Comprehensive analysis of CCCH zinc-finger-type transcription factors in the Brassica rapa genome

Alam I, Yang YQ, Wang Y, Zhu ML, Wang H-B, Chalhoub B, Lu YH (2017) Genome—wide identification, evolution and expression analysis of RING finger protein genes in Brassica rapa. Sci Rep 7:40690 Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L et al (2009) MEME suite: tools for motif discovery and searching. Nucl Acids Res 37:W202–W208 Berg JM, Shi Y (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science 271:1081–1085 Blackshear PJ (2002) Tris tetraprolin and other CCCH tandem zinc-finger proteins in the regulation of mRNA turnover. Biochem Soc Trans 30:945–952 Blanvillain R, Wei S, Wei P, Kim JH, Ow DW (2011) Stress tolerance to stress escape in plants: role of the OXS2 zinc-finger transcription factor family. EMBO J 30:3812–3822 Bogamuwa S, Jang JC (2013) The Arabidopsis tandem CCCH zinc finger proteins AtTZF4, 5 and 6 are involved in light-, abscisic acid- and gibberellic acid-mediated regulation of seed germination. Plant Cell Environ 36:1507–1519 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 Genom 13:253 Chen W-J, Zhao Y, Peng X-J, Dong Q, Jin J, Zhou W, Cheng B-J, Ma Q (2015) Significant micro synteny with new evolutionary highlights is detected through comparative genomic sequence analysis of maize CCCH IX gene subfamily. Int J Genomics. https://doi.org/10.1155/2015/824287 Cheng F, Mandáková T, Wu J, Xie Q, Lysak MA, Wang X (2013) Deciphering the diploid ancestral genome of the Mesohexaploid Brassica rapa. Plant Cell 25:1541–1554 Chorev M, Carmel L (2012) The function of introns. Front Genet 3:55 Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163 Dapeng W, Yubin Z, Zhang Z, Jiang Z, Jun Y (2010) KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinform 8:77–80 Dong H, Liu D, Han T, Zhao Y, Sun J, Lin S, Cao J, Chen Z-H, Huang L (2015) Diversification and evolution of the SDG gene family in Brassica rapa after the whole genome triplication. Sci Rep 5:16851 Gama-Carvalho M, Carmo-Fonseca M (2001) The rules and roles of nucleocytoplasmic shuttling proteins. FEBS Lett 498:157–163 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 Guo YH, Yu YP, Wang D, Wu CA, Yang GD, Huang JG, Zheng CC (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 Hu T, Banzhaf W (2008) Nonsynonymous to synonymous substitution ratio ka/ks: measurement for rate of evolution in evolutionary computation. In: Rudolph G, Jansen T, Beume N, Lucas S, Poloni C (eds) Parallel problem solving from nature—PPSN X. PPSN 2008. Lecture notes in computer science, vol 5199. Springer, Berlin, pp 448–457 Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297 Huang P, Ju H-W, Min J-H, Zhang X, Chung J-S, Cheong H-S, Kim CS (2012) Molecular and physiological characterization of the Arabidopsis thaliana oxidation-related zinc finger 2, a plasma membrane protein involved in ABA and salt stress response through the abi2-mediated signaling pathway. Plant Cell Physiol 53:193–203 Huang Z, Tang J, Duan W, Wang Z, Song X, Hou X (2015) Molecular evolution, characterization, and expression analysis of SnRK2 gene family in Pak-choi (Brassica rapa ssp. chinensis). Front Plant Sci 6:879 Jack T (2002) New members of the floral organ identity AGAMOUS pathway. Trends Plant Sci 7:7 Jan AMK, Todaka D, Kidokoro S, Abo M, Yoshimura E, Shinozaki K et al (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 Kayum MA, Jung HJ, Park JT, Ahmed NU, Saha G, Yang TJ et al (2015) Identification and expression analysis of WRKY family genes under biotic and abiotic stresses in Brassica rapa. Mol Genet Genomics 290:79–95 Kielkopf CL, Lucke S, Green MR (2004) U2AF homology motifs: protein recognition in the RRM world. Genes Dev 18:1513–1526 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 Kim J, Lee J, Choi J-P, Park I, Yang K, Kim MK et al (2014) Functional innovations of three chronological mesohexaploid Brassica rapa genomes. BMC Genom 15:606 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 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 Laity JH, Lee BM, Wright PE (2001) Zinc finger proteins: new insights into structural and functional diversity. Curr Opin Struct Biol 11:39–46 Lee TI, Young RA (2000) Transcription of eukaryotic protein-coding genes. Ann Rev Gen 34:77–137 Lee SC, Lim MH, Kim JA, Lee SI, Kim JS, Jin M et al (2008) Transcriptome analysis in Brassica rapa under the abiotic stresses using Brassica 24 K oligo microarray. Mol