Skip to main content
Log in

Genome-Wide Analysis of the C3H Zinc Finger Transcription Factor Family and Drought Responses of Members in Aegilops tauschii

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Transcription factors regulate gene expression in response to various external and internal cues by activating or suppressing downstream genes. In this study, a comprehensive computational analysis identified 36 C3H zinc finger family genes in Aegilops tauschii. Phylogenetic analysis divided the C3H zinc finger family into seven subfamilies. According to a de novo transcriptome assembly, ten C3H zinc finger genes were drought-induced; among them, AetTZF1 showed the most significant transcript level. Transient expression in A. tauschii protoplasts indicated that AetTZF1 protein was localized in the cell membrane. Yeast transactivation assays suggested that AetTZF1 could activate transcription in yeast. AetTZF1 increased stress tolerance to drought by promoting root growth and increasing germination rates in Arabidopsis. Overexpression of AetTZF1 led to an altered expression level of stress-related genes that made the plants more tolerant to drought. Putative cis-acting elements involved in abiotic stresses were observed in the AetTZF1 promoter region. Our comparative genomics analysis of C3H zinc finger family genes in A. tauschii provides data for functional dissection of this family.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

Abbreviations

ABA:

abscisic acid

ANK:

ankyrin

ARE:

AU-rich element

DBD:

DNA binding domain

Q-RT-PCR:

quantitative real-time PCR

TTP:

tristetraprolin

TZF:

tandem C3H-zinc finger

WT:

wild-type

References

  • Asad J, Maruyama K, Todaka D, Kidokoro S, Abo M, Yoshimura E, Shinozaki K, Nakashima K, Yamaguchi-Shinozaki K (2013) OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stress-related genes. Plant Physiol 161:1202–1216

    Article  Google Scholar 

  • Bechtold N, Pelletier G (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82:259–266

    PubMed  CAS  Google Scholar 

  • Berg JM, Shi Y (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science 271:1081–1085

    Article  PubMed  CAS  Google Scholar 

  • Blackshear PJ (2002) Tristetraprolin and other CCCH tandem zinc-finger proteins in the regulation of mRNA turnover. Biochem Soc Trans 30:945–952

    Article  PubMed  CAS  Google Scholar 

  • Blackshear PJ, Phillips RS, Lai WS (2005) Zfp36l3, a rodent X chromosome gene encoding a placenta-specific member of the tristetraprolin family of CCCH tandem zinc finger proteins. Biol Reprod 73:297–307

    Article  PubMed  CAS  Google Scholar 

  • Bogamuwa S, Jang JC (2013) The Arabidopsis tandem CCCH zinc finger proteins AtTZF4, 5 and 6 are involved in light-, abscisic acid- and gibberellic acid-mediated regulation of seed germination. Plant Cell Environ 36:1507–1519

    Article  PubMed  CAS  Google Scholar 

  • Carballo E, Lai WS, Blackshear PJ (1998) Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 281:1001–1005

    Article  PubMed  CAS  Google Scholar 

  • Carrick DM, Lai WS, Blackshear PJ (2004) The tandem CCCH zinc finger protein tristetraprolin and its relevance to cytokine mRNA turnover and arthritis. Arthritis Res Ther 6:248–264

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cattivelli L, Rizza F, Badeck FW, Mazzucotelli E, Mastrangelo AM, Francia E, Mare C, Tondelli A, Stanca AM (2008) Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crops Res 105:1–14

    Article  Google Scholar 

  • Cui J, Jander G, Racki LR, Kim PD, Pierce NE, Ausubel FM (2002) Signals involved in Arabidopsis resistance to Trichoplusia ni caterpillars induced by virulent and avirulent strains of the phytopathogen Pseudomonas syringae. Plant Physiol 129:551–564

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • De J, Lai WS, Thorn JM, Goldsworthy SM, Liu X, Blackwell TK, Blackshear PJ (1999) Identification of four CCCH zinc finger proteins in Xenopus, including a novel vertebrate protein with four zinc fingers and severely restricted expression. Gene 228:133–145

    Article  PubMed  CAS  Google Scholar 

  • Delaney KJ, Xu R, Zhang J, Li QQ, Yun KY, Falcone DL, Hunt AG (2006) Calmodulin interacts with and regulates the RNA-binding activity of an Arabidopsis polyadenylation factor subunit. Plant Physiol 140:1507–1521

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Deng H, Liu H, Li X, Xiao J, Wang S (2012) A CCCH-type zinc finger nucleic acid-binding protein quantitatively confers resistance against rice bacterial blight disease. Plant Physiol 158:876–889

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Diaz I, Vicente-Carbajosa J, Abraham Z, Martínez M, Moneda I-L, Carbonero P (2002) The GAMYB protein from barley interacts with the DOF transcription factor BPBF and activates endosperm-specific genes during seed development. Plant J 29:453–464

