Abstract
Key message
OsWRKY28 confers salinity tolerance by directly binding to OsDREB1B promoter and increasing its transcriptional activity, and negatively regulates abscisic acid mediated seedling establishment in rice.
Abstract
WRKY transcription factors have been reported to play a vital role in plants growth, development, abiotic and biotic stress responses. In this study, we explored the functions of a transcription factor OsWRKY28 in rice. The transcript level of OsWRKY28 was strikingly increased under drought, chilling, salt and abscisic acid treatments. The OsWRKY28 overexpression lines showed enhanced salinity stress tolerance, whereas the oswrky28 mutants displayed salt sensitivity compared to wild-type plants. Under salt stress treatment, the expression levels of OsbZIP05, OsHKT1;1 and OsDREB1B were significantly lower yet the level of OsHKT2;1 was significantly higher in oswrky28 mutants than those in wide type plants. Our data of yeast one-hybrid assay and dual-luciferase assay supported that OsWRKY28 could directly bind to the promoter of OsDREB1B to enhance salinity tolerance in rice. In addition, OsWRKY28 overexpression lines displayed hyposensitivity and the oswrky28 mutants showed hypersensitivity compared to wild-type plants under exogenous abscisic acid treatment. Based on the results of yeast two-hybrid assay and GAL4-dependent chimeric transactivation assay, OsWRKY28 physically interacts with OsMPK11 and its transcriptional activity could be regulated by OsMPK11. Together, OsWRKY28 confers salinity tolerance through directly targeting OsDREB1B promoter and further activating its transcription in rice.
Similar content being viewed by others
Data availability
Data supporting the findings of this work are available within the article and its Supporting Information files.
Abbreviations
- ABA:
-
Abscisic acid
- cDNA:
-
Complementary DNA
- CDS:
-
Coding sequence
- DREB:
-
Dehydration responsive element binding
- FLUC:
-
Firefly luciferase
- GA:
-
Gibberellin
- MAPK:
-
Mitogen-activated protein kinase
- MS:
-
Murashige and Skoog
- PEG:
-
Polyethylene glycol
- QRT-PCR:
-
Quantitative reverse transcription PCR
- RLUC:
-
Renilla luciferase
- ROS:
-
Reactive oxygen species
- TF:
-
Transcription factors
- WT:
-
Wild type
References
Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274
Bakshi M, Oelmuller R (2014) WRKY transcription factors: Jack of many trades in plants. Plant Signal Behav 9:e27700–e27700
Chen L, Zhao Y, Xu S, Zhang Z, Xu Y, Zhang J, Chong K (2018) OsMADS57 together with OsTB1 coordinates transcription of its target OsWRKY94 and D14 to switch its organogenesis to defense for cold adaptation in rice. New Phytol 218:219–231
Chujo T, Miyamoto K, Shimogawa T, Shimizu T, Otake Y, Yokotani N, Nishizawa Y, Shibuya N, Nojiri H, Yamane H, Minami E, Okada K (2013) OsWRKY28, a PAMP-responsive transrepressor, negatively regulates innate immune responses in rice against rice blast fungus. Plant Mol Biol 82:23–37
Danquah A, de Zelicourt A, Colcombet J, Hirt H (2014) The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol Adv 32:40–52
Deng X, Xu X, Liu Y, Zhang Y, Yang L, Zhang S, Xu J (2020) Induction of γ-aminobutyric acid plays a positive role to Arabidopsis resistance against Pseudomonas syringae. J Integr Plant Biol 62:1797–1812
Guo X, Hou X, Fang J, Wei P, Xu B, Chen M, Feng Y, Chu C (2013) The rice GERMINATION DEFECTIVE 1, encoding a B3 domain transcriptional repressor, regulates seed germination and seedling development by integrating GA and carbohydrate metabolism. Plant J 75:403–416
Gutha LR, Reddy AR (2008) Rice DREB1B promoter shows distinct stress-specific responses, and the overexpression of cDNA in tobacco confers improved abiotic and biotic stress tolerance. Plant Mol Biol 68:533–555
