Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice
Tóm tắt
Genes in the CCCH family encode zinc finger proteins containing the motif with three cysteines and one histidine residues. They have been known to play important roles in RNA processing as RNA-binding proteins in animals. To date, few plant CCCH proteins have been studied functionally. In this study, a comprehensive computational analysis identified 68 and 67 CCCH family genes in Arabidopsis and rice, respectively. A complete overview of this gene family in Arabidopsis was presented, including the gene structures, phylogeny, protein motifs, and chromosome locations. In addition, a comparative analysis between these genes in Arabidopsis and rice was performed. These results revealed that the CCCH families in Arabidopsis and rice were divided into 11 and 8 subfamilies, respectively. The gene duplication contributed to the expansion of the CCCH gene family in Arabidopsis genome. Expression studies indicated that CCCH proteins exhibit a variety of expression patterns, suggesting diverse functions. Finally, evolutionary analysis showed that one subfamily is higher plant specific. The expression profile indicated that most members of this subfamily are regulated by abiotic or biotic stresses, suggesting that they could have an effective role in stress tolerance. Our comparative genomics analysis of CCCH genes and encoded proteins in two model plant species provides the first step towards the functional dissection of this emerging family of potential RNA-binding proteins.
Tài liệu tham khảo
Takatsuji H: Zinc-finger transcription factors in plants. Cell Mol Life Sci. 1998, 54 (6): 582-596. 10.1007/s000180050186.
Moore M, Ullman C: Recent developments in the engineering of zinc finger proteins. Brief Funct Genomic Proteomic. 2003, 1 (4): 342-355. 10.1093/bfgp/1.4.342.
Freemont PS: The RING finger. A novel protein sequence motif related to the zinc finger. Ann N Y Acad Sci. 1993, 684: 174-192. 10.1111/j.1749-6632.1993.tb32280.x.
Arnaud D, Dejardin A, Leple JC, Lesage-Descauses MC, Pilate G: Genome-wide analysis of LIM gene family in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa. DNA Res. 2007, 14 (3): 103-116. 10.1093/dnares/dsm013.
Kosarev P, Mayer KF, Hardtke CS: Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome. Genome Biol. 2002, 3 (4): RESEARCH0016-10.1186/gb-2002-3-4-research0016.
Nakano T, Suzuki K, Fujimura T, Shinshi H: Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 2006, 140 (2): 411-432. 10.1104/pp.105.073783.
Zhang Y, Wang L: The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol. 2005, 5 (1): 1-10.1186/1471-2148-5-1.
Lijavetzky D, Carbonero P, Vicente-Carbajosa J: Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families. BMC Evol Biol. 2003, 3: 17-10.1186/1471-2148-3-17.
De J, Lai WS, Thorn JM, Goldsworthy SM, Liu X, Blackwell TK, Blackshear PJ: Identification of four CCCH zinc finger proteins in Xenopus, including a novel vertebrate protein with four zinc fingers and severely restricted expression. Gene. 1999, 228 (1–2): 133-145. 10.1016/S0378-1119(98)00617-9.
DuBois RN, McLane MW, Ryder K, Lau LF, Nathans D: A growth factor-inducible nuclear protein with a novel cysteine/histidine repetitive sequence. J Biol Chem. 1990, 265 (31): 19185-19191.
Gomperts M, Pascall JC, Brown KD: The nucleotide sequence of a cDNA encoding an EGF-inducible gene indicates the existence of a new family of mitogen-induced genes. Oncogene. 1990, 5 (7): 1081-1083.
Carrick DM, Lai WS, Blackshear PJ: The tandem CCCH zinc finger protein tristetraprolin and its relevance to cytokine mRNA turnover and arthritis. Arthritis Res Ther. 2004, 6 (6): 248-264. 10.1186/ar1441.
Ma Q, Wadleigh D, Chi T, Herschman H: The Drosophila TIS11 homologue encodes a developmentally controlled gene. Oncogene. 1994, 9 (11): 3329-3334.