    Article  PubMed  CAS  Google Scholar 

  • Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploidy wheat under domestication. Science 316:1862–1866

    Article  PubMed  CAS  Google Scholar 

  • DuBois RN, McLane MW, Ryder K, Lau LF, Nathans D (1990) A growth factor-inducible nuclear protein with a novel cysteine/histidine repetitive sequence. J Biol Chem 265:19185–19191

    PubMed  CAS  Google Scholar 

  • Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319

    Article  PubMed  CAS  Google Scholar 

  • Fox AH, Kowalski K, King GF, Mackay JP, Crossley M (1998) Key residues characteristic of GATA N-fingers are recognized by FOG. J Biol Chem 23:1–4

    CAS  Google Scholar 

  • Fox AH, Liew C, Holmes M, Kowalski K, Mackay J, Crossley M (1999) Transcriptional cofactors of the FOG family interact with GATA proteins by means of multiple zinc fingers. EMBO J 18:2812–2822

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gomperts M, Pascall JC, Brown KD (1990) The nucleotide sequence of a cDNA encoding an EGF-inducible gene indicates the existence of a new family of mitogen-induced genes. Oncogene 5:1081–1083

    PubMed  CAS  Google Scholar 

  • Guo YH, Yu YP, Wang D, Wu CA, Yang GD, Huang JG, Zheng CC (2009) GhZFP1, a novel CCCH-type zinc finger protein from cotton, enhances salt stress tolerance and fungal disease resistance in transgenic tobacco by interacting with GZIRD21A and GZIPR5. New Phytol 183:62–75

    Article  PubMed  CAS  Google Scholar 

  • Hall TM (2005) Multiple modes of RNA recognition by zinc finger proteins. Curr Opin Struct Biol 15:367–373

    Article  PubMed  CAS  Google Scholar 

  • International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768

    Article  Google Scholar 

  • Jan A, Maruyama K, Todaka D, Kidokoro S, Abo M, Yoshimura E, Shinozaki K, Nakashima K, Yamaguchi-Shinozaki K (2013) OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stress-related genes. Plant Physiol 161:1202–1216

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jia J, Zhao S, Kong X (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496:91–95

    Article  PubMed  CAS  Google Scholar 

  • Jin JP, Zhang H, Kong L, Gao G, Luo JC (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42:1182–1187

    Article  Google Scholar 

  • Kim DH, Yamaguchi S, Lim S, Oh E, Park J, Hanada A, Kamiya Y, Choi G (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell 20:1260–1277

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kong Z, Li M, Yang W, Xu W, Xue Y (2006) A novel nuclear-localized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol 141:1376–1388

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Krohn NM, Yanagisawa S, Grasser KD (2002) Specificity of the stimulatory interaction between chromosomal HMGB proteins and the transcription factor Dof2 and its negative regulation by protein kinase CK2-mediated phosphorylation. J Biol Chem 277:32438–32444

    Article  PubMed  CAS  Google Scholar 

  • Lai WS, Stumpo DJ, Blackshear PJ (1990) Rapid insulin-stimulated accumulation of an mRNA encoding a proline-rich protein. J Biol Chem 265:16556–16563

    PubMed  CAS  Google Scholar 

  • Lai WS, Carballo E, Strum JR, Kennington EA, Phillips RS, Blackshear PJ (1999) Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol 19:4311–4323

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lee JS, Galvin KM, Shi Y (1993) Evidence for physical interaction between the zinc-finger transcription factors YY1 and Sp1. Proc Natl Acad Sci U S A 90:6145–6149

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lee BM, Xu J, Clarkson BK, Martinez-Yamout MA, Dyson HJ, Case DA, Gottesfeld JM, Wright PE (2006) Induced fit and “lock and key” recognition of 5S RNA by zinc fingers of transcription factor IIIA. J Mol Biol 357:275–291

    Article  PubMed  CAS  Google Scholar 

  • Lee SJ, Jung HJ, Kang H, Kim SY (2012) Arabidopsis zinc finger proteins AtC3H49/AtTZF3 and AtC3H20/AtTZF2 are involved in ABA and JA responses. Plant Cell Physiol 53:673–686

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Thomas TL (1998) PEI1, an embryo-specific zinc finger protein gene required for heart-stage embryo formation in Arabidopsis. Plant Cell 10:383–398

    PubMed  CAS  PubMed Central  Google Scholar 

  • Li J, Jia D, Chen X (2001) HUA1, a regulator of stamen and carpel identities in Arabidopsis, codes for a nuclear RNA binding protein. Plant Cell 13:2269–2281