Hamel L-P, Nicole M-C, Sritubtim S, Morency M-J, Ellis M, Ehlting J, Beaudoin N, Barbazuk B, Klessig D, Lee J, Martin G, Mundy J, Ohashi Y, Scheel D, Sheen J, Xing T, Zhang S, Seguin A, Ellis BE (2006) Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci 11:192–198
Hauser F, Horie T (2010) A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant Cell Environ 33:552–565
Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282
Hou Y, Wang Y, Tang L, Tong X, Wang L, Liu L, Huang S, Zhang J (2019) SAPK10-mediated phosphorylation on WRKY72 releases its suppression on jasmonic acid biosynthesis and bacterial blight resistance. Iscience 16:499–510
Hu L, Ye M, Li R, Zhang T, Zhou G, Wang Q, Lu J, Lou Y (2015) The rice transcription factor WRKY53 suppresses herbivore-induced defenses by acting as a negative feedback modulator of mitogen-activated protein kinase activity. Plant Physiol 169:2907–2921
Huai J, Zhang X, Li J, Ma T, Zha P, Jing Y, Lin R (2018) SEUSS and PIF4 coordinately regulate light and temperature signaling pathways to control plant growth. Mol Plant 11:928–942
Huang K, Wu T, Ma Z, Li Z, Chen H, Zhang M, Bian M, Bai H, Jiang W, Du X (2021a) Rice transcription factor OsWRKY55 is involved in the drought response and regulation of plant growth. Int J Mol Sci 22:4337
Huang S, Hu L, Zhang S, Zhang M, Jiang W, Wu T, Du X (2021b) Rice OsWRKY50 mediates ABA-dependent seed germination and seedling growth, and ABA-independent salt stress tolerance. Int J Mol Sci 22:16
Jiang J, Ma S, Ye N, Jiang M, Cao J, Zhang J (2017) WRKY transcription factors in plant responses to stresses. J Integr Plant Biol 59:86–101
Joshi R, Wani SH, Singh B, Bohra A, Dar ZA, Lone AA, Pareek A, Singla-Pareek SL (2016) Transcription factors and plants response to drought stress: current understanding and future directions. Front Plant Sci 7:1029
Kaashyap M, Ford R, Bohra A, Kuvalekar A, Mantri N (2017) Improving salt tolerance of chickpea using modern genomics tools and molecular breeding. Curr Genomics 18:557–567
Kang G, Yan D, Chen X, Li Y, Yang L, Zeng R (2020) Molecular characterization and functional analysis of a novel WRKY transcription factor HbWRKY83 possibly involved in rubber production of Hevea brasiliensis. Plant Physiol Bioch 155:483–493
Kim C-Y, Kieu Thi Xuan V, Cong Danh N, Jeong D-H, Lee S-K, Kumar M, Kim S-R, Park S-H, Kim J-K, Jeon J-S (2016) Functional analysis of a cold-responsive rice WRKY gene, OsWRKY71. Plant Biotechnol Rep 10:13–23
Lan J, Lin Q, Zhou C, Ren Y, Liu X, Miao R, Jing R, Mou C, Nguyen T, Zhu X, Wang Q, Zhang X, Guo X, Liu S, Jiang L, Wan J (2020) Small grain and semi-dwarf 3, a WRKY transcription factor, negatively regulates plant height and grain size by stabilizing SLR1 expression in rice. Plant Mol Biol 104:429–450
Li Z, Fu D, Wang X, Zeng R, Zhang X, Tian J, Zhang S, Yang X, Tian F, Lai J, Shi Y, Yang S (2022) The transcription factor bZIP68 negatively regulates cold tolerance in maize. Plant Cell 34:2833–2851
Lim C, Kang K, Shim Y, Yoo S-C, Paek N-C (2022) Inactivating transcription factor OsWRKY5 enhances drought tolerance through abscisic acid signaling pathways. Plant Physiol 188:1900–1916
Lin R, Ding L, Casola C, Ripoll DR, Feschotte C, Wang H (2007) Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science 318:1302–1305
Liu M, Wang J, Gou J, Wang X, Li Z, Yang X, Sun S (2020) Overexpression of NtSnRK2.2 enhances salt tolerance in Nicotiana tabacum by regulating carbohydrate metabolism and lateral root development. Funct Plant Biol 47:537–543
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408
Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R, Wang B, Yang Z, Li H, Lin Y, Xie Y, Shen R, Chen S, Wang Z, Chen Y, Guo J, Chen L, Zhao X, Dong Z, Liu Y-G (2015) A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant 8:1274–1284
