Skip to main content
SpringerLink
Log in

Genome-wide identification of C2H2 zinc-finger gene family in rice and their phylogeny and expression analysis

  • Published:
Plant Molecular Biology 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 a pathway. In this study, we provide a complete overview of the genes encoding C2H2 zinc-finger transcription factors in rice, describing the gene structure, gene expression, genome localization, and phylogenetic relationship of each member. The genome of Oryza sativa codes for 189 C2H2 zinc-finger transcription factors, which possess two main types of zinc-fingers (named C and Q). The Q-type zinc fingers contain a conserved motif, QALGGH, and are plant specific, whereas C type zinc fingers are found in other organisms as well. A genome-wide microarray based gene expression analysis involving 14 stages of vegetative and reproductive development along with 3 stress conditions has revealed that C2H2 gene family in indica rice could be involved during all the stages of reproductive development from panicle initiation till seed maturation. A total of 39 genes are up-regulated more than 2-fold, in comparison to vegetative stages, during reproductive development of rice, out of which 18 are specific to panicle development and 12 genes are seed-specific. Twenty-six genes have been found to be up-regulated during three abiotic stresses and of these, 14 genes express specifically during the stress conditions analyzed while 12 are also up-regulated during reproductive development, suggesting that some components of the stress response pathways are also involved in reproduction.

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
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

C2H2 :

Cysteine2/Histidine2

EAR:

ERF-associated amphiphillic repression

HMM:

Hidden Markov Model

KOME:

Knowledge-based Oryza Molecular biological Encyclopedia

MPSS:

Massively parallel signature sequencing

NCBI:

National Center for Biotechnology Information

NJ:

Neighbour-joining

TIGR:

The Institute for Genomic Research

ZF:

Zinc-finger

ZFP:

Zinc-finger protein

ZPT:

C2H2 zinc-finger protein TFIIIA type

References

  • Black DL (1998) Splicing in the inner ear: a familiar tune, but what are the instruments? Neuron 20:165–168

    Article  PubMed  CAS  Google Scholar 

  • Blencowe BJ (2006) Alternative splicing: new insights from global analyses. Cell 126:37–47

    Article  PubMed  CAS  Google Scholar 

  • Blodner C, Goebel C, Feussner I, Gatz C, Polle A (2007) Warm and cold parental reproductive environments affect seed properties, fitness, and cold responsiveness in Arabidopsis thaliana progenies. Plant Cell Environ 30:165–175

    Article  PubMed  CAS  Google Scholar 

  • Bohm S, Frishman D, Mewes HW (1997) Variations of the C2H2 zinc finger motif in the yeast genome and classification of yeast zinc finger proteins. Nucleic Acids Res 25:2464–2469

    Article  PubMed  CAS  Google Scholar 

  • Bona E, Marsano F, Cavaletto M, Berta G (2007) Proteomic characterization of copper stress response in Cannabis sativa roots. Proteomics 7:1121–1130

    Article  PubMed  CAS  Google Scholar 

  • Cahill K (2004) Alternative splicing and genomic stability. Phys Biol 1:C1–C4

    Article  PubMed  CAS  Google Scholar 

  • Cooke HJ (2004) Silence of the centromeres—not. Trends Biotechnol 22:319–321

    Article  PubMed  CAS  Google Scholar 

  • Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139:847–856

    Article  PubMed  CAS  Google Scholar 

  • Dinkins R, Pflipsen C, Thompson A, Collins GB (2002) Ectopic expression of an Arabidopsis single zinc finger gene in tobacco results in dwarf plants. Plant Cell Physiol 43:743–750

    Article  PubMed  CAS  Google Scholar 

  • Dinneny JR, Weigel D, Yanofsky MF (2006) NUBBIN and JAGGED define stamen and carpel shape in Arabidopsis. Development 133:1645–1655

    Article  PubMed  CAS  Google Scholar 

  • Englbrecht CC, Schoof H, Bohm S (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5:39