Mello CC, Schubert C, Draper B, Zhang W, Lobel R, Priess JR: The PIE-1 protein and germline specification in C. elegans embryos. Nature. 1996, 382 (6593): 710-712. 10.1038/382710a0.
Nie XF, Maclean KN, Kumar V, McKay IA, Bustin SA: ERF-2, the human homologue of the murine Tis11d early response gene. Gene. 1995, 152 (2): 285-286. 10.1016/0378-1119(94)00696-P.
Seydoux G, Mello CC, Pettitt J, Wood WB, Priess JR, Fire A: Repression of gene expression in the embryonic germ lineage of C. elegans. Nature. 1996, 382 (6593): 713-716. 10.1038/382713a0.
Taylor GA, Lai WS, Oakey RJ, Seldin MF, Shows TB, Eddy RL, Blackshear PJ: The human TTP protein: sequence, alignment with related proteins, and chromosomal localization of the mouse and human genes. Nucleic Acids Res. 1991, 19 (12): 3454-10.1093/nar/19.12.3454.
Thompson MJ, Lai WS, Taylor GA, Blackshear PJ: Cloning and characterization of two yeast genes encoding members of the CCCH class of zinc finger proteins: zinc finger-mediated impairment of cell growth. Gene. 1996, 174 (2): 225-233. 10.1016/0378-1119(96)00084-4.
Li J, Jia D, Chen X: HUA1, a regulator of stamen and carpel identities in Arabidopsis, codes for a nuclear RNA binding protein. Plant Cell. 2001, 13 (10): 2269-2281. 10.1105/tpc.13.10.2269.
Delaney KJ, Xu R, Zhang J, Li QQ, Yun KY, Falcone DL, Hunt AG: Calmodulin interacts with and regulates the RNA-binding activity of an Arabidopsis polyadenylation factor subunit. Plant Physiol. 2006, 140 (4): 1507-1521. 10.1104/pp.105.070672.
Berg JM, Shi Y: The galvanization of biology: a growing appreciation for the roles of zinc. Science. 1996, 271 (5252): 1081-1085. 10.1126/science.271.5252.1081.
Lai WS, Carballo E, Strum JR, Kennington EA, Phillips RS, Blackshear PJ: Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol. 1999, 19 (6): 4311-4323.
Lai WS, Carballo E, Thorn JM, Kennington EA, Blackshear PJ: 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. 2000, 275 (23): 17827-17837. 10.1074/jbc.M001696200.
Lai WS, Kennington EA, Blackshear PJ: Tristetraprolin and its family members can promote the cell-free deadenylation of AU-rich element-containing mRNAs by poly(A) ribonuclease. Mol Cell Biol. 2003, 23 (11): 3798-3812. 10.1128/MCB.23.11.3798-3812.2003.
Lai WS, Stumpo DJ, Blackshear PJ: Rapid insulin-stimulated accumulation of an mRNA encoding a proline-rich protein. J Biol Chem. 1990, 265 (27): 16556-16563.
Ramos SB, Stumpo DJ, Kennington EA, Phillips RS, Bock CB, Ribeiro-Neto F, Blackshear PJ: The CCCH tandem zinc-finger protein Zfp36l2 is crucial for female fertility and early embryonic development. Development. 2004, 131 (19): 4883-4893. 10.1242/dev.01336.
Tenenhaus C, Subramaniam K, Dunn MA, Seydoux G: PIE-1 is a bifunctional protein that regulates maternal and zygotic gene expression in the embryonic germ line of Caenorhabditis elegans. Genes Dev. 2001, 15 (8): 1031-1040. 10.1101/gad.876201.
Li Z, Thomas TL: PEI1, an embryo-specific zinc finger protein gene required for heart-stage embryo formation in Arabidopsis. Plant Cell. 1998, 10 (3): 383-398. 10.1105/tpc.10.3.383.
Schmitz RJ, Hong L, Michaels S, Amasino RM: FRIGIDA-ESSENTIAL 1 interacts genetically with FRIGIDA and FRIGIDA-LIKE 1 to promote the winter-annual habit of Arabidopsis thaliana. Development. 2005, 132 (24): 5471-5478. 10.1242/dev.02170.
