Hichri, Imène
[UCL]
Muhovski, Yordan
[Département Sciences du Vivant, Centre Wallon de Recherches Agronomiques, Gembloux, Belgium,]
Zizkova, Eva
[Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Prague, Czechia]
Dobre, Petre
[Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Prague, Czechia]
Gharbi, Emna
[UCL]
Lutts, Stanley
[UCL]
Salinity threatens productivity of economically important crops such as tomato (Solanum lycopersicum L.). WRKY transcription factors appear, from a growing body of knowledge, as important regulators of abiotic stresses tolerance. Tomato SlWRKY3 is a nuclear protein binding to the consensus CGTTGACC/T W box. SlWRKY3 is preferentially expressed in aged organs, and is rapidly induced by NaCl, KCl, and drought. In addition, SlWRKY3 responds to salicylic acid, and 35S::SlWRKY3 tomatoes showed under salt treatment reduced contents of salicylic acid. In tomato, overexpression of SlWRKY3 impacted multiple aspects of salinity tolerance. Indeed, salinized (125 mM NaCl, 20 days) 35S::SlWRKY3 tomato plants displayed reduced oxidative stress and proline contents compared to WT. Physiological parameters related to plant growth (shoot and root biomass) and photosynthesis (stomatal conductance and chlorophyll a content) were retained in transgenic plants, together with lower NaC contents in leaves, and higher accumulation of KC and Ca2C. Microarray analysis confirmed that many stress-related genes were already up-regulated in transgenic tomatoes under optimal conditions of growth, including genes coding for antioxidant enzymes, ion and water transporters, or plant defense proteins. Together, these results indicate that SlWRKY3 is an important regulator of salinity tolerance in tomato.
Agarwal Parinita, Dabi Mitali, Sapara Komal K., Joshi Priyanka S., Agarwal Pradeep K., Ectopic Expression of JcWRKY Transcription Factor Confers Salinity Tolerance via Salicylic Acid Signaling, 10.3389/fpls.2016.01541
Albacete, J. Exp. Bot., 59, 4119 (2008)
Banerjee Aditya, Roychoudhury Aryadeep, WRKY Proteins: Signaling and Regulation of Expression during Abiotic Stress Responses, 10.1155/2015/807560
Bates L. S., Waldren R. P., Teare I. D., Rapid determination of free proline for water-stress studies, 10.1007/bf00018060
Berri Stefano, Abbruscato Pamela, Faivre-Rampant Odile, Brasileiro Ana CM, Fumasoni Irene, Satoh Kouji, Kikuchi Shoshi, Mizzi Luca, Morandini Piero, Pè Mario, Piffanelli Pietro, Characterization of WRKY co-regulatory networks in rice and Arabidopsis, 10.1186/1471-2229-9-120
Chang Wenjun, Liu Xiwen, Zhu Jiahong, Fan Wei, Zhang Zhili, An aquaporin gene from halophyte Sesuvium portulacastrum, SpAQP1, increases salt tolerance in transgenic tobacco, 10.1007/s00299-015-1891-9
Chen Ligang, Song Yu, Li Shujia, Zhang Liping, Zou Changsong, Yu Diqiu, The role of WRKY transcription factors in plant abiotic stresses, 10.1016/j.bbagrm.2011.09.002
