Skip to main content
SpringerLink
Log in

Comprehensive analysis of CCCH-type zinc finger gene family in citrus (Clementine mandarin) by genome-wide characterization

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The CCCH-type zinc finger proteins comprise a large gene family of regulatory proteins and are widely distributed in eukaryotic organisms. The CCCH proteins have been implicated in multiple biological processes and environmental responses in plants. Little information is available, however, about CCCH genes in plants, especially in woody plants such as citrus. The release of the whole-genome sequence of citrus allowed us to perform a genome-wide analysis of CCCH genes and to compare the identified proteins with their orthologs in model plants. In this study, 62 CCCH genes and a total of 132 CCCH motifs were identified, and a comprehensive analysis including the chromosomal locations, phylogenetic relationships, functional annotations, gene structures and conserved motifs was performed. Distribution mapping revealed that 54 of the 62 CCCH genes are unevenly dispersed on the nine citrus chromosomes. Based on phylogenetic analysis and gene structural features, we constructed 5 subfamilies of 62 CCCH members and integrative subfamilies from citrus, Arabidopsis, and rice, respectively. Importantly, large numbers of SNPs and InDels in 26 CCCH genes were identified from Poncirus trifoliata and Fortunella japonica using whole-genome deep re-sequencing. Furthermore, citrus CCCH genes showed distinct temporal and spatial expression patterns in different developmental processes and in response to various stress conditions. Our comprehensive analysis of CleC3Hs is a valuable resource that further elucidates the roles of CCCH family members in plant growth and development. In addition, variants and comparative genomics analyses deepen our understanding of the evolution of the CCCH gene family and will contribute to further genetics and genomics studies of citrus and other plant species.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adam SA, Nakagawa T, Swanson MS, Woodruff TK, Dreyfuss G (1986) mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence. Mol Cell Biol 6:2932–2943

    PubMed  CAS  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Baou M, Jewell A, Murphy JJ (2009) TIS11 family proteins and their roles in posttranscriptional gene regulation. J Biomed Biotechnol 2009:634520

    Article  PubMed  PubMed Central  Google Scholar 

  • Barreau C, Paillard L, Osborne HB (2005) AU-rich elements and associated factors are there unifying principles? Nucleic Acids Res 33:7138–7150

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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

    Article  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 

  • Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–1691

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bork P (1993) Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally? Proteins 17:363–374

    Article  PubMed  CAS  Google Scholar 

  • Brookes AJ (1999) The essence of SNPs. Gene 234:177–186

    Article  PubMed  CAS  Google Scholar 

  • Chai G, Hu R, Zhang D, Qi G, Zuo R, Cao Y, Chen P, Kong Y, Zhou G (2012) Comprehensive analysis of CCCH zinc finger family in poplar (Populus trichocarpa). BMC Genomics 13:253

    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 

  • Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer EL, Bateman A (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34:D247–D251

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gao G, Guo X, Goff SP (2002) Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein. Science 297:1703–1706

    Article  PubMed  CAS  Google Scholar 

  • Gmitter FG, Chen C, Machado MA, de Souza AA, Ollitrault P, Froehlicher Y, Shimizu T (2012) Citrus genomics. Tree Genet Genomes 8:611–626

    Article  Google Scholar 

  • Grabowska A, Wisniewska A, Tagashira N, Malepszy S, Filipecki M (2009) Characterization of CsSEF1 gene encoding putative CCCH-type zinc finger protein expressed during cucumber somatic embryogenesis. J Plant Physiol 166:310–323

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Guo A, Zhu Q, Chen X, Luo J (2007) GSDS: a gene structure display server. Yi Chuan 29:1023–1026

    Article  PubMed  CAS  Google Scholar 

  • Guo Y, Yu Y, Wang D, Wu C, Yang G, Huang J, Zheng C (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 

  • Hamon P, Seguin M, Perrier X, Glaszmann JC (2003) Genetic diversity of cultivated tropical plants. Cirad, Montpellier

    Google Scholar 

  • Han Y, Chagne D, Gasic K, Rikkerink EH, Beever JE, Gardiner SE, Korban SS (2009) BAC-end sequence-based SNPs and Bin mapping for rapid integration of physical and genetic maps in apple. Genomics 93:282–288

    Article  PubMed  CAS  Google Scholar 

  • Hou X, Liu S, Kan MRG, Hu C, Zhang J (2014) Genome-wide identification, classification, expression profiling, and SSR marker development of the MADS-Box Gene family in Citrus. Plant Mol Biol Rep 32:28–41

    Article  CAS  Google Scholar 

  • Hu R, Qi G, Kong Y, Kong D, Gao Q, Zhou G (2010) Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10:145

