Research Progress on Function Analysis of Rice WRKY Genes

doi:10.3969/j.issn.10017216.2009.05.01

Abstract

Abstract: WRKY DNA binding transcription factors play pivotal roles in the regulation of plant development, substance metabolism, resistance, and senescence. Based on the clear genome of rice, studies on WRKY gene function are dramatically enhanced nowadays. And several evidences implicate WRKY factors in transcriptional reprogramming during rice resistance response, senescence process, sugar metabolism, and plant architecture. In addition, previous nomenclature of rice WRKY proteins was confusing. Therefore it is necessary to collate the corresponding WRKY proteins and review the recent progress of WRKY protein research.

Key words: rice, WRKY gene, transcription factor, gene function

摘要： WRKY转录调控因子的生物学功能涉及植物生长发育、物质代谢、抗病耐逆、氧化衰老等诸多方面。水稻全基因组测序完成后，水稻WRKY转录调控因子基因的功能研究随之逐渐开展，目前已经发现它在植物抗病、耐逆、衰老、糖代谢以及形态建成方面发挥重要作用。随着研究的深入，水稻WRKY基因的编号未能统一，很容易让人混淆，有必要进行校正。结合作者实验室的一些研究结果，对水稻WRKY基因家族的研究现状进行了综述，以期为进一步深入开展WRKY基因家族的研究提供帮助。

关键词: 水稻, WRKY基因, 转录调控因子, 基因功能

SONG Yu ,JING Shaojuan ,YU Di-qiu . Research Progress on Function Analysis of Rice WRKY Genes[J]. Chinese Journal of Rice Science, DOI: 10.3969/j.issn.10017216.2009.05.01 .

宋钰, 荆邵娟, 余迪求,. 水稻WRKY转录调控因子基因功能研究进展[J]. 中国水稻科学, DOI: 10.3969/j.issn.10017216.2009.05.01 .

References

[1]Yu J, Wang J, Lin W, et al. The genomes of Oryza sativa: A history of duplications. PLoS Biol, 2005, 3(2): 266-281.

[2]Xiong Y Q, Liu T Y, Tian C G, et al. Transcription factors in rice: A genomewide comparative analysis between monocots and eudicots. Plant Mol Biol, 2005, 59: 191-203.

[3]Qu L J, Zhu Y X. Transcription factor families in Arabidopsis: Major progress and outstanding issues for future research. Curr Opin Plant Biol, 2006, 9(5): 544-549.

[4]Eulgem T, Rushton P J, Robatzek S, et al. The WRKY superfamily of plant transcription factors. Trends Plant Sci, 2000, 5: 199-206.

[5]Qiu Y P, Jing S J, Fu J, et al. Cloning and analysis of expression profile of 13 WRKY genes in rice. Chin Sci Bull, 2004, 49(20): 2159-2168.

[6]Ciolkowski I, Wanke D, Birkenbihl R P, et al. Studies on DNAbinding selectivity of WRKY transcription factors lend structural clues into WRKYdomain function. Plant Mol Biol, 2008, 68(1/2): 81-92.

[7]Ramamoorthy R, Jiang S Y, Kumar N, et al. A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol, 2008, 49(6): 865-879.

[8]Wu K L, Guo Z J, Wang H H, et al. The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res, 2005, 12(1): 9-26.

[9]Kim C Y, Lee S H, Park H C, et al. Identification of rice blast fungal elicitorresponsive genes by differential display analysis. Mol Plant Microbe Interact, 2000, 13(4): 470-474.

[10]Shimizu T, Satoh K, Kikuchi S, et al. The repression of cell wall and plastidrelated genes and the induction of defenserelated genes in rice plants infected with rice dwarf virus. Mol Plant Microbe Interact, 2007, 20(3): 247-254.

[11]Ryu H S, Han M, Lee S K, et al. A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep, 2006, 25(8): 836-847.

[12]Chujo T, Takai R, AkimotoTomiyama C, et al. Involvement of the elicitorinduced gene OsWRKY53 in the expression of defenserelated genes in rice. Biochim Biophys Acta, 2007, 1769(7/8): 497-505.

[13]Shimono M, Sugano S, Nakayama A, et al. Rice WRKY45 plays a crucial role in benzothiadiazoleinducible blast resistance. Plant Cell, 2007, 19(6): 2064-2076.

[14]Qiu Y P, Yu D Q. Overexpression of the stressinduced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ & Exp Bot, 2009, 65(1): 25-47.

[15]Wu X L, Shiroto Y, Kishitani S, et al. 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.

[16]Jing S J, Zhou X, Song Y, et al. Heterologous expression of OsWRKY23 gene enhances pathogen defense and cell senescence in Arabidopsis. Plant Growth Regul, 2009, 58(2): 181-190.