Chu Xiaoqian, Wang Chen, Chen Xiaobo, Lu Wenjing, Li Han, Wang Xiuling, Hao Lili, Guo Xingqi, The Cotton WRKY Gene GhWRKY41 Positively Regulates Salt and Drought Stress Tolerance in Transgenic Nicotiana benthamiana, 10.1371/journal.pone.0143022
Ciolkowski Ingo, Wanke Dierk, Birkenbihl Rainer P., Somssich Imre E., Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function, 10.1007/s11103-008-9353-1
Clough Steven J., Bent Andrew F., Floral dip: a simplified method forAgrobacterium-mediated transformation ofArabidopsis thaliana : Floral dip transformation of Arabidopsis, 10.1046/j.1365-313x.1998.00343.x
Cuartero J., Bolarín M. C., Asíns M. J., Moreno V., Increasing salt tolerance in the tomato, 10.1093/jxb/erj102
Ding Zhong Jie, Yan Jing Ying, Xu Xiao Yan, Yu Di Qiu, Li Gui Xin, Zhang Shu Qun, Zheng Shao Jian, Transcription factor WRKY46 regulates osmotic stress responses and stomatal movement independently in Arabidopsis, 10.1111/tpj.12538
Ellul P., Garcia-Sogo B., Pineda B., Ríos G., Roig L., Moreno V., The ploidy level of transgenic plants in Agrobacterium-mediated transformation of tomato cotyledons (Lycopersicon esculentum L.Mill.) is genotype and procedure dependent, 10.1007/s00122-002-0928-y
Fan Xinqi, Guo Qi, Xu Peng, Gong YuanYong, Shu Hongmei, Yang Yang, Ni Wanchao, Zhang Xianggui, Shen Xinlian, Transcriptome-Wide Identification of Salt-Responsive Members of the WRKY Gene Family in Gossypium aridum, 10.1371/journal.pone.0126148
Godoy Marta, Franco-Zorrilla José M., Pérez-Pérez Julián, Oliveros Juan C., Lorenzo Óscar, Solano Roberto, Improved protein-binding microarrays for the identification of DNA-binding specificities of transcription factors : Protein-binding microarrays for DNA-binding specificities of TFs, 10.1111/j.1365-313x.2011.04519.x
Gong Xiaoqing, Zhang Jingyan, Hu Jianbing, Wang Wei, Wu Hao, Zhang Qinghua, Liu Ji-Hong, FcWRKY70, a WRKY protein ofFortunella crassifolia, functions in drought tolerance and modulates putrescine synthesis by regulating arginine decarboxylase gene : FcWRKY70 regulates putrescine synthesis, 10.1111/pce.12539
GostinÄar Cene, Turk Martina, PlemenitaÅ¡ Ana, Gunde-Cimerman Nina, The expressions of Î9-, Î12-desaturases and an elongase by the extremely halotolerant black yeastHortaea werneckiiare salt dependent, 10.1111/j.1567-1364.2009.00481.x
Guo Dongshu, Zhang Jinzhe, Wang Xinlei, Han Xiang, Wei Baoye, Wang Jianqiao, Li Boxun, Yu Hao, Huang Qingpei, Gu Hongya, Qu Li-Jia, Qin Genji, The WRKY Transcription Factor WRKY71/EXB1 Controls Shoot Branching by Transcriptionally RegulatingRAXGenes in Arabidopsis, 10.1105/tpc.15.00829
Hichri Imène, Heppel Simon C., Pillet Jérémy, Léon Céline, Czemmel Stefan, Delrot Serge, Lauvergeat Virginie, Bogs Jochen, The Basic Helix-Loop-Helix Transcription Factor MYC1 Is Involved in the Regulation of the Flavonoid Biosynthesis Pathway in Grapevine, 10.1093/mp/ssp118
Hichri Imène, Muhovski Yordan, Clippe André, Žižková Eva, Dobrev Petre I., Motyka Vaclav, Lutts Stanley, SlDREB2, a tomato dehydration-responsive element-binding 2 transcription factor, mediates salt stress tolerance in tomato and Arabidopsis : SlDREB2 mediates salt tolerance in tomato, 10.1111/pce.12591