Kong Z, Li M, Yang W, Xu W, Xue Y: A novel nuclear-localized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol. 2006, 141 (4): 1376-1388. 10.1104/pp.106.082941.
Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X: A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science. 2002, 296 (5565): 79-92. 10.1126/science.1068037.
Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H: A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science. 2002, 296 (5565): 92-100. 10.1126/science.1068275.
Sasaki T, Matsumoto T, Yamamoto K, Sakata K, Baba T, Katayose Y, Wu J, Niimura Y, Cheng Z, Nagamura Y: The genome sequence and structure of rice chromosome 1. Nature. 2002, 420 (6913): 312-316. 10.1038/nature01184.
Feng Q, Zhang Y, Hao P, Wang S, Fu G, Huang Y, Li Y, Zhu J, Liu Y, Hu X: Sequence and analysis of rice chromosome 4. Nature. 2002, 420 (6913): 316-320. 10.1038/nature01183.
The Arabidopsis Genome Initiative: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000, 408 (6814): 796-815. 10.1038/35048692.
Jamison DC: Perl programming for biologists. 2003, Hoboken, N.J.: Wiley-Liss
Patwardhan N, Siever E, Spainhour S: Perl in a nutshell. 2002, Sebastopol, CA: O'Reilly, 2
Brown MC: Perl programmer's reference. 1999, Berkeley, CA: Osborne/McGraw-Hill
Schultz J, Copley RR, Doerks T, Ponting CP, Bork P: SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res. 2000, 28 (1): 231-234. 10.1093/nar/28.1.231.
Sonnhammer EL, Eddy SR, Durbin R: Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins. 1997, 28 (3): 405-420. 10.1002/(SICI)1097-0134(199707)28:3<405::AID-PROT10>3.0.CO;2-L.
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25 (24): 4876-4882. 10.1093/nar/25.24.4876.
Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987, 4 (4): 406-425.
Li X, Duan X, Jiang H, Sun Y, Tang Y, Yuan Z, Guo J, Liang W, Chen L, Yin J: Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol. 2006, 141 (4): 1167-1184. 10.1104/pp.106.080580.
Wu KL, Guo ZJ, Wang HH, Li J: The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res. 2005, 12 (1): 9-26. 10.1093/dnares/12.1.9.
Abel S, Savchenko T, Levy M: Genome-wide comparative analysis of the IQD gene families in Arabidopsis thaliana and Oryza sativa. BMC Evol Biol. 2005, 5: 72-10.1186/1471-2148-5-72.
Bailey TL, Elkan C: The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol. 1995, 3: 21-29.
Lorkovic ZJ, Barta A: Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res. 2002, 30 (3): 623-635. 10.1093/nar/30.3.623.
Vision TJ, Brown DG, Tanksley SD: The origins of genomic duplications in Arabidopsis. Science. 2000, 290 (5499): 2114-2117. 10.1126/science.290.5499.2114.
Bowers JE, Chapman BA, Rong J, Paterson AH: Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature. 2003, 422 (6930): 433-438. 10.1038/nature01521.
Chromosome Map Tool. [http://www.arabidopsis.org/jsp/ChromosomeMap/tool.jsp]
NCBI. [http://www.ncbi.nlm.nih.gov/]
TAIR. [http://www.Arabidopsis.org/]
Blanc G, Hokamp K, Wolfe KH: A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res. 2003, 13 (2): 137-144. 10.1101/gr.751803.
Blanc G, Wolfe KH: Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell. 2004, 16 (7): 1667-1678. 10.1105/tpc.021345.
Blanc G, Wolfe KH: Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell. 2004, 16 (7): 1679-1691. 10.1105/tpc.021410.
NSF Genomics of Loblolly Pine Embryogenesis Project. [http://www.tigr.org/tdb/e2k1/pine/index.shtml]
Crooks GE, Hon G, Chandonia JM, Brenner SE: WebLogo: a sequence logo generator. Genome Res. 2004, 14 (6): 1188-1190. 10.1101/gr.849004.