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  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 

  • Jiao Y, Wickett NJ, Ayyampalayan S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS, Soltis DE, Clifton SW, Schlarbaum SE, Schuster SC, Ma H, Leebeens-Mack J, dePamphilis CW (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100

    Article  PubMed  CAS  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 

  • 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

    Article  PubMed  CAS  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 

  • Kosarev P, Mayer KF, Hardtke CS (2002) Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome. Genome Biol 3:RESEARCH0016

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  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 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P (2004) SMART 4.0: towards genomic data integration. Nucleic Acids Res 32:D142–D144

    Article  PubMed  CAS  PubMed Central  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 

  • Liang J, Song W, Tromp G, Kolattukudy PE, Fu M (2008) Genome-wide survey and expression profiling of CCCH-zinc finger family reveals a functional module in macrophage activation. PLoS ONE 3:e2880

    Article  PubMed  PubMed Central  Google Scholar 

  • Lijavetzky D, Carbonero P, Vicente-Carbajosa J (2003) Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families. BMC Evol Biol 3:17

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu S, Li W, Long D, Hu C, Zhang J (2013) Development and characterization of genomic and expressed SSRs in Citrus by genome-wide analysis. PLoS ONE 8:e75149

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Moore RC, Purugganan MD (2003) The early stages of duplication gene evolution. Proc Natl Acad Sci USA 100:15682–15687

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nicolosi E, Deng ZN, Gentile A, Malfa S, Continella G, Tribulato E (2000) Citrus phylogeny and genetic origin of important species as investigated by molecular markers. Theor Appl Genet 100:1155–1166

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ollitrault P, Terol J, Garcia-Lor A, Berard A, Chauveau A, Froelicher Y, Belzile C, Morillon R, Navarro L, Brunel D, Talon M (2012) SNP mining in C. clementina BAC end sequences; transferability in the Citrus genus (Rutaceae), phylogenetic inferences and perspectives for genetic mapping. BMC Genomics 13:13

    Article  PubMed  CAS  PubMed Central  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 M, Hah C, Lin PC, Kang SG, Finer JJ, Blackshear PJ, Jang JC (2010a) 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  CAS  PubMed Central  Google Scholar 

  • Pomeranz M, Lin PC, Finer J, Jang JC (2010b) AtTZF gene family localizes to cytoplasmic foci. Plant Signal Behav 5:190–192

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33:W116–W120

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Rickert AM, Kim JH, Meyer S, Nagel A, Ballvora A, Oefner PJ, Gebhardt C (2003) First-generation SNP/InDel markers tagging loci for pathogen resistance in the potato genome. Plant Biotechnol J 1:399–410

    Article  PubMed  CAS  Google Scholar 

  • Salamov AA, Solovyev VV (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Res 10:516–522

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Schmid R, Blaxter ML (2008) annot8r: GO, EC and KEGG annotation of EST datasets. BMC Bioinform 9:180

    Article  Google Scholar 

  • Schmitz RJ, Hong L, Michaels S, Amasino RM (2005) FRIGIDA-ESSENTIAL 1 interacts genetically with FRIGIDA and FRIGIDALIKE 1 to promote the winter-annual habit of Arabidopsis thaliana. Development 132:5471–5478

    Article  PubMed  CAS  Google Scholar 

  • Sedgwick SG, Smerdon SJ (1999) The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci 24:311–316

    Article  PubMed  CAS  Google Scholar 

  • Song X, Huang Z, Duan W, Ren J, Liu T, Li Y, Hou X (2013) Genome-wide analysis of the bHLH transcription factor family in Chinese cabbage (Brassica rapa ssp. pekinensis). Mol Genet Genomics 289(1):77–91

    Article  PubMed  Google Scholar 

  • Stumpo DJ, Broxmeyer HE, Ward T, Cooper S, Hangoc G, Chung YJ, Shelley WC, Richfield EK, Ray MK, Yoder MC, Aplan PD, Blackshear PJ (2009) Targeted disruption of Zfp36l2, encoding a CCCH tandem zinc finger RNA-binding protein, results in defective hematopoiesis. Blood 114:2401–2410

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sun J, Jiang H, Xu Y, Li H, Wu X, Xie Q, Li Q (2007) The CCCH-type zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. Plant Cell Physiol 48(8):1148–1158

    Article  PubMed  CAS  Google Scholar 

  • Swanson MS, Nakagawa TY, LeVan K, Dreyfuss G (1987) Primary structure of human nuclear ribonucleoprotein particle C proteins: conservation of sequence and domain structures in heterogeneous nuclear RNA, mRNA, and pre-rRNA-binding proteins. Mol Cell Biol 7:1731–1739