    Article  PubMed  CAS  Google Scholar 

  • Florea L, Hartzell G, Zhang Z, Rubin GM, Miller W (1998) A computer program for aligning a cDNA sequence with a genomic DNA sequence. Genome Res 8:967–974

    PubMed  CAS  Google Scholar 

  • Gamsjaeger R, Liew CK, Loughlin FE, Crossley M, Mackay JP (2007) Sticky fingers: zinc-fingers as protein-recognition motifs. Trends Biochem Sci doi:10.1016/j.tibs.2006.1012.1007

  • Gibson CW, Thomson NH, Abrams WR, Kirkham J (2005) Nested genes: biological implications and use of AFM for analysis. Gene 350:15–23

    Article  PubMed  CAS  Google Scholar 

  • Grigg SP, Canales C, Hay A, Tsiantis M (2005) SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis. Nature 437:1022–1026

    Article  PubMed  CAS  Google Scholar 

  • Haas BJ, Delcher AL, Wortman JR, Salzberg SL (2004) DAGchainer: a tool for mining segmental genome duplications and synteny. Bioinformatics 20:3643–3646

    Article  PubMed  CAS  Google Scholar 

  • Hiratsu K, Mitsuda N, Matsui K, Ohme-Takagi M (2004) Identification of the minimal repression domain of SUPERMAN shows that the DLELRL hexapeptide is both necessary and sufficient for repression of transcription in Arabidopsis. Biochem Biophys Res Commun 321:172–178

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Wang J, Zhang H (2005) Rice ZFP15 gene encoding for a novel C2H2-type zinc finger protein lacking DLN box, is regulated by spike development but not by abiotic stresses. Mol Biol Rep 32:177–183

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Wang JF, Wang QH, Zhang HS (2005) Identification of a rice zinc finger protein whose expression is transiently induced by drought, cold but not by salinity and abscisic acid. DNA Seq 16:130–136

    Article  PubMed  CAS  Google Scholar 

  • Hulo N, Bairoch A, Bulliard V, Cerutti L, De Castro E, Langendijk-Genevaux PS, Pagni M, Sigrist CJ (2006) The PROSITE database. Nucleic Acids Res 34:D227–230

    Article  PubMed  CAS  Google Scholar 

  • Iuchi S (2001) Three classes of C2H2 zinc finger proteins. Cell Mol Life Sci 58:625–635

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice: genome-wide analysis, classification and spatial and temporal gene expression during panicle and seed development and regulation by light and abiotic stress. Plant Physiol 143:1467–1483

    Article  PubMed  CAS  Google Scholar 

  • Jeong YM, Mun JH, Lee I, Woo JC, Hong CB, Kim SG (2006) Distinct roles of the first introns on the expression of Arabidopsis profilin gene family members. Plant Physiol 140:196–209

    Article  PubMed  CAS  Google Scholar 

  • Kapoor S, Kobayashi A, Takatsuji H (2002) Silencing of the tapetum-specific zinc finger gene TAZ1 causes premature degeneration of tapetum and pollen abortion in petunia. Plant Cell 14:2353–2367

    Article  PubMed  CAS  Google Scholar 

  • Kapoor S, Takatsuji H (2006) Silencing of an anther-specific zinc-finger gene, MEZ1, causes aberrant meiosis and pollen abortion in petunia. Plant Mol Biol 61:415–430

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi S, Satoh K, Nagata T, Kawagashira N, Doi K, Kishimoto N, Yazaki J, Ishikawa M, Yamada H, Ooka H, Hotta I, Kojima K, Namiki T, Ohneda E, Yahagi W, Suzuki K, Li CJ, Ohtsuki K, Shishiki T, Otomo Y, Murakami K, Iida Y, Sugano S, Fujimura T, Suzuki Y, Tsunoda Y, Kurosaki T, Kodama T, Masuda H, Kobayashi M, Xie Q, Lu M, Narikawa R, Sugiyama A, Mizuno K, Yokomizo S, Niikura J, Ikeda R, Ishibiki J, Kawamata M, Yoshimura A, Miura J, Kusumegi T, Oka M, Ryu R, Ueda M, Matsubara K, Kawai J, Carninci P, Adachi J, Aizawa K, Arakawa T, Fukuda S, Hara A, Hashizume W, Hayatsu N, Imotani K, Ishii Y, Itoh M, Kagawa I, Kondo S, Konno H, Miyazaki A, Osato N, Ota Y, Saito R, Sasaki D, Sato K, Shibata K, Shinagawa A, Shiraki T, Yoshino M, Hayashizaki Y, Yasunishi A (2003) Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301:376–379