Meyers BC, Vu TH, Tej SS, Ghazal H, Matvienko M, Agrawal V, Ning J, Haudenschild CD: Analysis of the transcriptional complexity of Arabidopsis thaliana by massively parallel signature sequencing. Nat Biotechnol. 2004, 22 (8): 1006-1011. 10.1038/nbt992.
UniGene of NCBI. [http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db5unigene]
Martin C, Paz-Ares J: MYB transcription factors in plants. Trends Genet. 1997, 13 (2): 67-73. 10.1016/S0168-9525(96)10049-4.
Bork P: Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally?. Proteins. 1993, 17 (4): 363-374. 10.1002/prot.340170405.
Lin JH, Makris A, McMahon C, Bear SE, Patriotis C, Prasad VR, Brent R, Golemis EA, Tsichlis PN: The ankyrin repeat-containing adaptor protein Tvl-1 is a novel substrate and regulator of Raf-1. J Biol Chem. 1999, 274 (21): 14706-14715. 10.1074/jbc.274.21.14706.
Mosavi LK, Minor DL, Peng ZY: Consensus-derived structural determinants of the ankyrin repeat motif. Proc Natl Acad Sci USA. 2002, 99 (25): 16029-16034. 10.1073/pnas.252537899.
Becerra C, Jahrmann T, Puigdomenech P, Vicient CM: Ankyrin repeat-containing proteins in Arabidopsis: characterization of a novel and abundant group of genes coding ankyrin-transmembrane proteins. Gene. 2004, 340 (1): 111-121. 10.1016/j.gene.2004.06.006.
la Cour T, Gupta R, Rapacki K, Skriver K, Poulsen FM, Brunak S: NESbase version 1.0: a database of nuclear export signals. Nucleic Acids Res. 2003, 31 (1): 393-396. 10.1093/nar/gkg101.
Gama-Carvalho M, Carmo-Fonseca M: The rules and roles of nucleocytoplasmic shuttling proteins. FEBS Lett. 2001, 498 (2–3): 157-163. 10.1016/S0014-5793(01)02487-5.
AbuQamar S, Chen X, Dhawan R, Bluhm B, Salmeron J, Lam S, Dietrich RA, Mengiste T: Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. Plant J. 2006, 48 (1): 28-44. 10.1111/j.1365-313X.2006.02849.x.
Genevestigator. [http://www.genevestigator.ethz.ch/at/]
Hudson BP, Martinez-Yamout MA, Dyson HJ, Wright PE: Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d. Nat Struct Mol Biol. 2004, 11 (3): 257-264. 10.1038/nsmb738.
Guex N, Peitsch MC: SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis. 1997, 18 (15): 2714-2723. 10.1002/elps.1150181505.
Barreau C, Paillard L, Osborne HB: AU-rich elements and associated factors: are there unifying principles?. Nucleic Acids Res. 2005, 33 (22): 7138-7150. 10.1093/nar/gki1012.
Bakheet T, Williams BR, Khabar KS: ARED 3.0: the large and diverse AU-rich transcriptome. Nucleic Acids Res. 2006, D111-114. 10.1093/nar/gkj052. 34 Database
TIGR. [http://www.tigr.org]
DATF. [http://datf.cbi.pku.edu.cn/index.php]
MAtDB. [http://mips.gsf.de/proj/plant/jsf/athal/index.jsp]
TIGR Rice Genome Annotation Database and Resource. [http://www.tigr.org/tdb/e2k1/osa1/]
Rice Genome Database-japonica of the Rice Genome Research Program. [http://rgp.dna.affrc.go.jp/]
The International Rice Genome Sequencing Project. [http://rgp.dna.affrc.go.jp]
DBSubLoc. [http://www.bioinfo.tsinghua.edu.cn/dbsubloc.html]
Paralogons in Arabidopsis. [http://wolfe.gen.tcd.ie/athal/dup]
Physcomitrella EST Project. [http://moss.nibb.ac.jp/]