[17]Sperotto R A, Boff T, Duarte G L, et al. Increased senescenceassociated gene expression and lipid peroxidation induced by iron deficiency in rice roots. Plant Cell Rep, 2008, 27(1): 183-195.

[18]Liu L, Zhou Y, Zhou G, et al. Identification of early senescenceassociated genes in rice flag leaves. Plant Mol Biol, 2008, 67(1/2): 37-55.

[19]宋钰, 刘冬梅, 余迪求. 高表达水稻WRKY72基因影响拟南芥生长素信号传导. 云南植物研究, 2008, 30(6): 699-705.

[20]Zhang J, Peng Y L, Guo Z J. Constitutive expression of pathogeninducible OsWRKY31 enhances disease resistance and affects root growth and auxin response in transgenic rice plants. Cell Res, 2008, 18: 508-521.

[21]Zhang Z L, Xie Z, Zou X L, et al. A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol, 2004, 134(4): 1500-1513.

[22]Xie Z, Zhang Z L, Zou X L, et al. Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol, 2005, 137(1): 176-189.

[23]Zhang Y J, Wang L J. The WRKY transcription factor superfamily: Its origin in eukaryotes and expansion in plants. BMC Evol Biol, 2005, 5(1): 1-12.

[24]Ross C A, Liu Y, Shen Q X J. The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol, 2007, 49(6): 827-842.

[25]Eulgem T, Somssich I E. Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol, 2007, 10(4): 366-371.

[26]Liu X Q, Bai X Q, Qian Q, et al. OsWRKY03, a rice transcriptional activator that functions in defense signaling pathway upstream of OsNPR1. Cell Res, 2005, 15(8): 593-603.

[27]Qiu D Y, Xiao J, Ding X H, et al. OsWRKY13 mediates rice disease resistance by regulating defenserelated genes in salicylate and jasmonatedependent signaling. Mol Plant Microbe Interact, 2007, 20(5): 492-499.

[28]Liu X Q, Bai X Q, Wang X J, et al. OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol, 2007, 164(8): 969-979.

[29]Chujo T, Kato T, Yamada K, et al. Characterization of an elicitorinduced rice WRKY gene, OsWRKY71. Biosci Biotech Biochem, 2008, 72(1): 240-245.

[30]Wang H H, Hao J J, Chen X J, et al. Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant Mol Biol, 2007, 65(6): 799-815.

[31]Chujo T, Takai R, Kaku H, et al. Isolation and characterization of two elicitorresponsive genes encoding WRKY DNAbinding proteins from rice. Plant Cell Physiol, 2004, 45: S51-S51.

[32]Chujo T, Okada K, Kaku I, et al. Characterization of elicitorresponsive genes encoding WRKY DNAbinding proteins from rice. Plant Cell Physiol, 2005, 46: S175-S175.

[33]Chujo T, Takai R, Minami E, et al. Characterization of elicitorresponsive WRKY transcription factor, OsWRKY71, from rice. Plant Cell Physiol, 2006, 47: S82-S82.

[34]Shimono M, Sugano S, Jiang C J, et al. A WRKY transcription factor plays a role in BTHinducible disease resistance in rice. Plant Cell Physiol, 2006, 47: S83-S83.

[35]Wen N, Chu Z, Wang S. Three types of defenseresponsive genes are involved in resistance to bacterial blight and fungal blast diseases in rice. Mol Genet Gen, 2003, 269(3): 331-339.

[36]Cao Y L, Ding X H, Cai M, et al. The expression pattern of a rice disease resistance gene Xa3/Xa26 is differentially regulated by the genetic backgrounds and developmental stages that influence its function. Gene, 2007, 177: 523-533.

[37]Cai M, Qiu D Y, Yuan T, et al. Identification of novel pathogenresponsive ciselements and their binding proteins in the promoter of OsWRKY13, a gene regulating rice disease resistance. Plant Cell Environ, 2008, 31(1): 86-96.

[38]Gloria M C. Analysis of the interaction transcriptome during biotrophic invasion by the blast fungus, Magnaporthe oryzae[PhD dissertation]. Kansas, USA: Kansas State University, 2007: 88-90.

[39]Wang H H, Xie K, Wu K L, et al. Isolation of a rice WRKY gene OsWRKY52, whose expression is induced by Magnaporthe grisea. Prog Biochem Biophys, 2005, 32(10): 937-946.

[40]Swarbrick P J, Huang K, Liu G, et al. Global patterns of gene expression in rice cultivars undergoing a susceptible or resistant interaction with the parasitic plant Striga hermonthica. New Phytol, 2008, 179(2): 515-529.

