Vittorioso P (2015) DOF AFFECTING GERMINATION 2 is a positive regulator of light-mediated seed germination and is repressed by DOF AFFECTING GERMINATION 1. BMC Plant Biol 15:1
Stone SL, Hauksdóttir H, Troy A, Herschleb J, Kraft E, Callis J (2005) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol 137:13–30
Wang L, Xu C, Wang C, Wang Y (2012) Characterization of a eukaryotic translation initiation factor 5A homolog from Tamarix androssowii involved in plant abiotic stress tolerance. BMC Plant Biol 12:1
Wang C, Gao C, Wang L, Zheng L, Yang C, Wang Y (2014) Comprehensive transcriptional profiling of NaHCO3-stressed Tamarix hispida roots reveals networks of responsive genes. Plant Mol Biol 84:145–157
Wang G, Wei P, Tan F, Yu M, Zhang X, Chen Q, Wang X (2016) The transcription factor AtDOF4. 7 is involved in ethylene-and IDA-mediated organ abscission in Arabidopsis. Front Plant Sci 7:863
Wu W, Cheng Z, Liu M, Yang X, Qiu D (2014) C3HC4-type RING finger protein Nb ZFP1 is involved in growth and fruit development in Nicotiana benthamiana. PLoS ONE 9:e99352
Xu P, Chen H, Ying L, Cai W (2016) AtDOF5. 4/OBP4, a DOF transcription factor gene that negatively regulates cell cycle progression and cell expansion in Arabidopsis thaliana. Sci Rep 6
Yang C, Fang X, Wu X, Mao Y, Wang L, Chen X (2012) Transcriptional regulation of plant secondary metabolism. J Integr Plant Biol 54:703–712
Yang Y, Fu D, Zhu C, He Y, Zhang H, Liu T, Wu C (2015) The RING-finger ubiquitin ligase HAF1 mediates heading date 1 degradation during photoperiodic flowering in rice. Plant Cell 27:2455–2468
Yu Y, Xu W, Wang J, Wang L, Yao W, Yang Y, Xu Y, Ma F, Du Y, Wang Y (2013) The Chinese wild grapevine (Vitis pseudoreticulata) E3 ubiquitin ligase Erysiphe necator-induced RING finger protein 1 (EIRP1) activates plant defense responses by inducing proteolysis of the VpWRKY11 transcription factor. New Phytol 200:834–846
Zang D, Wang C, Ji X, Wang Y (2015) Tamarix hispida zinc finger protein ThZFP1 participates in salt and osmotic stress tolerance by increasing proline content and SOD and POD activities. Plant Sci 235:111–121
Zeba N, Isbat M, Kwon NJ, Lee MO, Kim SR, Hong CB (2009) Heat-inducible C3HC4 type RING zinc finger protein gene from Capsicum annuum enhances growth of transgenic tobacco. Planta 229:861
Zhang Y, Yang C, Li Y, Zheng N, Chen H, Zhao Q, Xie Q (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 19:1912–1929
Zhang X, Wang L, Meng H, Wen H, Fan Y, Zhao J (2011) Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species. Plant Mol Biol 75:365–378
Funding
The funding was provided by the project of the culture of the young scientists in scientific innovation in Xinjiang Province (Grant No. 201371101), Innovation Project of State Key Laboratory of Tree Genetics and Breeding (Grant No. 2013A05) and Fundamental Research Funds for the Central Universities (Grant No. 2572015AA08).
Author contributions
YW designed research and wrote the paper. DZ performed research. DZ analyzed data and wrote the paper. LW and YZ contributed to genes expression analysis. HZ cloned the gene. All the authors reviewed the manuscript.
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Zang, D., Wang, L., Zhang, Y. et al. ThDof1.4 and ThZFP1 constitute a transcriptional regulatory cascade involved in salt or osmotic stress in Tamarix hispida . Plant Mol Biol 94, 495–507 (2017). https://doi.org/10.1007/s11103-017-0620-x
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DOI: https://doi.org/10.1007/s11103-017-0620-x