Abstract
In this study, 108 WRKY genes with complete conserved WRKY domain and zinc-finger motif were identified from poplar in silico, and they were classified into three subfamilies named I, II, and III. The WRKY members in group II were further clustered into five subgroups (IIa–e), where members in group I and III formed a single cluster. Thirteen highly expressed genes were employed to profile their spatio-temporal expression patterns in response to osmotic stress and ABA treatment by qRT-PCR. Under both osmotic stress and ABA treatment, overall gene expression displayed a dynamic pattern of “induced amplification—recover” in leaves, but not in roots and stems. Regarding individual gene expression across the seven time points and the three tissues, five genes (PthWRKY28, 56, 62, 88, and 106) were involved in regulation of both osmotic stress tolerance and ABA signaling transduction pathways. Meanwhile, four genes (PthWRKY41, 44, 51, and 116) played distinct roles in either osmotic stress or ABA treatment condition. These suggested that WRKY genes and corresponding pathways may play a critical role in regulating poplar responses to osmotic stress and ABA treatment in a dynamic and tissue-specific manner.
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Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78
An X, Liao YW, Zhang JY, Dai LJ, Zhang N, Wang B, Liu LJ, Peng DX (2015) Overexpression of rice NAC gene SNAC1 in ramie improves drought and salt tolerance. Plant Growth Regul 76(2):211–223
Blanc G, Hokamp K, Wolf KH (2003) A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res 13:137–144
Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438
Chakravarthy S, Tuori RP, D’Ascenzo MD, Fobert PR, Despres C, Martin GB (2003) The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements. Plant Cell 15:3033–3050
Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801
Dietz KJ, Vogel MO, Viehhauser A (2010) AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signalling. Protoplasma 245:3–14
Du L, Chen Z (2000) 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 24(6):837–847
Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE (1999) Early nuclear events in plant defense: rapid gene activation by WRKY transcription factors. EMBO J 18(17):4689–4699
Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206
Fahad S, Hussain S, Matloob A, Khan FA, Khaliq A, Saud S, Hassan S, Shan D, Khan F, Ullah N, Faiq M, Khan MR, Tareen AK, Khan A, Ullah A, Ullah N, Huang JL (2015) Phytohormones and plant responses to salinity stress: a review. Plant Growth Regul 75(2):391–404
Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45
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
Himmelbach A, Yang Y, Grill E (2003) Relay and control of abscisic acid signaling. Curr Opin Plant Biol 6:470–479
Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA 96:15348–15353
Hui D, Iqbal J, Lehmann K, Gase K, Saluz HP, Baldwin IT (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata: V. microarray analysis and further characterization of large-scale changes in herbivore-induced mRNAs. Plant Physiol 131:1877–1893
Jiang Y, Duan Y, Yin J, Ye S, Zhu J, Zhang F, Lu W, Fan D, Luo K (2014) 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 65(22):6629–6644
Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357
Kizis D, Lumbreras V, Pagès M (2001) Role of AP2/EREBP transcription factors in gene regulation during abiotic stress. FEBS Lett 498:187–189
Robatzek S, Somssich IE (2001) A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence-and defence-related processes. Plant J 28(2):123–133
Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417
Singh K, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5(5):430–436
Song Y, Chen L, Zhang L, Yu D (2010) Overexpression of OsWRKY72 gene interferes in the ABA signal and auxin transport pathway of Arabidopsis. J Biosci 35:459–471
Sun C, Palmqvist S, Olsson H, Borén M, Ahlandsberg S, Jansson C (2003) A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar-responsive elements of the iso1 promoter. Plant Cell 15:2076–2092
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
Taylor S, Wakem M, Dijkman G, Alsarraj M, Nguyen M (2010) A practical approach to RT-qPCR-publishing data that conform to the MIQE guidelines. Methods 50:S1–S5
Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604
Ulker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7(5):494–498
Ulker B, Shahid Mukhtar M, Somssich IE (2007) The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways. Planta 226(1):125–137
Vision TJ, Brown DG, Tanksley SD (2000) The origins of genomic duplications in Arabidopsis. Science 290:2114–2117
Wang S, Wang J, Yao W, Zhou B, Li R, Jiang T (2014) Expression patterns of WRKY genes in di-haploid Populus simonii × P. nigra in response to salinity stress revealed by quantitative real-time PCR and RNA sequencing. Plant Cell Rep 33:1687–1696
Wu KL, Guo ZJ, Wang HH, Li J (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12:9–26
Xu YH, Wang JW, Wang S, Wang JY, Chen XY (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-delta-cadinene synthase-A. Plant Physiol 135:507–515
Ying S, Zhang DF, Fu J, Shi YS, Song YC, Wang TY, Li Y (2012) Cloning and characterization of a maize bZIP transcription factor, ZmbZIP72, confers drought and salt tolerance in transgenic Arabidopsis. Planta 235:253–266
Zhang H, Huang Z, Xie B, Chen Q, Tian X, Zhang X, Zhang H, Lu X, Huang D, Huang R (2004) The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco. Planta 220:262–270
Zhang H, Jin J, Tang L, Zhao Y, Gu X, Gao G, Luo J (2011) PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res 39:D1114–D1117
Zhao J, Wang J, An L, Doerge RW, Chen ZJ, Grau CR, Meng J, Osborn TC (2007) Analysis of gene expression profiles in response to Sclerotinia sclerotiorum in Brassica napus. Planta 227(1):13–24
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 6:486–503
Zhu JK (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4(5):401–406
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This work was supported by the National Hi-Tech Research and Development Program of China (2013AA102701) and the Fundamental Research Funds for The Central Universities (2572015AA06).
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Wang, S., Wang, J., Yao, W. et al. Expression patterns of WRKY genes in di-haploid Populus simonii × P. nigra in response to osmotic stress and ABA treatment. Plant Growth Regul 78, 325–333 (2016). https://doi.org/10.1007/s10725-015-0095-1
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DOI: https://doi.org/10.1007/s10725-015-0095-1