Abstract
C2H2 type of zinc finger transcription factors (TFs) play crucial roles in plant stress response and hormone signal transduction. Hence considering its importance, genome-wide investigation and characterization of C2H2 zinc finger proteins were performed in Arabidopsis, rice and poplar but no such study was conducted in foxtail millet which is a C4 Panicoid model crop well known for its abiotic stress tolerance. The present study identified 124 C2H2-type zinc finger TFs in foxtail millet (SiC2H2) and physically mapped them onto the genome. The gene duplication analysis revealed that SiC2H2s primarily expanded in the genome through tandem duplication. The phylogenetic tree classified these TFs into five groups (I–V). Further, miRNAs targeting SiC2H2 transcripts in foxtail millet were identified. Heat map demonstrated differential and tissue-specific expression patterns of these SiC2H2 genes. Comparative physical mapping between foxtail millet SiC2H2 genes and its orthologs of sorghum, maize and rice revealed the evolutionary relationships of C2H2 type of zinc finger TFs. The duplication and divergence data provided novel insight into the evolutionary aspects of these TFs in foxtail millet and related grass species. Expression profiling of candidate SiC2H2 genes in response to salinity, dehydration and cold stress showed differential expression pattern of these genes at different time points of stresses.
Similar content being viewed by others
References
Agarwal P, Arora R, Ray S, Singh AK, Singh VP, Takatsuji H, Kapoor S, Tyagi AK (2007) Genome-wide identification of C2H2 zinc-finger gene family in rice and their phylogeny and expression analysis. Plant Mol Biol 65:467–485
Bennetzen JL, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli AC, Estep M, Feng L, Vaughn JN, Grimwood J, Jenkins J, Barry K, Lindquist E, Hellsten U, Deshpande S, Wang X, Wu X, Mitros T, Triplett J, Yang X, Ye CY, Mauro-Herrera M, Wang L, Li P, Sharma M, Sharma R, Ronald PC, Panaud O, Kellogg EA, Brutnell TP, Doust AN, Tuskan GA, Rokhsar D, Devos KM (2012) Reference genome sequence of the model plant Setaria. Nat Biotechnol 30:555–561
Bjellqvist B, Hughes GJ, Pasquali C, Paquet N, Ravier F, Sanchez J-C, Frutiger S, Hochstrasser DF (1993) The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis 14:1023–1031
Cochrane G, Alako B, Amid C, Bower L, Cerdeño-Tárraga A, Cleland I, Gibson R, Goodgame N, Jang M, Kay S, Leinonen R, Lin X, Lopez R, McWilliam H, Oisel A, Pakseresht N, Pallreddy S, Park Y, Plaister S, Radhakrishnan R, Rivière S, Rossello M, Senf A, Silvester N, Smirnov D, Ten Hoopen P, Toribio A, Vaughan D, Zalunin V (2013) Facing growth in the European Nucleotide Archive. Nucleic Acids Res 41:D30–35
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676
Doust AN, Kellogg EA, Devos KM, Bennetzen JL (2009) Foxtail millet: a sequence-driven grass model system. Plant Physiol 149:137–141
Du D, Zhang Q, Cheng T, Pan H, Yang W, Sun L (2012) Genome-wide identification and analysis of late embryogenesis abundant (LEA) genes in Prunus mume. Mol Biol Rep 40:1937–1946
Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763
Englbrecht CC, Schoof H, Böhm S (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5:39
Gourcilleau D, Lenne C, Armenise C, Moulia B, Julien JL, Bronner G, Leblanc-Fournier N (2011) Phylogenetic study of plant Q-type C2H2 zinc finger proteins and expression analysis of poplar genes in response to osmotic, cold and mechanical stresses. DNA Res 18:77–92
Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan 29:1023–1026
Gupta S, Kumari K, Muthamilarasan M, Parida SK, Prasad M (2014) Population structure and association mapping of yield contributing agronomic traits in foxtail millet. Plant Cell Rep. doi:10.1007/s00299-014-1564-0
Jain M, Khurana P, Tyagi AK, Khurana JP (2008) Genome-wide analysis of intronless genes in rice and Arabidopsis. Funct Integr Genomics 8:69–78
Jia G, Huang X, Zhi H, Zhao Y, Zhao Q, Li W, Chai Y, Yang L, Liu K, Lu H, Zhu C, Lu Y, Zhou C, Fan D, Weng Q, Guo Y, Huang T, Zhang L, Lu T, Feng Q, Hao H, Liu H, Lu P, Zhang N, Li Y, Guo E, Wang S, Wang S, Liu J, Zhang W, Chen G, Zhang B, Li W, Wang Y, Li H, Zhao B, Li J, Diao X, Han B (2013) A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica). Nat Genet 45:957–961