Cell 26:595–605 Lee SJ, Jung HJ, Kang H, Kim SY (2012) Arabidopsis zinc finger proteins AtC3H49/AtTZF3 and AtC3H20/AtTZF2 are involved in ABA and JA responses. Plant Cell Physiol 53:673–686 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 Lin PC, Pomeranz MC, Jikumaru Y, Kang SG, Hah C, Fujioka S et al (2011) The Arabidopsis tandem zinc finger protein AtTZF1 affects ABA- and GA-mediated growth, stress and gene expression responses. Plant J 65:253–268 Liu S, Khan RMG, Li Y, Zhang J, Hu C (2014) Comprehensive analysis of CCCH-type zinc finger gene family in citrus (Clementine mandarin) by genome-wide characterization. Mol Genet Genomics 289:855–872 Ma J, Li MY, Wang F, Tang J, Xiong AS (2015) Genome-wide analysis of Dof family transcription factors and their responses to abiotic stresses in Chinese cabbage. BMC Genom 16:33 Maris C, Dominguez C, Allain FH (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272:2118–2131 Mosavi LK, Minor DL, Peng ZY (2002) Consensus-derived structural determinants of the ankyrin repeat motif. Proc Natl Acad Sci USA 99:16029–16034 Park JI, Ahmed NU, Jung HJ, Arasan SK, Chung MY, Cho YG et al (2014) Identification and characterization of LIM gene family in Brassica rapa. BMC Genom 15:641 Paul P, Dhandapani V, Rameneni JJ, Li X, Sivanandhan G, Choi SR et al (2016) Genome-wide analysis and characterization of Aux/IAA family genes in Brassica rapa. PLoS ONE 11:e0151522 Peng X, Zhao Y, Cao J, Zhang W, Jiang H, Li X 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 Ramchiary N, Lim YP (2011) Genetics of Brassica rapa L. In: Schmidt R, Bancroft I (eds) Genetics and genomics of the Brassicaceae. Springer, New York, pp 215–260 Rameneni JJ, Dhandapani V, Paul P, Im S, Oh M-H, Choi SR, Lim YP (2014) Genome-wide identification, characterization, and comparative phylogeny analysis of MADS-box transcription factors in Brassica rapa. Genes Genomics 36:509–525 Rameneni JJ, Lee Y, Dhandapani V, Yu X, Choi SR, Oh M-H et al (2015) Genomic and posttranslational modification analysis of leucine-rich repeat receptor-like kinases in Brassica rapa. PLoS ONE 10:e0142255 Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110 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 Schranz ME, Lysak MA, Mitchell-Olds T (2006) The ABCs of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11:535–542 Song X, Li Y, Hou X (2013) Genome-wide analysis of the AP2/ERF transcription factor superfamily in Chinese cabbage (Brassica rapa ssp. pekinensis). BMC Genom 14:573 Stirnimann CU, Petsalaki E, Russell RB, Müller CW (2010) WD40 proteins propel cellular networks. Trends Biochem Sci 35:565–574 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, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729 Tong C, Wang X, Yu J, Wu J, Li W, Huang J et al (2013) Comprehensive analysis of RNA-seq data reveals the complexity of the transcriptome in Brassica rapa. BMC Genom 14:689 Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14 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 Genom 9:44 Wang Y, Zhang W-Z, Song L-F, Zou J-J, Su Z, Wu W-H (2008b) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148:1201–1211 Wang D, Zhang Y, Zhang Z, Zhu J, Yu J (2010) KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinform 8:77–80 Wang X, Wang H, Wang J et al (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 28:1035–1039 Wang F, Qiu N, Ding Q, Li J, Zhang Y, Li H, Gao J (2014a) Genome-wide identification and analysis of the growth-regulating factor family in Chinese cabbage (Brassica rapa L. ssp. pekinensis). BMC Genom 15:807 Wang X-L, Zhong Y, Cheng Z-M (2014b) Evolution and expression analysis of the CCCH zinc finger gene family in Vitis vinifera. Plant Genome 7:15. https://doi.org/10.3835/plantgenome2014.05.0019 Wang Z, Tang J, Hu R, Wu P, Hou X-L, Song X-M, Xiong A-S (2015) Genome-wide analysis of the R2R3-MYB transcription factor genes in Chinese cabbage (Brassica rapa ssp. pekinensis) reveals their stress and hormone responsive patterns. BMC Genom 16:17 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 Yang Z, Bielawski JP (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496–503 Yuan S, Xu B, Zhang J, Xie Z, Cheng Q, Yang Z, Cai Q, Huang B (2015) Comprehensive analysis of CCCH-type zinc finger family genes facilitates functional gene discovery and reflects recent allopolyploidization event in tetraploid switchgrass. BMC Genom 16:129 Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632