Comparative genomic analysis of the WRKY III gene family in populus, grape, arabidopsis and rice
Tóm tắt
WRKY III genes have significant functions in regulating plant development and resistance. In plant, WRKY gene family has been studied in many species, however, there still lack a comprehensive analysis of WRKY III genes in the woody plant species poplar, three representative lineages of flowering plant species are incorporated in most analyses: Arabidopsis (a model plant for annual herbaceous dicots), grape (one model plant for perennial dicots) and Oryza sativa (a model plant for monocots). In this study, we identified 10, 6, 13 and 28 WRKY III genes in the genomes of Populus trichocarpa, grape (Vitis vinifera), Arabidopsis thaliana and rice (Oryza sativa), respectively. Phylogenetic analysis revealed that the WRKY III proteins could be divided into four clades. By microsynteny analysis, we found that the duplicated regions were more conserved between poplar and grape than Arabidopsis or rice. We dated their duplications by Ks analysis of Populus WRKY III genes and demonstrated that all the blocks were formed after the divergence of monocots and dicots. Strong purifying selection has played a key role in the maintenance of WRKY III genes in Populus. Tissue expression analysis of the WRKY III genes in Populus revealed that five were most highly expressed in the xylem. We also performed quantitative real-time reverse transcription PCR analysis of WRKY III genes in Populus treated with salicylic acid, abscisic acid and polyethylene glycol to explore their stress-related expression patterns. This study highlighted the duplication and diversification of the WRKY III gene family in Populus and provided a comprehensive analysis of this gene family in the Populus genome. Our results indicated that the majority of WRKY III genes of Populus was expanded by large-scale gene duplication. The expression pattern of PtrWRKYIII gene identified that these genes play important roles in the xylem during poplar growth and development, and may play crucial role in defense to drought stress. Our results presented here may aid in the selection of appropriate candidate genes for further characterization of their biological functions in poplar. This article was reviewed by Prof Dandekar and Dr Andrade-Navarro.
Tài liệu tham khảo
Cai C, Niu E, Du H, Zhao L, Feng Y, Guo W. Genome-wide analysis of the WRKY transcription factor gene family in Gossypium raimondii and the expression of orthologs in cultivated tetraploid cotton. Crop J. 2014;2(2):87–101.
Huang S, Gao Y, Liu J, Peng X, Niu X, Fei Z, et al. Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol Genet Genomics. 2012;287(6):495–513. doi:10.1007/s00438-012-0696-6.
Eulgem T, Rushton PJ, Robatzek S, Somssich IE. The WRKY superfamily of plant transcription factors. Trends Plant Sci. 2000;5(5):199–206.
Wu K-L, Guo Z-J, Wang H-H, Li J. The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res. 2005;12(1):9–26.
Guo C, Guo R, Xu X, Gao M, Li X, Song J, et al. Evolution and expression analysis of the grape (Vitis vinifera L.) WRKY gene family. J Exp Bot. 2014;65(6):1513–28. doi:10.1093/jxb/eru007.
He H, Dong Q, Shao Y, Jiang H, Zhu S, Cheng B, et al. Genome-wide survey and characterization of the WRKY gene family in Populus trichocarpa. Plant Cell Rep. 2012;31(7):1199–217. doi:10.1007/s00299-012-1241-0.
Jiang Y, Duan Y, Yin J, Ye S, Zhu J, Zhang F, et al. Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses. J Exp Bot. 2014;65(22):6629–44. doi:10.1093/jxb/eru381.
Llorca CM, Potschin M, Zentgraf U. bZIPs and WRKYs: two large transcription factor families executing two different functional strategies. Front Plant Sci. 2014;5.
Ling J, Jiang W, Zhang Y, Yu H, Mao Z, Gu X, et al. Genome-wide analysis of WRKY gene family in Cucumis sativus. BMC Genomics. 2011;12(1):471.
Du L, Chen Z. Identification of genes encoding receptor‐like protein kinases as possible targets of pathogen‐and salicylic acid‐induced WRKY DNA‐binding proteins in Arabidopsis. Plant J. 2000;24(6):837–47.
Pandey SP, Somssich IE. The role of WRKY transcription factors in plant immunity. Plant Physiol. 2009;150(4):1648–55.
Zhou X, Wang G, Sutoh K, Zhu J-K, Zhang W. Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim Biophys Acta. 2008;1779(11):780–8.
Zou C, Jiang W, Yu D. Male gametophyte-specific WRKY34 transcription factor mediates cold sensitivity of mature pollen in Arabidopsis. J Exp Bot. 2010;61(14):3901–14. doi:10.1093/jxb/erq204.
Jiang Y, Deyholos MK. Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol. 2009;69(1–2):91–105.
Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K. Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep. 2009;28(1):21–30.
Jiang Y, Liang G, Yu D. Activated expression of WRKY57 confers drought tolerance in Arabidopsis. Mol Plant. 2012;5(6):1375–88. doi:10.1093/mp/sss080.
Ren X, Chen Z, Liu Y, Zhang H, Zhang M, Liu Q, et al. ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J. 2010;63(3):417–29. doi:10.1111/j.1365-313X.2010.04248.x.
Shen H, Liu C, Zhang Y, Meng X, Zhou X, Chu C, et al. OsWRKY30 is activated by MAP kinases to confer drought tolerance in rice. Plant Mol Biol. 2012;80(3):241–53. doi:10.1007/s11103-012-9941-y.
Zhang YJ, Wang LJ. The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol. 2005;5. doi:10.1186/1471-2148-5-1.
Kalde M, Barth M, Somssich IE, Lippok B. Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Mol Plant Microbe Interact. 2003;16(4):295–305.