Hichri I., Muhovski Y., i kova E., Dobrev P. I., Franco-Zorrilla J. M., Solano R., Lopez-Vidriero I., Motyka V., Lutts S., The Solanum lycopersicum Zinc Finger2 Cysteine-2/Histidine-2 Repressor-Like Transcription Factor Regulates Development and Tolerance to Salinity in Tomato and Arabidopsis, 10.1104/pp.113.225920
Hu Yanru, Chen Ligang, Wang Houping, Zhang Liping, Wang Fang, Yu Diqiu, Arabidopsis transcription factor WRKY8 functions antagonistically with its interacting partner VQ9 to modulate salinity stress tolerance, 10.1111/tpj.12159
Huang Shengxiong, Gao Yongfeng, Liu Jikai, Peng Xiaoli, Niu Xiangli, Fei Zhangjun, Cao Shuqing, Liu Yongsheng, Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum, 10.1007/s00438-012-0696-6
Jiang Yuanqing, Deyholos Michael K., Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses, 10.1007/s11103-008-9408-3
Karimi Mansour, Inzé Dirk, Depicker Ann, GATEWAY™ vectors for Agrobacterium-mediated plant transformation, 10.1016/s1360-1385(02)02251-3
Kim K.-C., Lai Z., Fan B., Chen Z., Arabidopsis WRKY38 and WRKY62 Transcription Factors Interact with Histone Deacetylase 19 in Basal Defense, 10.1105/tpc.107.055566
Li Huie, Xu Yan, Xiao Yu, Zhu Ziguo, Xie Xiaoqing, Zhao Heqing, Wang Yuejin, Expression and functional analysis of two genes encoding transcription factors, VpWRKY1 and VpWRKY2, isolated from Chinese wild Vitis pseudoreticulata, 10.1007/s00425-010-1258-y
Li Jing-bin, Luan Yu-shi, Jin Hui, The tomato SlWRKY gene plays an important role in the regulation of defense responses in tobacco, 10.1016/j.bbrc.2012.09.120
Li Jing-bin, Luan Yu-shi, Liu Zhen, Overexpression ofSpWRKY1promotes resistance toPhytophthora nicotianaeand tolerance to salt and drought stress in transgenic tobacco, 10.1111/ppl.12315
Liu Qing-Lin, Zhong Ming, Li Shuang, Pan Yuan-Zhi, Jiang Bei-Bei, Jia Yin, Zhang Hai-Qing, Overexpression of a chrysanthemum transcription factor gene, DgWRKY3, in tobacco enhances tolerance to salt stress, 10.1016/j.plaphy.2013.04.016
Lu Yandu, Chi Xiaoyuan, Li Zhaoxin, Yang Qingli, Li Fuchao, Liu Shaofang, Gan Qinhua, Qin Song, Isolation and Characterization of a Stress-Dependent Plastidial Δ12 Fatty Acid Desaturase from the Antarctic Microalga Chlorella vulgaris NJ-7, 10.1007/s11745-009-3381-8
Lutts Stanley, Almansouri Malika, Kinet Jean-Marie, Salinity and water stress have contrasting effects on the relationship between growth and cell viability during and after stress exposure in durum wheat callus, 10.1016/j.plantsci.2004.02.014
LUTTS S, NaCl-induced Senescence in Leaves of Rice (Oryza sativaL.) Cultivars Differing in Salinity Resistance, 10.1006/anbo.1996.0134
Navarro Josefa M, Martı́nez Vicente, Carvajal Micaela, Ammonium, bicarbonate and calcium effects on tomato plants grown under saline conditions, 10.1016/s0168-9452(00)00272-7
