Skip to main content
Log in

Genome-wide identification and expression profiling of ankyrin-repeat gene family in maize

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

Members of the ankyrin repeats (ANK) gene family encode ANK domain that are common in diverse organisms and play important roles in cell growth and development, such as cell-cell signal transduction and cell cycle regulation. Recently, genome-wide identification and evolutionary analyses of the ANK gene family have been carried out in Arabidopsis and rice. However, little is known regarding the ANK genes in the entire maize genome. In this study, we described the identification and structural characterization of 71 ANK genes in maize (ZmANK). Then, comprehensive bioinformatics analyses of ZmANK genes family were performed including phylogenetic, domain and motif analysis, chromosomal localization, intron/exon structural patterns, gene duplications and expression profiling. Domain composition analyses showed that ZmANK genes formed ten subfamilies. Five tandem duplications and 14 segmental duplications were identified in ZmANK genes. Furthermore, we took comparative analysis of the total ANK gene family in Arabidopsis, rice and maize, ZmANKs were more closely paired with OsANKs than with AtANKs. At last, expression profile analyses were performed. Forty-one members of ZmANK genes held EST sequences records. Semi-quantitative expression and microarray data analysis of these 41 ZmANK genes demonstrated that ZmANK genes exhibit a various expression pattern, suggesting that functional diversification of ZmANK genes family. The results will present significant insights to explore ANK genes expression and function in future studies in maize.

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
Figure 7
Fig. 8

Similar content being viewed by others

References

  • AbuQamar S, Chen X, Dhawan R, Bluhm B, Salmeron J, Lam S, Dietrich RA, Mengiste T (2006) Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. Plant J 48:28–44

    Article  PubMed  CAS  Google Scholar 

  • Al-Khodor S, Price CT, Kalia A, Abu Kwaik Y (2010) Functional diversity of ankyrin repeats in microbial proteins. Trends Microbiol 18:132–139

    Article  PubMed  CAS  Google Scholar 

  • Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–373

    Article  PubMed  CAS  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 

  • Bennetzen JL, Chandler VL, Schnable P (2001) National Science Foundation-sponsored workshop report. Maize genome sequencing project. Plant Physiol 127:1572–1578

    Article  PubMed  CAS  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 

  • Breeden L, Nasmyth K (1987) Similarity between cell-cycle genes of budding yeast and fission yeast and the Notch gene of Drosophila. Nature 329:651–654

    Article  PubMed  CAS  Google Scholar 

  • Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63

    Article  PubMed  CAS  Google Scholar 

  • Chinenov Y, Schmidt T, Yang XY, Martin ME (1998) Identification of redox-sensitive cysteines in GA-binding protein-alpha that regulate DNA binding and heterodimerization. J Biol Chem 273:6203–6209

    Article  PubMed  CAS  Google Scholar 

  • Choi MS, Kim MC, Yoo JH, Moon BC, Koo SC, Park BO, Lee JH, Koo YD, Han HJ, Lee SY et al (2005) Isolation of a calmodulin-binding transcription factor from rice (Oryza sativa L). J Biol Chem 280:40820–40831

    Article  PubMed  CAS  Google Scholar 

  • Cunha SR, Mohler PJ (2009) Ankyrin protein networks in membrane formation and stabilization. J Cell Mol Med 13:4364–4376

    Article  PubMed  CAS  Google Scholar 

  • Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763

    Article  PubMed  CAS  Google Scholar 

  • Elmendorf HG, Rohrer SC, Khoury RS, Bouttenot RE, Nash TE (2005) Examination of a novel head-stalk protein family in Giardia lamblia characterised by the pairing of ankyrin repeats and coiled-coil domains. Int J Parasitol 35:1001–1011

    Article  PubMed  CAS  Google Scholar 

  • Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL et al (2008) The Pfam protein families database. Nucleic Acids Res 36:D281–288

    Article  PubMed  CAS  Google Scholar 

  • Gijsen HJ, Berthelot D, Zaja M, Brone B, Geuens I, Mercken M (2010) Analogues of morphanthridine and the tear gas dibenz[b, f][1,4]oxazepine (CR) as extremely potent activators of the human transient receptor potential ankyrin 1 (TRPA1) channel. J Med Chem 53:7011–7020

    Article  PubMed  CAS  Google Scholar 

  • Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan 29(8):1023–1026

    Article  PubMed  CAS  Google Scholar 

  • Guo J, Wu J, Ji Q, Wang C, Luo L, Yuan Y, Wang Y, Wang J (2008) Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. J Genet Genomics 35:105–118

    Article  PubMed  CAS  Google Scholar 

  • Gu Q, Ferrandiz C, Yanofsky MF, Martienssen R (1998) The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125:1509–1517

    PubMed  CAS  Google Scholar 

  • Hashemi SM, Hund TJ, Mohler PJ (2009) Cardiac ankyrins in health and disease. J Mol Cell Cardiol 47:203–209

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Zhao X, Yu H, Ouyang Y, Wang L, Zhang Q (2009) The ankyrin repeat gene family in rice: genome-wide identification, classification and expression profiling. Plant Mol Biol 71:207–226

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Kaur N, Garg R, Thakur JK, Tyagi AK, Khurana JP (2006) Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa). Funct Integr Genomics 6:47–59

    Article  PubMed  CAS  Google Scholar 

  • Leseberg CH, Li A, Kang H, Duvall M, Mao L (2006) Genome-wide analysis of the MADS-box gene family in Populus trichocarpa. Gene 378:84–94

    Article  PubMed  CAS  Google Scholar 

  • Li J, Mahajan A, Tsai MD (2006) Ankyrin repeat: a unique motif mediating protein–protein interactions. Biochemistry 45:15168–15178