[41]Marè C, Mazzucotelli E, Crosatti C, et al. HvWRKY38: A new transcription factor involved in cold and droughtresponse in barley. Plant Mol Biol, 2004, 55(3): 399-416.

[42]Zou X L, Shen Q X J, Neuman D. An ABA inducible WRKY gene integrates responses of creosote bush (Larrea tridentata) to elevated CO2 and abiotic stresses. Plant Sci, 2007, 172(5): 997-1004.

[43]Robatzek S, Somssich I E. A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence and defenserelated processes. Plant J, 2001, 28(2): 123-133.

[44]Miao Y, Laun T, Zimmermann P, et al. Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol, 2004, 55(6): 853-867.

[45]Ulker B, Mukhtar M S, Somssich I E. The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways. Planta, 2007, 226(1): 125-137.

[46]Ishiguro S, Nakamura K. Characterization of a cDNAencoding a novel DNAbinding protein, SPF1, that recognizes Sp8 sequences in the 5′upstream regions of genescoding for sporamin and betaamylase from sweetpotato. Mol Gen Genet, 1994, 244(6): 563-571.

[47]Sun C X, Palmqvist S, Olsson H, et al. 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, 2003, 15(9): 2076-2092.

[48]Xie Z, Zhang Z L, Hanzlik S, et al. Salicylic acid inhibits gibberellininduced alphaamylase expression and seed germination via a pathway involving an abscisicacidinducible WRKY gene. Plant Mol Biol, 2007, 64(3): 293-303.

[49]Zhang Z L, Shin M, Zou X, et al. A negative regulator encoded by a rice WRKY gene represses both abscisic acid and gibberellins signaling in aleurone cells. Plant Mol Biol, 2009, 10 70(1/2): 139-151.

[50]Xie Z, Zhang Z L, Zou X L, et al. Interactions of two abscisicacid induced WRKY genes in repressing gibberellin signaling in aleurone cells. Plant J, 2006, 46(2): 231-242.

[51]Wang H J, Wan A R, Hsu C M, et al. Transcriptomic adaptations in rice suspension cells under sucrose starvation. Plant Mol Biol, 2007, 63(4): 441-463.

[52]Johnson C S, Kolevski B, Smyth D R. TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell, 2002, 14(6): 1359-1375.

[53]Ishida T, Hattori S, Sano R, et al. Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell, 2007, 19(8): 2531-2543.

[54]Devaiah B N, Karthikeyan A S, Raghothama K G. WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol, 2007, 143(4): 1789-1801.

[55]Dai Y, Wang H Z, Li B H, et al. Increased expression of MAP KINASE KINASE7 causes deficiency in polar auxin transport and leads to plant architectural abnormality in Arabidopsis. Plant Cell, 2006, 18(2): 308-320.

[56]Sun C X, Hglund A S, Olsson H, et al. Antisense oligodeoxynucleotide inhibition as a potent strategy in plant biology: Identification of SUSIBA2 as a transcriptional activator in plant sugar signaling. Plant J, 2005, 44(1): 128-138.

[57]Yuan Y X, Zhong S H, Li Q, et al. Functional analysis of rice NPR1like genes reveals that OsNPR1/NH1 is the rice ortholog conferring disease resistance with enhanced herbivore susceptibility. Plant Biotech J, 2007, 5(2): 313-324.

[58]Nemoto T, Okada A, Okada K, et al. Promoter analysis of the rice stemar13ene synthase gene OsDTC2, which is involved in the biosynthesis of the phytoalexin oryzalexin S. Biochim Biophys Acta, 2007, 1769(11/12): 678-683.

[59]Ulker B, Somssich I E. WRKY transcription factors: From DNA binding towards biological function. Curr Opin Plant Biol, 2004, 7(5): 491-498.

[60]Grunewald W, Karimi M, Wieczorek K, et al. A role for AtWRKY23 in feeding site establishment of plantparasitic nematodes. Plant Physiol, 2008, 148(1): 358-368.

[61]Skibbe M, Qu N, Galis I, et al. Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell, 2008, 20(7): 1984-2000.

[62]Miller G, Shulaev V, Mittler R. Reactive oxygen signaling and abiotic stress. Physiol Plant, 2008, 133(3): 481-489.

[63]Contento A L, Kim S J, Bassham D C. Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation. Plant Physiol, 2004, 135(4): 2330-2347.

[64]Palmieri M C, Sell S, Huang X, et al. Nitric oxideresponsive genes and promoters in Arabidopsis thaliana: A bioinformatics approach. J Exp Bot, 2008, 59(2): 177-186.

[65]Nemhauser J L, Hong F X, Chory J. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell, 2006, 126(3): 467-475.