Nie Lingling, Feng Juanjuan, Fan Pengxiang, Chen Xianyang, Guo Jie, Lv Sulian, Bao Hexigeduleng, Jia Weitao, Tai Fang, Jiang Ping, Wang Jinhui, Li Yinxin, Comparative proteomics of root plasma membrane proteins reveals the involvement of calcium signalling in NaCl-facilitated nitrate uptake inSalicornia europaea, 10.1093/jxb/erv216
NIU CAN-FANG, WEI WEI, ZHOU QI-YUN, TIAN AI-GUO, HAO YU-JUN, ZHANG WAN-KE, MA BIAO, LIN QING, ZHANG ZHENG-BIN, ZHANG JIN-SONG, CHEN SHOU-YI, Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants : Wheat WRKY genes in stress tolerance, 10.1111/j.1365-3040.2012.02480.x
Núñez-Ramírez Rafael, Sánchez-Barrena María José, Villalta Irene, Vega Juan F., Pardo Jose M., Quintero Francisco J., Martinez-Salazar Javier, Albert Armando, Structural Insights on the Plant Salt-Overly-Sensitive 1 (SOS1) Na+/H+ Antiporter, 10.1016/j.jmb.2012.09.015
ORELLANA SANDRA, YAÑEZ MÓNICA, ESPINOZA ANALÍA, VERDUGO ISABEL, GONZÁLEZ ENRIQUE, RUIZ-LARA SIMÓN, CASARETTO JOSÉ A., The transcription factor SlAREB1 confers drought, salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato : SlAREB1 confers stress tolerance in tomato, 10.1111/j.1365-3040.2010.02220.x
Ouyang Bo, Yang Ting, Li Hanxia, Zhang Liang, Zhang Yuyang, Zhang Junhong, Fei Zhangjun, Ye Zhibiao, Identification of early salt stress response genes in tomato root by suppression subtractive hybridization and microarray analysis, 10.1093/jxb/erl258
Pandey Girdhar K., Kanwar Poonam, Singh Amarjeet, Steinhorst Leonie, Pandey Amita, Yadav Akhlilesh K., Tokas Indu, Sanyal Sibaji K., Kim Beom-Gi, Lee Sung-Chul, Cheong Yong-Hwa, Kudla Jörg, Luan Sheng, Calcineurin B-Like Protein-Interacting Protein Kinase CIPK21 Regulates Osmotic and Salt Stress Responses in Arabidopsis, 10.1104/pp.15.00623
Parida Asish Kumar, Das Anath Bandhu, Salt tolerance and salinity effects on plants: a review, 10.1016/j.ecoenv.2004.06.010
P�rez-Alfocea F., Balibrea M. E., Cruz A. Santa, Esta� M. T., Agronomical and physiological characterization of salinity tolerance in a commercial tomato hybrid, 10.1007/bf00015308
Phukan Ujjal J., Jeena Gajendra S., Shukla Rakesh K., WRKY Transcription Factors: Molecular Regulation and Stress Responses in Plants, 10.3389/fpls.2016.00760
Qin Yuxiang, Tian Yanchen, Liu Xiuzhi, A wheat salinity-induced WRKY transcription factor TaWRKY93 confers multiple abiotic stress tolerance in Arabidopsis thaliana, 10.1016/j.bbrc.2015.06.128
Redmann R. E., Haraldson J., Gusta L. V., Leakage of UV-absorbing substances as a measure of salt injury in leaf tissue of woody species, 10.1111/j.1399-3054.1986.tb01267.x
Rinerson Charles I, Rabara Roel C, Tripathi Prateek, Shen Qingxi J, Rushton Paul J, The evolution of WRKY transcription factors, 10.1186/s12870-015-0456-y
Rinerson Charles I., Scully Erin D., Palmer Nathan A., Donze-Reiner Teresa, Rabara Roel C., Tripathi Prateek, Shen Qingxi J, Sattler Scott E., Rohila Jai S., Sarath Gautam, Rushton Paul J., The WRKY transcription factor family and senescence in switchgrass, 10.1186/s12864-015-2057-4