    PubMed  CAS  PubMed Central  Google Scholar 

  • Swingle WT, Reece PC (1967) The botany of citrus and its wild relatives of the orange subfamily (family Rutaceae, subfamily Aurantioideae). University of California Press, Berkley

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Taylor JS, Raes J (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 38:615–643

    Article  PubMed  CAS  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 

  • Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  PubMed  CAS  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 9:44

    Article  PubMed  PubMed Central  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 rtholtion, mediates rice architecture via brassinosteroids signaling. PLoS ONE 3:e3521

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu Q, Chen LL, Ruan X et al (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59–66

    Article  PubMed  CAS  Google Scholar 

  • Yang S, Zhang X, Yue JX, Tian D, Chen JQ (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genomics 280:187–198

    Article  PubMed  CAS  Google Scholar 

  • Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298

    Article  Google Scholar 

  • Zhang Y, Wang L (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5:1

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang H, Jin J, Tang L, Zhao Y, Gu X, Gao G, Luo J (2011a) PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res 39:D1114–D1117

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang J, Ai X, Sun L, Zhang D, Guo W, Deng X, Hu C (2011b) Molecular cloning and functional characterization of genes associated with flowering in citrus using an early-flowering trifoliate orange (Poncirus trifoliata L. Raf.) mutant. Plant Mol Biol 76:187–204

    Article  PubMed  CAS  Google Scholar 

  • Zhang C, Zhang H, Zhao Y, Jiang H, Zhu S, Cheng B, Xiang Y (2013) Genome-wide analysis of the CCCH zinc finger gene family in Medicago truncatula. Plant Cell Rep 32:1543–1555

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We appreciate the editor and the reviewers for their constructive suggestions and comments. This research was supported financially by the National Natural Science Foundation of China (Grant Nos. 31130046, 31372046 and 31071777). We acknowledge the International Citrus Genome Consortium for using the Clementine genome sequences, and other institutions and organizations for providing the public release of genome sequences used in our investigation. We also appreciate Zhongchi Liu and Rachel Maczis Shahan for their support and comments during the preparation of this manuscript.

Author information

Authors and Affiliations

  1. Key Laboratory of Horticultural Plant Biology (Ministry of Education), College of Horticulture and Forestry Science, Huazhong Agricultural University, Wuhan, 430070, China

    Shengrui Liu, Muhammad Rehman Gul Khan, Yongping Li, Jinzhi Zhang & Chungen Hu

Authors
  1. Shengrui Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Muhammad Rehman Gul Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yongping Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jinzhi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chungen Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chungen Hu.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Source 1. Genomic, coding, and protein sequences and motif sequences of the 62 citrus CCCH genes.

Online Source 2. An overview phylogenetic tree of 62 full-length CCCH proteins from citrus Clementine was conducted by ClustalX2.1 and was constructed using MEGA4.0 with 1,000 bootstrap replicates. It was mainly divided into nine subfamilies and each subfamily is shown in different colors.

Online Source 3. GO terms for Citrus CCCH genes of biological process, molecular function, and cellular component. A. GO annotation of 61 CCCH genes for their biological process. B. Molecular functions predicted of 61 CCCH genes. C. Cellular component analysis of 61 CCCH genes. Different groups displayed on the left of annotations.

Online Source 4. The detailed information (length, position and e-value) of 16 identified conserved motifs.

Online Source 5. Sequence logos for the CCCH motifs of Citrus (A), Arabidopsis (B), Rice (C) and Populus (D). Numbers on the x-axis represent the sequence positions in CCCH motifs. The y-axis represents the information content measured in bits.

Online Source 6. Detailed information for gene-specific primers for the selected 24 genes and the β-actin internal reference gene for qRT-PCR.

Online Source 7. The Ct value and standard deviation of CleC3Hs genes under two stress conditions.

Supplementary material 1 (XLSX 147 kb)

Supplementary material 2 (JPEG 1092 kb)

Supplementary material 3 (JPEG 534 kb)

Supplementary material 4 (XLSX 19 kb)

Supplementary material 5 (JPEG 420 kb)

Supplementary material 6 (XLSX 14 kb)

Supplementary material 7 (XLSX 12 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, S., Khan, M.R.G., Li, Y. et al. Comprehensive analysis of CCCH-type zinc finger gene family in citrus (Clementine mandarin) by genome-wide characterization. Mol Genet Genomics 289, 855–872 (2014). https://doi.org/10.1007/s00438-014-0858-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-014-0858-9

Keywords

Search

Navigation