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lin PC, Pomeranz MC, Jikumaru Y, Kang SG, Hah C, Fujioka S, Kamiya Y, Jang JC (2011) The Arabidopsis tandem zinc finger protein AtTZF1 affects ABA- and GA-mediated growth, stress and gene expression responses. Plant J 65:253–268

    Article  PubMed  CAS  Google Scholar 

  • Liu P, Xu ZS, Pan-Pan L, Hu D, Chen M, Li LC, Ma YZ (2013) A wheat PI4K gene whose product possesses threonine autophosphorylation activity confers tolerance to drought and salt in Arabidopsis. J Exp Bot 64:2915–2927

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta DeltaC(T)) method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Lu D, Searles MA, Klug A (2003) Crystal structure of a zinc-finger–RNA complex reveals two modes of molecular recognition. Nature 426:96–100

    Article  PubMed  CAS  Google Scholar 

  • Ma Q, Wadleigh D, Chi T, Herschman H (1994) The Drosophila TIS11 homologue encodes a developmentally controlled gene. Oncogene 9:3329–3334

    PubMed  CAS  Google Scholar 

  • Mackay JP, Crossley M (1998) Zinc fingers are sticking together. Trends Biochem Sci 23:1–4

    Article  PubMed  CAS  Google Scholar 

  • Mello CC, Schubert C, Draper B, Zhang W, Lobel R, Priess JR (1996) The PIE-1 protein and germline specification in C. elegans embryos. Nature 382:710–712

    Article  PubMed  CAS  Google Scholar 

  • Mohler J, Weiss N, Murli S, Mohammadi S, Vani K, Vasilakis G, Song CH, Epstein A, Kuang T, English J (1992) The embryonically active gene, unkempt, of Drosophila encodes a Cys3His finger protein. Genetics 131:377–388

    PubMed  CAS  PubMed Central  Google Scholar 

  • Moore M, Ullman C (2003) Recent developments in the engineering of zinc finger proteins. Brief Funct Genomics Proteomics 1:342–355

    Article  CAS  Google Scholar 

  • Muhamman J, Waqas I, Asia B (2010) Constitutive expression of OsC3H33, OsC3H50 and OsC3H37 genes in rice under salt stress. Pak J Bot 42:4003–4009

    Google Scholar 

  • Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci U S A 101:6309–6314

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nie XF, Maclean KN, Kumar V, McKay IA, Bustin SA (1995) ERF-2, the human homologue of the murine Tis11d early response gene. Gene 152:285–286

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Peng X, Zhao Y, Cao J, Zhang W, Jiang H, Li X, Ma Q, Zhu S, 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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pomeranz MC, Hah C, Lin PC, Kang SG, Finer JJ, Blackshear PJ, Jang JC (2009) The Arabidopsis tandem zinc finger protein AtTZF1 traffics between the nucleus and cytoplasmic foci and binds both DNA and RNA. Plant Physiol 152:151–165

    Article  PubMed  Google Scholar 

  • Pomeranz M, Zhang L, Finer J, Jang J-C (2011) Can AtTZF1 act as a transcriptional activator or repressor in plants? Plant Signal Behav 6:719–722

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Price J, Laxmi A, St Martin SK, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16:2128–2150

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ptashne M (1988) How eukaryotic transcriptional activators work. Nature 335:683–689

    Article  PubMed  CAS  Google Scholar 

  • Qu LJ, Zhu YX (2006) Transcription factor families in Arabidopsis: major progress and outstanding issues for future research. Curr Opin Plant Biol 9:544–549

    Article  PubMed  CAS  Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    Article  PubMed  CAS  Google Scholar 

  • Rudrabhatla P, Rajasekharan R (2002) Developmentally regulated dual-specificity kinase from peanut that is induced by abiotic stresses. Plant Physiol 130:380–390

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zinc finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Salamini F, Ozkan H, Brandolini A, Schäfer-Pregl R, Martin W (2002) Genetics and geography of wild cereal domestication in the near east. Nat Rev Genet 3:429–441

    PubMed  CAS  Google Scholar 

  • Schumann U, Prestele J, O’Geen H, Brueggeman R, Wanner G, Gietl C (2007) Requirement of the C3HC4 zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts. Proc Natl Acad Sci U S A 104:1069–1074

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Seydoux G, Mello CC, Pettitt J, Wood WB, Priess JR, Fire A (1996) Repression of gene expression in the embryonic germ lineage of C. elegans. Nature 382:713–716

    Article  PubMed  CAS  Google Scholar 

  • Simpson RJ, Yi Lee SH, Bartle N, Sum EY, Visvader JE, Matthews JM, Mackay JP, Crossley M (2004) A classic zinc finger from friend of GATA mediates an interaction with the coiled-coil of transforming acidic coiled-coil 3. J Biol Chem 279:39789–39797