    Article  PubMed  Google Scholar 

  • Kim JC, Jeong JC, Park HC, Yoo JH, Koo YD, Yoon HW, Koo SC, Lee SH, Bahk JD, Cho MJ (2001) Cold accumulation of SCOF-1 transcripts is associated with transcriptional activation and mRNA stability. Mol Cells 12:204–208

    PubMed  CAS  Google Scholar 

  • Kim JC, Lee SH, Cheong YH, Yoo CM, Lee SI, Chun HJ, Yun DJ, Hong JC, Lee SY, Lim CO, Cho MJ (2001) A novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants. Plant J 25:247–259

    Article  PubMed  CAS  Google Scholar 

  • Klug A, Schwabe JW (1995) Protein motifs 5. Zinc fingers. FASEB J 9:597–604

    PubMed  CAS  Google Scholar 

  • Kobayashi A, Sakamoto A, Kubo K, Rybka Z, Kanno Y, Takatsuji H (1998) Seven zinc-finger transcription factors are expressed sequentially during the development of anthers in petunia. Plant J 13:571–576

    Article  PubMed  CAS  Google Scholar 

  • Kozaki A, Hake S, Colasanti J (2004) The maize ID1 flowering time regulator is a zinc finger protein with novel DNA binding properties. Nucleic Acids Res 32:1710–1720

    Article  PubMed  CAS  Google Scholar 

  • Kubo K, Sakamoto A, Kobayashi A, Rybka Z, Kanno Y, Nakagawa H, Takatsuji H (1998) Cys2/His2 zinc-finger protein family of petunia: evolution and general mechanism of target-sequence recognition. Nucleic Acids Res 26:608–615

    Article  PubMed  CAS  Google Scholar 

  • Le Hir H, Nott A, Moore MJ (2003) How introns influence and enhance eukaryotic gene expression. Trends Biochem Sci 28:215–220

    Article  PubMed  CAS  Google Scholar 

  • Li K, Yang J, Liu J, Du X, Wei C, Su W, He G, Zhang Q, Hong F, Qian X (2006) Cloning, characterization and tissue-specific expression of a cDNA encoding a novel EMBRYONIC FLOWER 2 gene (OsEMF2) in Oryza sativa. DNA Seq 17:74–78

    PubMed  CAS  Google Scholar 

  • Lippuner V, Cyert MS, Gasser CS (1996) Two classes of plant cDNA clones differentially complement yeast calcineurin mutants and increase salt tolerance of wild-type yeast. J Biol Chem 271:12859–12866

    Article  PubMed  CAS  Google Scholar 

  • Lorkovic ZJ, Wieczorek Kirk DA, Lambermon MH, Filipowicz W (2000) Pre-mRNA splicing in higher plants. Trends Plant Sci 5:160–167

    Article  PubMed  CAS  Google Scholar 

  • Lucyshyn D, Busch BL, Abolmaali S, Steiner B, Chandler E, Sanjarian F, Mousavi A, Nicholson P, Buerstmayr H, Adam G (2007) Cloning and characterization of the ribosomal protein L3 (RPL3) gene family from Triticum aestivum. Mol Genet Genomics doi:10.1007/s00438-00006-00201-00431

  • Luo M, Bilodeau P, Koltunow A, Dennis ES, Peacock WJ, Chaudhury AM (1999) Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:296–301