Rushton Paul J., Somssich Imre E., Ringler Patricia, Shen Qingxi J., WRKY transcription factors, 10.1016/j.tplants.2010.02.006
Schluttenhofer Craig, Yuan Ling, Regulation of Specialized Metabolism by WRKY Transcription Factors, 10.1104/pp.114.251769
Shen Yue, Shen Like, Shen Zhenxing, Jing Wen, Ge Hongliang, Zhao Jiangzhe, Zhang Wenhua, The potassium transporter OsHAK21 functions in the maintenance of ion homeostasis and tolerance to salt stress in rice : OsHAK21 involvement in responses to salt stress, 10.1111/pce.12586
Shi Weina, Hao Lili, Li Jing, Liu Dongdong, Guo Xingqi, Li Han, The Gossypium hirsutum WRKY gene GhWRKY39-1 promotes pathogen infection defense responses and mediates salt stress tolerance in transgenic Nicotiana benthamiana, 10.1007/s00299-013-1548-5
Song Hui, Wang Pengfei, Hou Lei, Zhao Shuzhen, Zhao Chuanzhi, Xia Han, Li Pengcheng, Zhang Ye, Bian Xiaotong, Wang Xingjun, Global Analysis of WRKY Genes and Their Response to Dehydration and Salt Stress in Soybean, 10.3389/fpls.2016.00009
Subramanian Chitra, Woo Jongchan, Cai Xue, Xu Xiaodong, Servick Stein, Johnson Carl H., Nebenführ Andreas, von Arnim Albrecht G., A suite of tools and application notes forin vivoprotein interaction assays using bioluminescence resonance energy transfer (BRET), 10.1111/j.1365-313x.2006.02851.x
Ülker Bekir, Somssich Imre E, WRKY transcription factors: from DNA binding towards biological function, 10.1016/j.pbi.2004.07.012
Vandesompele Jo, De Preter Katleen, Pattyn Filip, Poppe Bruce, Van Roy Nadine, De Paepe Anne, Speleman Frank, 10.1186/gb-2002-3-7-research0034
Volkmar K. M., Hu Y., Steppuhn H., Physiological responses of plants to salinity: A review, 10.4141/p97-020
Wang Chen, Deng Pengyi, Chen Liulin, Wang Xiatian, Ma Hui, Hu Wei, Yao Ningcong, Feng Ying, Chai Ruihong, Yang Guangxiao, He Guangyuan, A Wheat WRKY Transcription Factor TaWRKY10 Confers Tolerance to Multiple Abiotic Stresses in Transgenic Tobacco, 10.1371/journal.pone.0065120
Wang Fang, Chen Hao-Wei, Li Qing-Tian, Wei Wei, Li Wei, Zhang Wan-Ke, Ma Biao, Bi Ying-Dong, Lai Yong-Cai, Liu Xin-Lei, Man Wei-Qun, Zhang Jin-Song, Chen Shou-Yi, GmWRKY27 interacts with GmMYB174 to reduce expression ofGmNAC29for stress tolerance in soybean plants, 10.1111/tpj.12879
Wang Hua-Sen, Yu Chao, Tang Xian-Feng, Zhu Zhu-Jun, Ma Na-Na, Meng Qing-Wei, A tomato endoplasmic reticulum (ER)-type omega-3 fatty acid desaturase (LeFAD3) functions in early seedling tolerance to salinity stress, 10.1007/s00299-013-1517-z
Wang Lin, Li Qingtian, Lei Qiong, Feng Chao, Gao Yinan, Zheng Xiaodong, Zhao Yu, Wang Zhi, Kong Jin, MzPIP2;1: An Aquaporin Involved in Radial Water Movement in Both Water Uptake and Transportation, Altered the Drought and Salt Tolerance of Transgenic Arabidopsis, 10.1371/journal.pone.0142446
Wang Xiatian, Zeng Jian, Li Ying, Rong Xiaoli, Sun Jiutong, Sun Tao, Li Miao, Wang Lianzhe, Feng Ying, Chai Ruihong, Chen Mingjie, Chang Junli, Li Kexiu, Yang Guangxiao, He Guangyuan, Expression of TaWRKY44, a wheat WRKY gene, in transgenic tobacco confers multiple abiotic stress tolerances, 10.3389/fpls.2015.00615