Khan Y, Yadav A, Suresh BV, Muthamilarasan M, Yadav CB, Prasad M (2014) Comprehensive genome-wide identification and expression profiling of foxtail millet [Setaria italica (L.)] miRNAs in response to abiotic stress and development of miRNA database. Plant Cell Tissue Organ Cult. doi:10.1007/s11240-014-0480-x
Kiełbowicz-Matuk A (2011) Involvement of plant C2H2-type zinc finger transcription factors in stress responses. Plant Sci 186:78–85
Kodaira KS, Qin F, Tran LS, Maruyama K, Kidokoro S, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K (2011) Arabidopsis Cys2/His2 zinc-finger proteins AZF1 and AZF2 negatively regulate abscisic acid-repressive and auxin-inducible genes under abiotic stress conditions. Plant Physiol 157:742–756
Kumar K, Muthamilarasan M, Prasad M (2013) Reference genes for quantitative Real-time PCR analysis in the model plant foxtail millet (Setaria italica L.) subjected to abiotic stress conditions. Plant Cell Tissue Organ Cult 115:13–22
Kumari K, Muthamilarasan M, Misra G, Gupta S, Subramanian A, Parida SK, Chattopadhyay D, Prasad M (2013) Development of eSSR-markers in Setaria italica and their applicability in studying genetic diversity, cross-transferability and comparative mapping in millet and non-millet species. PLoS ONE 8:e67742
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359
Lata C, Gupta S, Prasad M (2013) Foxtail millet: a model crop for genetic and genomic studies in bioenergy grasses. Crit Rev Biotechnol 33:328–343
Lecharny A, Boudet N, Gy I, Aubourg S, Kreis M (2003) Introns in, introns out in plant gene families: a genomic approach of the dynamics of gene structure. J Struct Funct Genom 3:111–116
Longeman J, Schell J, Willmitzer L (1987) Improved method for the isolation of RNA from plant tissues. Anal Biochem 163:16–20
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155
Mishra AK, Muthamilarasan M, Khan Y, Parida SK, Prasad M (2014) Genome-wide investigation and expression analyses of WD40 protein family in the model plant foxtail millet (Setaria italica L.). PLoS ONE 9:e86852
Muthamilarasan M, Theriappan P, Prasad M (2013) Recent advances in crop genomics for ensuring food security. Curr Sci 105:155–158
Muthamilarasan M, Venkata Suresh B, Pandey G, Kumari K, Parida SK, Prasad M (2014) Development of 5123 intron-length polymorphic markers for large-scale genotyping applications in foxtail millet. DNA Res 21:41–52
Pandey G, Misra G, Kumari K, Gupta S, Parida SK, Chattopadhyay D, Prasad M (2013) Genome-wide development and use of microsatellite markers for large-scale genotyping applications in foxtail millet [Setaria italica (L.)]. DNA Res 20:197–207
Pérez-Rodríguez P, Riaño-Pachón DM, Corrêa LG, Rensing SA, Kersten B, Mueller-Roeber B (2009) PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38:D822–D827
Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381
Puranik S, Sahu PP, Mandal SN BVS, Parida SK, Prasad M (2013) Comprehensive genome-wide survey, genomic constitution and expression profiling of the NAC transcription factor family in foxtail millet (Setaria italica L.). PLoS ONE 8:e64594
Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374–378
Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J (2006) TM4 microarray software suite. Methods Enzymol 411:134–193
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Shiu S-H, Bleecker AB (2003) Expansion of the Receptor-Like Kinase/Pelle Gene Family and Receptor-Like Proteins in Arabidopsis. Plant Physiol 132:530–543
Sigrist CJ, de Castro E, Cerutti L, Cuche BA, Hulo N, Bridge A, Bougueleret L, Xenarios I (2013) New and continuing developments at PROSITE. Nucleic Acids Res 41:D344–D347
Sun SJ, Guo SQ, Yang X, Bao YM, Tang HJ, Sun H, Huang J, Zhang HS (2010) Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. J Exp Bot 61:2807–2818
Suresh BV, Muthamilarasan M, Misra G, Prasad M (2013) FmMDb: a versatile database of foxtail millet markers for millets and bioenergy grasses research. PLoS ONE 8:e71418
Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609–W612
Takatsuji H (1999) Zinc-finger proteins: the classical zinc finger emerges in contemporary plant science. Plant Mol Biol 39:1073–1078
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH (2008) Synteny and collinearity in plant genomes. Science 320:486–488