    Article  PubMed  CAS  Google Scholar 

  • Sun J, Jiang H, Xu Y, Li H, Wu X, Xie Q, Li C (2007) The CCCH-type zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. Plant Cell Physiol 48:1148–1158

    Article  PubMed  CAS  Google Scholar 

  • Takatsuji H (1998) Zinc-finger transcription factors in plants. Cell Mol Life Sci 54:582–596

    Article  PubMed  CAS  Google Scholar 

  • Taylor GA, Lai WS, Oakey RJ, Seldin MF, Shows TB, Eddy RL Jr, Blackshear PJ (1991) The human TTP protein: sequence, alignment with related proteins, and chromosomal localization of the mouse and human genes. Nucleic Acids Res 19:3454

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tenenhaus C, Subramaniam K, Dunn MA, Seydoux G (2001) PIE-1 is a bifunctional protein that regulates maternal and zygotic gene expression in the embryonic germ line of Caenorhabditis elegans. Genes Dev 15:1031–1040

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Thompson MJ, Lai WS, Taylor GA, Blackshear PJ (1996) Cloning and characterization of two yeast genes encoding members of the CCCH class of zinc finger proteins: zinc finger-mediated impairment of cell growth. Gene 174:225–233

    Article  PubMed  CAS  Google Scholar 

  • Toppo S, Vanin S, Bosello V, Tosatto SC (2008) Evolutionary and structural insights into the multifaceted glutathione peroxidase (Gpx) superfamily. Antioxid Redox Signal 10:1501–1514

    Article  PubMed  CAS  Google Scholar 

  • Varnum BC, Ma QF, Chi TH, Fletcher B, Herschman HR (1991) The TISll primary response gene is a member of a gene family that encodes proteins with a highly conserved sequence containing an unusual Cys–His repeat. Mol Cell Biol 11:1754–1758

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wang D, Guo Y, Wu C, Yang G, Li Y, Zheng C (2008a) Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice. BMC Genomics 27:9–44

    Google Scholar 

  • Wang L, Xu Y, Zhang C, Ma Q, Joo SH, Kim SK, Xu Z, Chong K (2008b) OsLIC, a novel CCCH-type zinc finger protein with transcription activation, mediates rice architecture via brassinosteroid signaling. PLoS One 3:e3521

    Article  PubMed  PubMed Central  Google Scholar 

  • Wei PC, Tan F, Gao XQ, Zhang XQ, Wang GQ, Xu H, Li LJ, Chen J, Wang XC (2010) Overexpression of AtDOF4.7, an Arabidopsis DOF family transcription factor, induces floral organ abscission deficiency in Arabidopsis. Plant Physiol 153:1031–1045

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Xu ZS, Chen M, Li LC, Ma YZ (2008a) Functions of the ERF transcription factor family in plants. Botany 86:969–977

    Article  CAS  Google Scholar 

  • Xu ZS, Ni ZY, Liu L, Nie LN, Li LC, Chen M, Ma YZ (2008b) Characterization of the TaAIDFa gene encoding a CRT/DRE-binding factor responsive to drought, high-salt, and cold stress in wheat. Mol Genet Genomics 280:497–508

    Article  PubMed  CAS  Google Scholar 

  • Xu ZS, Chen M, Li LC, Ma YZ (2011) Functions and application of the AP2/ERF transcription factor family in crop improvement. J Integr Plant Biol 53:570–585

    Article  PubMed  CAS  Google Scholar 

  • Yanagisawa S (1997) Dof DNA-binding domains of plant transcription factors contribute to multiple protein–protein interactions. Eur J Biochem 250:403–410

    Article  PubMed  CAS  Google Scholar 

  • Yang XD, Dong CJ, Liu JY (2006) A plant mitochondrial phospholipid hydroperoxide glutathione peroxidase: its precise localization and higher enzymatic activity. Plant Mol Biol 62:951–962

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was financially supported by the National Natural Science Foundation of China (31371620) and the National Transgenic Key Project of MOA (2014ZX08009-016B). We are grateful to Dr. Jizeng Jia (Institute of Crop Science, Chinese Academy of Agricultural Sciences) for providing RNA-seq data of A. tauschii.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Zhao-Shi Xu or You-Zhi Ma.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1

Expression of C3H genes in various tissues or organs (XLSX 22 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, AL., Xu, ZS., Zhao, GY. et al. Genome-Wide Analysis of the C3H Zinc Finger Transcription Factor Family and Drought Responses of Members in Aegilops tauschii . Plant Mol Biol Rep 32, 1241–1256 (2014). https://doi.org/10.1007/s11105-014-0719-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-014-0719-z

Keywords

Navigation