    Article  CAS  Google Scholar 

  • Macknight R, Duroux M, Laurie R, Dijkwel P, Simpson G, Dean C (2002) Functional significance of the alternative transcript processing of the Arabidopsis floral promoter FCA. Plant Cell 14:877–888

    Article  PubMed  CAS  Google Scholar 

  • Meissner R, Michael AJ (1997) Isolation and characterisation of a diverse family of Arabidopsis two and three-fingered C2H2 zinc finger protein genes and cDNAs. Plant Mol Biol 33:615–624

    Article  PubMed  CAS  Google Scholar 

  • Nagaki K, Cheng Z, Ouyang S, Talbert PB, Kim M, Jones KM, Henikoff S, Buell CR, Jiang J (2004) Sequencing of a rice centromere uncovers active genes. Nat Genet 36:138–145

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa H, Jiang CJ, Sakakibara H, Kojima M, Honda I, Ajisaka H, Nishijima T, Koshioka M, Homma T, Mander LN, Takatsuji H (2005) Overexpression of a petunia zinc-finger gene alters cytokinin metabolism and plant forms. Plant J 41:512–523

    Article  PubMed  CAS  Google Scholar 

  • Ohta M, Matsui K, Hiratsu K, Shinshi H, Ohme-Takagi M (2001) Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13:1959–1968

    Article  PubMed  CAS  Google Scholar 

  • Pruitt KD, Tatusova T, Maglott DR (2005) NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 33:D501–504

    Article  PubMed  CAS  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:W116–120

    Article  PubMed  CAS  Google Scholar 

  • Reddy ASN (2001) Nuclear pre-mRNA splicing in plants. Critical Reviews in Plant Sciences 20:523–571

    Article  CAS  Google Scholar 

  • Rose AB (2002) Requirements for intron-mediated enhancement of gene expression in Arabidopsis. RNA 8:1444–1453

    Article  PubMed  CAS  Google Scholar 

  • Runkel F, Michels M, Franz T (2003) Fxyd3 and Lgi4 expression in the adult mouse: a case of endogenous antisense expression. Mamm Genome 14:665–672

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto H, Araki T, Meshi T, Iwabuchi M (2000) Expression of a subset of the Arabidopsis Cys2/His2-type zinc-finger protein gene family under water stress. Gene 248:23–32

    Article  PubMed  CAS  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  Google Scholar 

  • Schuh R, Aicher W, Gaul U, Cote S, Preiss A, Maier D, Seifert E, Nauber U, Schroder C, Kemler R, et al. (1986) A conserved family of nuclear proteins containing structural elements of the finger protein encoded by Krüppel, a Drosophila segmentation gene. Cell 47:1025–1032

    Article  PubMed  CAS  Google Scholar 

  • Schwarz Z, Jolly SO, Steinmetz AA, Bogorad L (1981) Overlapping divergent genes in the maize chloroplast chromosome and in vitro transcription of the gene for tRNA His. Proc Natl Acad Sci USA 78:3423–3427

    Article  PubMed  CAS  Google Scholar 

  • Shao H, Zhu C, Zhao Z, Guo M, Qiu H, Liu H, Wang D, Xue L, Gao L, Sun C, Li W (2006) KRAB-containing zinc finger gene ZNF268 encodes multiple alternatively spliced isoforms that contain transcription regulatory domains. Int J Mol Med 18:457–463

    PubMed  CAS  Google Scholar 

  • Sharp PA (1994) Split genes and RNA splicing. Cell 77:805–815

    Article  PubMed  CAS  Google Scholar 

  • Singh G, Kumar S, Singh P (2003) A quick method to isolate RNA from wheat and other carbohydrate-rich seeds. Plant Mol Biol Rep 21:93a-f

    Article  Google Scholar 

  • Smith CW, Valcarcel J (2000) Alternative pre-mRNA splicing: the logic of combinatorial control. Trends Biochem Sci 25:381–388