Xiong Wangdan, Xu Xueqin, Zhang Lin, Wu Pingzhi, Chen Yaping, Li Meiru, Jiang Huawu, Wu Guojiang, Genome-wide analysis of the WRKY gene family in physic nut (Jatropha curcas L.), 10.1016/j.gene.2013.04.047
Yamasaki Kazuhiko, Kigawa Takanori, Watanabe Satoru, Inoue Makoto, Yamasaki Tomoko, Seki Motoaki, Shinozaki Kazuo, Yokoyama Shigeyuki, Structural Basis for Sequence-specific DNA Recognition by anArabidopsisWRKY Transcription Factor, 10.1074/jbc.m111.279844
Yang Li, Zhao Xin, Yang Fan, Fan Di, Jiang Yuanzhong, Luo Keming, PtrWRKY19, a novel WRKY transcription factor, contributes to the regulation of pith secondary wall formation in Populus trichocarpa, 10.1038/srep18643
Yang Qing, Chen Zhi-Zhong, Zhou Xiao-Feng, Yin Hai-Bo, Li Xia, Xin Xiu-Fang, Hong Xu-Hui, Zhu Jian-Kang, Gong Zhizhong, Overexpression of SOS (Salt Overly Sensitive) Genes Increases Salt Tolerance in Transgenic Arabidopsis, 10.1093/mp/ssn058
Song Yu, Chen Ligang, Zhang Liping, Yu Diqiu, Overexpression of OsWRKY72 gene interferes in the abscisic acid signal and auxin transport pathway of Arabidopsis, 10.1007/s12038-010-0051-1
Zhang Chang-Quan, Xu Yong, Lu Yan, Yu Heng-Xiu, Gu Ming-Hong, Liu Qiao-Quan, The WRKY transcription factor OsWRKY78 regulates stem elongation and seed development in rice, 10.1007/s00425-011-1423-y
Zhang Liyuan, Gu Lingkun, Ringler Patricia, Smith Stanley, Rushton Paul J., Shen Qingxi J., Three WRKY transcription factors additively repress abscisic acid and gibberellin signaling in aleurone cells, 10.1016/j.plantsci.2015.04.014
Zheng Lei, Liu Guifeng, Meng Xiangnan, Liu Yujia, Ji Xiaoyu, Li Yanbang, Nie Xianguang, Wang Yucheng, A WRKY gene from Tamarix hispida, ThWRKY4, mediates abiotic stress responses by modulating reactive oxygen species and expression of stress-responsive genes, 10.1007/s11103-013-0063-y
Zhou Li, Wang Na-Na, Gong Si-Ying, Lu Rui, Li Yang, Li Xue-Bao, Overexpression of a cotton ( Gossypium hirsutum ) WRKY gene, GhWRKY34 , in Arabidopsis enhances salt-tolerance of the transgenic plants, 10.1016/j.plaphy.2015.08.016
Zhou Qi-Yun, Tian Ai-Guo, Zou Hong-Feng, Xie Zong-Ming, Lei Gang, Huang Jian, Wang Chun-Mei, Wang Hui-Wen, Zhang Jin-Song, Chen Shou-Yi, Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants : Roles of GmWRKY genes in abiotic stress tolerance, 10.1111/j.1467-7652.2008.00336.x
Zhu Mingku, Chen Guoping, Zhang Jianling, Zhang Yanjie, Xie Qiaoli, Zhao Zhiping, Pan Yu, Hu Zongli, The abiotic stress-responsive NAC-type transcription factor SlNAC4 regulates salt and drought tolerance and stress-related genes in tomato (Solanum lycopersicum), 10.1007/s00299-014-1662-z
Bibliographic reference
Hichri, Imène ; Muhovski, Yordan ; Zizkova, Eva ; Dobre, Petre ; Gharbi, Emna ; et. al. The Solanum lycopersicum WRKY transcription factor SlWRKY3 is involved in salt stress tolerance in tomato. In: Frontiers in Plant Science, Vol. 8, no.1343, p. 18 p. (2017)