Abstract
Key message
In this study, we identified 34 CCCH Znf genes in Medicago truncatula and the results of semi-quantitative RT-PCR revealed that the expression patterns of subfamily VI members were diverse.
Abstract
CCCH-type zinc finger (Znf) proteins are specific transcriptional factors with a typical motif consisting of three cysteine residues and one histidine residue. Increasing evidences have revealed that CCCH Znf proteins participated in the regulation of plant growth, developmental processes and environmental responses. Survey and characterization of CCCH Znf genes in leguminous species would facilitate a better understanding of the evolutionary processes and functions of this gene family. In this study, we performed a comprehensive analysis of CCCH Znf genes in M. truncatula by describing the phylogenetic relationships, chromosomal location and gene structure of each family member. A total of 34 CCCH Znf genes were identified in the latest M. truncatula genome sequence. The 34 predicted members were clustered into nine subfamilies based on their phylogenetic analysis and structure features. In addition, the 34 Medicago CCCH Znf genes were found to be unevenly distributed on eight chromosomes. Furthermore, the expression profiles of subfamily VI were investigated under different stress conditions (PEG-6000, NaCl and ABA) by using semi-quantitative RT-PCR. The data showed that these genes displayed different expression levels in response to various stress conditions. The results presented in this study provide basic information about Medicago CCCH Znf genes and form a fundamental clue for cloning genes with specific functions in further studies and applications.
Similar content being viewed by others
References
Arnaud D, Dejardin A, Leple JC, Lesage-Descauses MC, Pilate G (2007) Genome-wide analysis of LIM gene family in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa. DNA Res 14:103–116
Becerra C, Jahrmann T, Puigdomenech P, Vicient CM (2004) Ankyrin repeat-containing proteins in Arabidopsis: characterization of a novel and abundant group of genes coding ankyrin-transmembrane proteins. Gene 340:111–121
Berg JM, Shi Y (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science 271:1081–1085
Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10
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
Chai GH, Hu RB, Zhang DY et al (2012) Comprehensive analysis of CCCH zinc finger family in poplar (Populus trichocarpa). BMC Genomics 13:253
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
Gao G, Guo X, Goff SP (2002) Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein. Science 297:1703–1706
Grabowskaa A, Wisniewskab A, Tagashirac N, Malepszyd S, Filipeckid M (2009) Characterization of CsSEF1 gene encoding putative CCCH-type zinc finger protein expressed during cucumber somatic embryogenesis. J Plant Physiol 166:310–323
Gu Z, Cavalcanti A, Chen FC, Bouman P, Li WH (2002) Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol Biol Evol 19:256–262
Guo YH, Yu YP, Wang D, Wu CA, Yang GD et al (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
Hall TM (2005) Multiple modes of RNA recognition by zinc finger proteins. Curr Opin Struct Biol 15:367–373
Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2:516–527
Hudson BP, Martinez-Yamout MA, Dyson HJ, Wright PE (2004) Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d. Nat Struct Mol Biol 11:257–264
Khurana P, Gaikwad K (2005) The map-based sequence of the rice genome. Nature 436:793–800
Kim DH, Yamaguchi S, Lim S, Oh E, Park J, Hanada A, Kamiya Y, Choia 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
Ko JH, Kim WC, Han KH (2009) Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis. Plant J 60:649–665
Kolkman JA, Stemmer WP (2001) Directed evolution of proteins by exon shuffling. Nat Biotechnol 19:423–428
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(4):1376–1388
Kosarev P, Mayer KF, Hardtke CS (2002) Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome. Genome Biol 3:research0016.0011–research0016.0012
Kramer S, Kimblin NC, Carrington M (2010) Genome-wide in silico screen for CCCH-type zinc finger proteins of Trypanosoma brucei, Trypanosoma cruzi and Leishmania major. BMC Genomics 11:283
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
Lai WS, Carballo E, Thorn JM, Kennington EA, Blackshear PJ (2000) Interactions of CCCH zinc finger proteins with mRNA. Binding of tristetraprolin-related zinc finger proteins to Au-rich elements and destabilization of mRNA. J Biol Chem 275:17827–17837
Lai WS, Kennington EA, Blackshear PJ (2003) Tristetraprolin and its family members can promote the cell-free deadenylation of AU-rich element-containing mRNAs by poly (A) ribonuclease. Mol Cell Biol 23:3798–3812
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
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
Lorkovic ZJ, Barta A (2002) Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res 30:623–635
Lunde BM, Moore C, Varani G (2007) RNA-binding proteins: modular design for efficient function. Nat Rev Mol Cell Biol 8:479–490
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
Mosavi LK, Minor DL Jr, Peng ZY (2002) Consensus-derived structural determinants of the ankyrin repeat motif. Proc Natl Acad Sci 99:16029–16034
Ogura K, Kishimoto N, Mitani S, Gengyo-Ando K, Kohara Y (2003) Translational control of maternal glp-1 mRNA by POS-1 and its interacting protein SPN-4 in Caenorhabditis elegans. Development 130:2495–2503
Peng XJ, Zhao Y, Cheng BJ et al (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
Ramos SB, Stumpo DJ, Kennington EA, Phillips RS, Bock CB, Ribeiro-Neto F, Blackshear PJ (2004) The CCCH tandem zinc-finger protein Zfp36l2 is crucial for female fertility and early embryonic development. Development 131:4883–4893
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
Schultz J, Copley RR, Doerks T, Ponting CP, Bork P (2000) SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res 28:231–234
Sonnhammer EL, Eddy SR, Durbin R (1997) Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 28:405–420
Sun JQ, Jiang HL, Xu YX, Li HM, Wu XY, Xie Q, Li CY (2007) The CCCH-type zinc finger proteins ATSZF1 and ATSZF2 regulate salt stress responses in Arabidopsis. Plant Cell Physiol 48:1148–1158
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
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
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
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Vision TJ, Brown DG, Tanksley SD (2000) The origins of genomic duplications in Arabidopsis. Science 290:2114–2117
Wang D, Guo YH, Wu CG, Yang GD, Li YY, Zheng CC (2008a) Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice. BMC Genomics 9:44
Wang L, Xu YY, Zhang C, Ma QB, Joo SH, Kim SK, Xu ZH, Chong K (2008b) OsLIC, a novel CCCH-type zinc finger protein with transcription activation, mediates rice architecture via brassinosteroids signaling. PLoS One 3:e3521
Wang HZ, Avcib U, Nakashimaa J, Hahn MG, Chen F, Dixona RA (2010) Mutation of WRKY transcription factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants. Proc Natl Acad Sci 21:22338–22343
Wei F, Coe E, Nelson W, Bharti AK, Engler F et al (2007) Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet 3:e123
Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2009) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149:981–993
Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, Rockman MV, Romano LA (2003) The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 20:1377–1419
Yanagisawa S (2004) Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants. Plant Cell Physiol 45:386–391
Yang S, Zhang X, Yue JX, Tian D, Chen JQ (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genom 280:187–198
Zhang Y, Wang L (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5:1. doi:10.1186/1471-2148-1185-1181
Acknowledgments
This work was supported by grants from the National Science Technology Support Program (No. 2009BADA6B06-1). We thank the members of the Laboratory of Modern Biotechnology for their assistance. We especially thank Guo Wei and Yuanhua Shao for their support and comments during the preparation of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Q. Zhao.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, C., Zhang, H., Zhao, Y. et al. Genome-wide analysis of the CCCH zinc finger gene family in Medicago truncatula . Plant Cell Rep 32, 1543–1555 (2013). https://doi.org/10.1007/s00299-013-1466-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-013-1466-6