Lynch M, Conery JS. The evolutionary fate and consequences of duplicate genes. Science. 2000;290(5494):1151–5.
Dwight SS, Harris MA, Dolinski K, Ball CA, Binkley G, Christie KR, et al. Saccharomyces Genome Database (SGD) provides secondary gene annotation using the Gene Ontology (GO). Nucleic Acids Res. 2002;30(1):69–72. doi:10.1093/nar/30.1.69.
Li Z, Jiang H, Zhou L, Deng L, Lin Y, Peng X, et al. Molecular evolution of the HD-ZIP I gene family in legume genomes. Gene. 2014;533(1):218–28. doi:10.1016/j.gene.2013.09.084.
Lin Y, Cheng Y, Jin J, Jin X, Jiang H, Yan H, et al. Genome duplication and gene loss affect the evolution of heat shock transcription factor genes in legumes. PLoS One. 2014;9(7):e102825.
Cannon SB, McCombie WR, Sato S, Tabata S, Denny R, Palmer L, et al. Evolution and microsynteny of the apyrase gene family in three legume genomes. Mol Genet Genomics. 2003;270(4):347–61. doi:10.1007/s00438-003-0928-x.
Maher C, Stein L, Ware D. Evolution of Arabidopsis microRNA families through duplication events. Genome Res. 2006;16(4):510–9.
Deleu W, González V, Monfort A, Bendahmane A, Puigdomènech P, Arús P, et al. Structure of two melon regions reveals high microsynteny with sequenced plant species. Mol Genet Genomics. 2007;278(6):611–22.
Song Y, Gao J. Genome-wide analysis of WRKY gene family in Arabidopsis lyrata and comparison with Arabidopsis thaliana and Populus trichocarpa. Chin Sci Bull. 2014;59(8):754–65.
Chen L, Song Y, Li S, Zhang L, Zou C, Yu D. The role of WRKY transcription factors in plant abiotic stresses. Biochim Biophys Acta. 2012;1819(2):120–8.
Luo X, Bai X, Sun X, Zhu D, Liu B, Ji W, et al. Expression of wild soybean WRKY20 in Arabidopsis enhances drought tolerance and regulates ABA signalling. J Exp Bot. 2013;64(8):2155–69.
Wang M, Vannozzi A, Wang G, Liang Y-H, Tornielli GB, Zenoni S et al. Genome and transcriptome analysis of the grapevine (Vitis vinifera L.) WRKY gene family. Horticulture Res. 2014;1. doi:10.1038/hortres.2014.16.
Rushton DL, Tripathi P, Rabara RC, Lin J, Ringler P, Boken AK, et al. WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnol J. 2012;10(1):2–11. doi:10.1111/j.1467-7652.2011.00634.x.
Yan L, Liu Z-Q, Xu Y-H, Lu K, Wang X-F, Zhang D-P. Auto- and cross-repression of three Arabidopsis WRKY transcription factors WRKY18, WRKY40, and WRKY60 negatively involved in ABA signaling. J Plant Growth Regul. 2013;32(2):399–416. doi:10.1007/s00344-012-9310-8.
Wang L, Zhu W, Fang L, Sun X, Su L, Liang Z et al. Genome-wide identification of WRKY family genes and their response to cold stress in Vitis vinifera. BMC Plant Biol. 2014;14. doi:10.1186/1471-2229-14-103.
Dittmar K, Liberles D. Evolution after gene duplication. John Wiley & Sons; 2011.
Feng L, Chen Z, Ma H, Chen X, Li Y, Wang Y, et al. The IQD gene family in soybean: structure, phylogeny, evolution and expression. PLoS One. 2014;9(10):e110896.
Besseau S, Li J, Palva ET. WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. J Exp Bot. 2012;63(7):2667–79. doi:10.1093/jxb/err450.
Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 2003;31(13):3784–8. doi:10.1093/nar/gkg563.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9.
Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406–25.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28(10):2731–9. doi:10.1093/molbev/msr121.
Hu R, Qi G, Kong Y, Kong D, Gao Q, Zhou G. Comprehensive analysis of NAC domain transcription factor gene family in populus trichocarpa. BMC Plant Biol. 2010;10. doi:10.1186/1471-2229-10-145.
Guo A-Y, Zhu Q-H, Chen X, Luo J-C. GSDS: a gene structure display server. Yi Chuan. 2007;29(8):1023–6.
Bailey TL, Elkan C, editors. The value of prior knowledge in discovering motifs with MEME. Ismb; 1995.
Cai B, Yang X, Tuskan GA, Cheng Z-M. MicroSyn: A user friendly tool for detection of microsynteny in a gene family. BMC Bioinformatics. 2011;12(1):79.
Wang L, Guo K, Li Y, Tu Y, Hu H, Wang B, et al. Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biol. 2010;10(1):282.
Zhang X, Feng Y, Cheng H, Tian D, Yang S, Chen J-Q. Relative evolutionary rates of NBS-encoding genes revealed by soybean segmental duplication. Mol Genet Genomics. 2011;285(1):79–90. doi:10.1007/s00438-010-0587-7.
Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 2006;34:W609–12. doi:10.1093/nar/gkl315.
Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24(8):1586–91.
Ma H, Feng L, Chen Z, Chen X, Zhao H, Xiang Y. Genome-wide identification and expression analysis of the IQD gene family in Populus trichocarpa. Plant Sci. 2014;229:96–110.
Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc. 2008;3(6):1101–8.
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(−Delta Delta C) method. Methods. 2001;25(4):402–8. doi:10.1006/meth.2001.1262.
Bryfczynski S, editor. GraphPad: a CS2/CS7 tool for graph creation. Proceedings of the 47th Annual Southeast Regional Conference; 2009: ACM.