    Article  PubMed  CAS  Google Scholar 

  • Lu H, Rate DN, Song JT, Greenberg JT (2003) ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell 15:2408–2420

    Article  PubMed  CAS  Google Scholar 

  • Lux SE, John KM, Bennett V (1990) Analysis of cDNA for human erythrocyte ankyrin indicates a repeated structure with homology to tissue-differentiation and cell-cycle control proteins. Nature 344:36–42

    Article  PubMed  CAS  Google Scholar 

  • Mahmood N, Moosa MM, Tamanna N, Sarker SK, Najnin RA, Alam SS (2012) In silico analysis reveals the presence of a large number of ankyrin repeat containing proteins in Ectocarpus siliculosus. Interdiscip Sci Comput Life Sci 4:291–295

    Article  CAS  Google Scholar 

  • Michaely P, Bennett V (1992) The ANK repeat: a ubiquitous motif involved in macromolecular recognition. Trends Cell Biol 2:127–129

    Article  PubMed  CAS  Google Scholar 

  • Miles MC, Janket ML, Wheeler ED, Chattopadhyay A, Majumder B, Dericco J, Schafer EA, Ayyavoo V (2005) Molecular and functional characterization of a novel splice variant of ANKHD1 that lacks the KH domain and its role in cell survival and apoptosis. FEBS J 272:4091–4102

    Article  PubMed  CAS  Google Scholar 

  • Mosavi LK, Cammett TJ, Desrosiers DC, Peng ZY (2004) The ankyrin repeat as molecular architecture for protein recognition. Protein Sci 13:1435–1448

    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  Google Scholar 

  • Nam J, Nei M (2005) Evolutionary change of the numbers of homeobox genes in bilateral animals. Mol Biol Evol 22:2386–2394

    Article  PubMed  CAS  Google Scholar 

  • Neilsen PM, Cheney KM, Li CW, Chen JD, Cawrse JE, Schulz RB, Powell JA, Kumar R, Callen DF (2008) Identification of ANKRD11 as a p53 coactivator. J Cell Sci 121:3541–3552

    Article  PubMed  CAS  Google Scholar 

  • Nodzon LA, Xu WH, Wang Y, Pi LY, Chakrabarty PK, Song WY (2004) The ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis. Plant J 40:996–1006

    Article  PubMed  CAS  Google Scholar 

  • Ohlrogge J, Benning C (2000) Unraveling plant metabolism by EST analysis. Curr Opin Plant Biol 3:224–228

    PubMed  CAS  Google Scholar 

  • Saeed AI, Sharov V, White J, Li J, Liang W et al (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34(2):374–378

    PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  PubMed  CAS  Google Scholar 

  • Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95:5857–5864

    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 

  • Sekhon RS, Lin H, Childs KL, Hansey CN, Buell CR, de Leon N, Kaeppler SM (2011) Genome-wide atlas of transcription during maize development. Plant J 66:553–63

    Article  PubMed  CAS  Google Scholar 

  • Shearer HL, Wang LP, DeLong C, Despres C, Fobert PR (2009) NPR1 enhances the DNA binding activity of the Arabidopsis bZIP transcription factor TGA7. Botany 87(6):561–570

    Article  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 

  • Terol J, Domingo C, Talon M (2006) The GH3 family in plants: genome wide analysis in rice and evolutionary history based on EST analysis. Gene 371:279–290

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, 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 

  • 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 

  • Yan JQ, Wang J, Zhang H (2002) An ankyrin repeat-containing protein plays a role in both disease resistance and antioxidation metabolism. Plant J 29:193–202

    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 

  • Yuan C, Li J, Mahajan A, Poi MJ, Byeon IJL, Tsai MDT (2004) Solution structure of the human oncogenic protein gankyrin containing seven ankyrin repeats and analysis of its structure-function relationship. Biochemistry 43:12152–12161

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Scheirer DC, Fowle WH, Goodman HM (1992) Expression of antisense or sense RNA of an ankyrin repeat-containing gene blocks chloroplast differentiation in Arabidopsis. Plant Cell 4:1575–1588

    PubMed  CAS  Google Scholar 

  • Zhang X, Li D, Zhang H, Wang X, Zheng Z, Song F (2010) Molecular characterization of rice OsBIANK1, encoding a plasma membrane-anchored ankyrin repeat protein, and its inducible expression in defense responses. Mol Biol Rep 37:653–660

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We extend our thanks to the reviewers for their careful reading and helpful comments on this manuscript. This work was supported by Natural Science Foundation of China (11075001) and Scientific and Technological Research Plan of Anhui (1206c0805032, KJ2011A110).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Haiyang Jiang or Suwen Zhu.

Additional information

Communicated by: Sureshkumar Balasubramanian

H. Jiang and Q. Wu contributed equally to this work

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

The primers list used in the semi-quantitative RT-PCR (DOC 65 kb)

Table S2

The expression fold change of 41 genes compared with the control by microarray analysis (XLS 12 kb)

Fig. S1

Distribution of conserved motifs in the ZmANK genes family. The name of each member on the left, while a scale bar at the bottom indicates the length of each motif. Different motifs are indicated with boxes of different colors numbered 1 to 20. The length and order of motifs represent the actual situation in each protein. Detailed information on the 20 motifs is given in Table 3 (JPEG 2.41 mb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiang, H., Wu, Q., Jin, J. et al. Genome-wide identification and expression profiling of ankyrin-repeat gene family in maize. Dev Genes Evol 223, 303–318 (2013). https://doi.org/10.1007/s00427-013-0447-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-013-0447-7

Keywords

Navigation