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
Tian ZD, Zhang Y, Liu J, Xie CH (2010) Novel potato C2H2-type zinc finger protein gene, StZFP1, which responds to biotic and abiotic stress, plays a role in salt tolerance. Plant Biol 12:689–697
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wang Y, Dou D, Wang X, Li A, Sheng Y, Hua C, Cheng B, Chen X, Zheng X, Wang Y (2009) The PsCZF1 gene encoding a C2H2 zinc finger protein is required for growth, development and pathogenesis in Phytophthora sojae. Microb Pathog 47:78–86
Wang N, Zheng Y, Xin H, Fang L, Li S (2013) Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep 32:61–75
Xiao H, Tang J, Li Y, Wang W, Li X, Jin L, Xie R, Luo H, Zhao X, Meng Z, He G, Zhu L (2009) STAMENLESS 1, encoding a single C2H2 zinc finger protein, regulates floral organ identity in rice. Plant J 59:789–801
Yadav CB, Muthamilarasan M, Pandey G, Prasad M (2014) Identification, characterization and expression profiling of Dicer-like. Argonaute and RNA-dependent RNA polymerase gene families in foxtail millet. Plant Mol Biol Report. doi:10.1007/s11105-014-0736-y
Yang Z, Gu S, Wang X, Li W, Tang Z, Xu C (2008) Molecular evolution of the cpp-like gene family in plants: insights from comparative genomics of Arabidopsis and rice. J Mol Evol 67:266–277
Yi F, Xie S, Liu Y, Qi X, Yu J (2014) Genome-wide characterization of microRNA in foxtail millet (Setaria italica). BMC Plant Biol 13:212
Zdobnov EM, Apweiler R (2001) InterProScan—an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848
Zhang G, Liu X, Quan Z, Cheng S, Xu X, Pan S, Xie M, Zeng P, Yue Z, Wang W, Tao Y, Bian C, Han C, Xia Q, Peng X, Cao R, Yang X, Zhan D, Hu J, Zhang Y, Li H, Li H, Li N, Wang J, Wang C, Wang R, Guo T, Cai Y, Liu C, Xiang H, Shi Q, Huang P, Chen Q, Li Y, Wang J, Zhao Z, Wang J (2012) Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential Nature. Biotech 30:549–554
Acknowledgments
This work was financially supported by the core grant of National Institute of Plant Genome Research (NIPGR), New Delhi, India. Mr. Mehanathan Muthamilarasan and Mr. Awdhesh Kumar Mishra acknowledge the awards of Research Fellowship from University Grants Commission and Council of Scientific and Industrial Research, New Delhi, India, respectively. The authors also thank Mr. Subodh Verma, NIPGR for his timely assistance.
Author information
Authors and Affiliations
Corresponding author
Additional information
Mehanathan Muthamilarasan and Venkata Suresh Bonthala contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Figure S1
Intron-exon positions of 124 C2H2-type of zinc finger protein encoding genes of foxtail millet. Exons and introns are represented by green boxes and black lines, respectively. (PDF 153 kb)
Supplementary Figure S2
Distribution of C2H2-type of zinc finger protein in sequenced plant genomes. The data was retrieved from Plant Transcription Factor Database (http://planttfdb.cbi.pku.edu.cn/). (GIF 274 kb)
Supplementary Table S1
Details of primers used for quantitative real-time PCR. (DOC 32 kb)
Supplementary Table S2
Characteristic features of 124 C2H2-type of zinc finger protein encoding genes in foxtail millet. (XLS 52 kb)
Supplementary Table S3
Summary of functional domains present in 124 SiC2H2 proteins revealed through PROSITE and InterProScan. (XLS 58 kb)
Supplementary Table S4
List of predicted miRNAs targeting SiC2H2 transcripts (Setaria italica miRNAs are given in bold). (XLS 26 kb)
Supplementary Table S5
Details of SiC2H2 transcription factor-based markers. (XLS 45 kb)
Supplementary Table S6
Blast2GO annotation details of SiC2H2 protein sequences. (XLS 37 kb)
Supplementary Table S7
Summary of cis-acting regulatory elements present in the upstream sequences of all the 124 C2H2-type of zinc finger proteins. (XLS 1008 kb)
Supplementary Table S8
The Ka/Ks ratios and estimated divergence time for orthologous SiC2H2 proteins between foxtail millet, sorghum, maize and rice. (XLS 27 kb)
Rights and permissions
About this article
Cite this article
Muthamilarasan, M., Bonthala, V.S., Mishra, A.K. et al. C2H2 type of zinc finger transcription factors in foxtail millet define response to abiotic stresses. Funct Integr Genomics 14, 531–543 (2014). https://doi.org/10.1007/s10142-014-0383-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-014-0383-2