    Article  PubMed  CAS  Google Scholar 

  • Sugano S, Kaminaka H, Rybka Z, Catala R, Salinas J, Matsui K, Ohme-Takagi M, Takatsuji H (2003) Stress-responsive zinc finger gene ZPT2–3 plays a role in drought tolerance in petunia. Plant J 36:830–841

    Article  PubMed  CAS  Google Scholar 

  • Takatsuji H, Mori M, Benfey PN, Ren L, Chua NH (1992) Characterization of a zinc finger DNA-binding protein expressed specifically in petunia petals and seedlings. EMBO J 11:241–249

    PubMed  CAS  Google Scholar 

  • Takatsuji H, Nakamura N, Katsumoto Y (1994) A new family of zinc finger proteins in petunia: structure, DNA sequence recognition, and floral organ-specific expression. Plant Cell 6:947–958

    Article  PubMed  CAS  Google Scholar 

  • Takatsuji H, Matsumoto T (1996) Target-sequence recognition by separate-type Cys2/His2 zinc finger proteins in plants. J Biol Chem 271:23368–23373

    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 

  • Takatsuji H (1999) Zinc-finger proteins: the classical zinc finger emerges in contemporary plant science. Plant Mol Biol 39:1073–1078

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wang BB, Brendel V (2006) Genomewide comparative analysis of alternative splicing in plants. Proc Natl Acad Sci USA 103:7175–7180

    Article  PubMed  CAS  Google Scholar 

  • Werneke JM, Chatfield JM, Ogren WL (1989) Alternative mRNA splicing generates the two ribulosebisphosphate carboxylase/oxygenase activase polypeptides in spinach and Arabidopsis. Plant Cell 1:815–825

    Article  PubMed  CAS  Google Scholar 

  • Worch S, Fiedler E, Hansmann I, Schlote D (2006) Genomic organization and expression pattern of scapinin (PHACTR3) in mouse and human. Cytogenet Genome Res 115:23–29

    Article  PubMed  CAS  Google Scholar 

  • Wu Z, Irizarry RA, Gentleman R, Murillo FM, Spencer F 2003: A Model Based Background Adjustment for Oligonucleotide Expression Arrays. Technical Report, Department of Biostatistics Working Papers, Baltimore, MD

  • Xu Y, Ma QH (2004) Medicago truncatula Mt-ZFP1 encoding a root enhanced zinc finger protein is regulated by cytokinin, abscisic acid and jasmonate, but not cold. DNA Seq 15:104–109

    PubMed  CAS  Google Scholar 

  • Yang L, Liu Z, Lu F, Dong A, Huang H (2006) SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J 47:841–850

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The research work was supported by the Department of Biotechnology, Government of India. UGC Research Fellowship to P.A. and CSIR Research Fellowship to R.A. and S.R. are acknowledged.

Author information

Authors and Affiliations

  1. Interdisciplinary Centre for Plant Genomics and Department of Plant Molecular Biology, University of Delhi South Campus, Benito Juarez Road, New Delhi, 110021, India

    Pinky Agarwal, Rita Arora, Swatismita Ray, Sanjay Kapoor & Akhilesh K. Tyagi

  2. Division of Genetics, Indian Agricultural Research Institute, New Delhi, 110012, India

    Ashok K. Singh & Vijay P. Singh

  3. Plant Disease Resistance Research Unit, National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, 305-8602, Ibaraki, Japan

    Hiroshi Takatsuji

Authors
  1. Pinky Agarwal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rita Arora
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Swatismita Ray
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ashok K. Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vijay P. Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hiroshi Takatsuji
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sanjay Kapoor
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Akhilesh K. Tyagi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Akhilesh K. Tyagi.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Agarwal, P., Arora, R., Ray, S. et al. Genome-wide identification of C2H2 zinc-finger gene family in rice and their phylogeny and expression analysis. Plant Mol Biol 65, 467–485 (2007). https://doi.org/10.1007/s11103-007-9199-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-007-9199-y

Keywords

Search

Navigation