Abstract
The WRKY superfamily of transcription factors was shown to be involved in biotic and abiotic stress responses in plants such as wheat (Triticum aestivum L.), one of the major crops largely cultivated and consumed all over the world. Drought is an important abiotic stress resulting in a considerable amount of loss in agronomical yield. Therefore, identification of drought responsive WRKY members in wheat has a profound significance. Here, a total of 160 TaWRKY proteins were characterized according to sequence similarity, motif varieties, and their phylogenetic relationships. The conserved sequences of the TaWRKYs were aligned and classified into three main groups and five subgroups. A novel motif in wheat, WRKYGQR, was identified. To putatively determine the drought responsive TaWRKY members, publicly available RNA-Seq data were analyzed for the first time in this study. Through in silico searches, 35 transcripts were detected having an identity to ten known TaWRKY genes. Furthermore, relative expression levels of TaWRKY16/TaWRKY16-A, TaWRKY17, TaWRKY19-C, TaWRKY24, TaWRKY59, TaWRKY61, and TaWRKY82 were measured in root and leaf tissues of drought-tolerant Sivas 111/33 and susceptible Atay 85 cultivars. All of the quantified TaWRKY transcripts were found to be up-regulated in root tissue of Sivas 111/33. Differential expression of TaWRKY16, TaWRKY24, TaWRKY59, TaWRKY61 and TaWRKY82 genes was discovered for the first time upon drought stress in wheat. These comprehensive analyses bestow a better understanding about the WRKY TFs in bread wheat under water deficit, and increased number of drought responsive WRKYs would contribute to the molecular breeding of tolerant wheat cultivars.
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Abbreviations
- HMM:
-
Hidden Markov model
- NCBI:
-
National Center for Biotechnology Information
- PlantTFDB:
-
Plant Transcription Factor Database
- qRT-PCR:
-
Quantitative reverse transcription PCR
- SRA:
-
Sequence Read Archive
- TF:
-
Transcription factor
References
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37(Web Server issue):W202–W208. doi:10.1093/nar/gkp335
Brenchley R, Spannagl M, Pfeifer M, Barker GL, D’Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo MC, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KF, Edwards KJ, Bevan MW, Hall N (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491(7426):705–710. doi:10.1038/nature11650
Budak H, Akpinar BA, Unver T, Turktas M (2013) Proteome changes in wild and modern wheat leaves upon drought stress by two-dimensional electrophoresis and nanoLC-ESI-MS/MS. Plant Mol Biol 83(1–2):89–103. doi:10.1007/s11103-013-0024-5
Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X (2010) Roles of arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10:281. doi:10.1186/1471-2229-10-281
Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6(11):836–846. doi:10.1038/nrg1711
Ergen NZ, Thimmapuram J, Bohnert HJ, Budak H (2009) Transcriptome pathways unique to dehydration tolerant relatives of modern wheat. Funct Integr Genomics 9(3):377–396. doi:10.1007/s10142-009-0123-1
Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5(5):199–206
Gregersen PL, Holm PB (2007) Transcriptome analysis of senescence in the flag leaf of wheat (Triticum aestivum L.). Plant Biotechnol J 5(1):192–206. doi:10.1111/j.1467-7652.2006.00232.x
He H, Dong Q, Shao Y, Jiang H, Zhu S, Cheng B, Xiang Y (2012) Genome-wide survey and characterization of the WRKY gene family in Populus trichocarpa. Plant Cell Rep 31(7):1199–1217. doi:10.1007/s00299-012-1241-0
Huang S, Gao Y, Liu J, Peng X, Niu X, Fei Z, Cao S, Liu Y (2012) Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol Genet Genomics 287(6):495–513. doi:10.1007/s00438-012-0696-6
Jin J, Zhang H, Kong L, Gao G, Luo J (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42(1):D1182–D1187. doi:10.1093/nar/gkt1016
Ling J, Jiang W, Zhang Y, Yu H, Mao Z, Gu X, Huang S, Xie B (2011) Genome-wide analysis of WRKY gene family in Cucumis sativus. BMC Genomics 12:471. doi:10.1186/1471-2164-12-471
Mangelsen E, Kilian J, Berendzen KW, Kolukisaoglu UH, Harter K, Jansson C, Wanke D (2008) Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare) WRKY transcription factor family reveals putatively retained functions between monocots and dicots. BMC Genomics 9:194. doi:10.1186/1471-2164-9-194
Manickavelu A, Kawaura K, Oishi K, Shin IT, Kohara Y, Yahiaoui N, Keller B, Abe R, Suzuki A, Nagayama T, Yano K, Ogihara Y (2012) Comprehensive functional analyses of expressed sequence tags in common wheat (Triticum aestivum). DNA Res 19(2):165–177. doi:10.1093/dnares/dss001
Niu CF, Wei W, Zhou QY, Tian AG, Hao YJ, Zhang WK, Ma B, Lin Q, Zhang ZB, Zhang JS, Chen SY (2012) Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant Cell Environ 35(6):1156–1170. doi:10.1111/j.1365-3040.2012.02480.x
Nuruzzaman M, Sharoni AM, Satoh K, Kumar A, Leung H, Kikuchi S (2014) Comparative transcriptome profiles of the WRKY gene family under control, hormone-treated, and drought conditions in near-isogenic rice lines reveal differential, tissue specific gene activation. J Plant Physiol 171(1):2–13. doi:10.1016/j.jplph.2013.09.010
Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40(Database issue): D290–D301 doi: 10.1093/nar/gkr1065
Ramiro D, Jalloul A, Petitot A-S, Grossi De Sá MF, Maluf MP, Fernandez D (2010) Identification of coffee WRKY transcription factor genes and expression profiling in resistance responses to pathogens. Tree Genet Genomes 6(5):767–781. doi:10.1007/s11295-010-0290-1
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15(5):247–258. doi:10.1016/j.tplants.2010.02.006
Saad AS, Li X, Li HP, Huang T, Gao CS, Guo MW, Cheng W, Zhao GY, Liao YC (2013) A rice stress-responsive NAC gene enhances tolerance of transgenic wheat to drought and salt stresses. Plant Sci 203–204:33–40. doi:10.1016/j.plantsci.2012.12.016
Shewry PR, Tatham AS (1997) Biotechnology of wheat quality. J Sci Food Agric 73:397–406
Song Y, Jing S, Yu D (2010) Overexpression of the stress-induced OsWRKY08 improves osmotic stress tolerance in Arabidopsis. Chin Sci Bull 54(24):4671–4678. doi:10.1007/s11434-009-0710-5
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729
Tombuloglu H, Kekec G, Sakcali MS, Unver T (2013) Transcriptome-wide identification of R2R3-MYB transcription factors in barley with their boron responsive expression analysis. Mol Genet Genomics 288(3–4):141–155. doi:10.1007/s00438-013-0740-1
Tripathi P, Rabara RC, Langum TJ, Boken AK, Rushton DL, Boomsma DD, Rinerson CI, Rabara J, Reese RN, Chen X, Rohila JS, Rushton PJ (2012) The WRKY transcription factor family in Brachypodium distachyon. BMC Genomomics 13:270
Tripathi P, Rabara RC, Rushton PJ (2014) A systems biology perspective on the role of WRKY transcription factors in drought responses in plants. Planta 239:255–266. doi:10.1007/s00425-013-1985-y
Turktas M, Inal B, Okay S, Erkilic EG, Dundar E, Hernandez P, Dorado G, Unver T (2013) Nutrition metabolism plays an important role in the alternate bearing of the olive tree (Olea europaea L.). PLoS ONE 8(3):e59876. doi:10.1371/journal.pone.0059876
Ulker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7(5):491–498. doi:10.1016/j.pbi.2004.07.012
Wang X, Liu W, Chen X, Tang C, Dong Y, Ma J, Huang X, Wei G, Han Q, Huang L, Kang Z (2010) Differential gene expression in incompatible interaction between wheat and stripe rust fungus revealed by cDNA-AFLP and comparison to compatible interaction. BMC Plant Biol 10:9. doi:10.1186/1471-2229-10-9
Wang C, Deng P, Chen L, Wang X, Ma H, Hu W, Yao N, Feng Y, Chai R, Yang G, He G (2013) A wheat WRKY transcription factor TaWRKY10 confers tolerance to multiple abiotic stresses in transgenic tobacco. PLoS ONE 8(6):e65120. doi:10.1371/journal.pone.0065120
Wu K-L, Guo Z-J, Wang H–H, Li J (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12:9–26
Wu H, Ni Z, Yao Y, Guo G, Sun Q (2008) Cloning and expression profiles of 15 genes encoding WRKY transcription factor in wheat (Triticum aestivum L.). Progress Nat Sci 18(6):697–705. doi:10.1016/j.pnsc.2007.12.006
Xie Z, Zhang ZL, Zou X, Huang J, Ruas P, Thompson D, Shen QJ (2005) Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol 137(1):176–189. doi:10.1104/pp.104.054312
Yang B, Jiang Y, Rahman MH, Deyholos MK, Kav NN (2009) Identification and expression analysis of WRKY transcription factor genes in canola (Brassica napus L.) in response to fungal pathogens and hormone treatments. BMC Plant Biol 9:68. doi:10.1186/1471-2229-9-68
Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, Wang CM, Wang HW, Zhang JS, Chen SY (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol J 6(5):486–503. doi:10.1111/j.1467-7652.2008.00336.x
Zhu X, Liu S, Meng C, Qin L, Kong L, Xia G (2013) WRKY transcription factors in wheat and their induction by biotic and abiotic stress. Plant Mol Biol Rep 31(5):1053–1067. doi:10.1007/s11105-013-0565-4
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The authors thank Bianka Martinez (International Language Learning Center, Cankiri Karatekin University) for revising the manuscript.
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Communicated by S. Hohmann.
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Okay, S., Derelli, E. & Unver, T. Transcriptome-wide identification of bread wheat WRKY transcription factors in response to drought stress. Mol Genet Genomics 289, 765–781 (2014). https://doi.org/10.1007/s00438-014-0849-x
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DOI: https://doi.org/10.1007/s00438-014-0849-x