Machens F, Becker M, Umrath F, Hehl R (2014) Identification of a novel type of WRKY transcription factor binding site in elicitor-responsive cis-sequences from Arabidopsis thaliana. Plant Mol Biol 84:371–385
Mao D, Xin Y, Tan Y, Hu X, Bai J, Liu Z-y, Yu Y, Li L, Peng C, Fan T, Zhu Y, Guo Y-l, Wang S, Lu D, Xing Y, Yuan L, Chen C (2019) Natural variation in the HAN1 gene confers chilling tolerance in rice and allowed adaptation to a temperate climate. P Natl Acad Sci USA 116:3494–3501
Mukherjee K, Choudhury AR, Gupta B, Gupta S, Sengupta DN (2006) An ABRE-binding factor, OSBZ8, is highly expressed in salt tolerant cultivars than in salt sensitive cultivars of indica rice. Bmc Plant Biol 6:18
Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci 10:339–346
Peng Y, Bartley LE, Chen X, Dardick C, Chern M, Ruan R, Canlas PE, Ronald PC (2008) OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice. Mol Plant 1:446–458
Phukan UJ, Jeena GS, Shukla RK (2016) WRKY transcription factors: molecular regulation and stress responses in plants. Front Plant Sci 7:760
Qin Y, Tian Y, Liu X (2015) A wheat salinity-induced WRKY transcription factor TaWRKY93 confers multiple abiotic stress tolerance in Arabidopsis thaliana. Biochem Bioph Res Co 464:428–433
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258
Shen H, Liu C, Zhang Y, Meng X, Zhou X, Chu C, Wang X (2012) OsWRKY30 is activated by MAP kinases to confer drought tolerance in rice. Plant Mol Biol 80:241–253
Ueno Y, Yoshida R, Kishi-Kaboshi M, Matsushita A, Jiang CJ, Goto S, Takahashi A, Hirochika H, Takatsuji H (2015) Abiotic stresses antagonize the rice defence pathway through the tyrosine-dephosphorylation of OsMPK6. PLoS Pathog 11:e1005231
Wang R, Jing W, Xiao L, Jin Y, Shen L, Zhang W (2015) The rice high-affinity potassium transporter1;1 is involved in salt tolerance and regulated by an MYB-type transcription factor. Plant Physiol 168:1076–1090
Wang P, Xu X, Tang Z, Zhang W, Huang X, Zhao F (2018) OsWRKY28 regulates phosphate and arsenate accumulation, root system architecture and fertility in rice. Front Plant Sci 9:1330
Wei H, Wang X, He Y, Xu H, Wang L (2021) Clock component OsPRR73 positively regulates rice salt tolerance by modulating OsHKT2;1-mediated sodium homeostasis. EMBO J 40:e105086
Xiong L, Schumaker KS, Zhu J (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(Suppl):S165-183
Yan L, Zhang H, Zheng Y, Cong Y, Liu C, Fan F, Zheng C, Yuan G, Pan G, Yuan D, Duan M (1800) Transcription factor OsMADS25 improves rice tolerance to cold stress. Yi Chuan 43:1078–1087
Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, Okada K, Yamane H, Shimono M, Sugano S, Takatsuji H, Kaku H, Minami E, Nishizawa Y (2013) WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot 64:5085–5097
Zhang C, Liu J, Zhao T, Gomez A, Li C, Yu C, Li H, Lin J, Yang Y, Liu B, Lin C (2016) A drought-inducible transcription factor delays reproductive timing in rice. Plant Physiol 171:334–343
Zhang G, Xu N, Chen H, Wang G, Huang J (2018) OsMADS25 regulates root system development via auxin signalling in rice. Plant J 95:1004–1022
Zhang M, Zhao R, Huang K, Huang S, Wang H, Wei Z, Li Z, Bian M, Jiang W, Wu T, Du X (2022) The OsWRKY63-OsWRKY76-OsDREB1B module regulates chilling tolerance in rice. Plant J 112:383–398
Zhou C, Lin Q, Lan J, Zhang T, Liu X, Miao R, Mou C, Nguyen T, Wang J, Zhang X, Zhou L, Zhu X, Wang Q, Zhang X, Guo X, Liu S, Jiang L, Wan J (2020) WRKY transcription factor OsWRKY29 represses seed dormancy in rice by weakening abscisic acid response. Front Plant Sci 11:691
Zhu J (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324
Zhu H, Zhou Y, Zhai H, He S, Zhao N, Liu Q (2020) A novel sweetpotato WRKY transcription factor, IbWRKY2, positively regulates drought and salt tolerance in transgenic Arabidopsis. Biomolecules 10:506
Acknowledgements
This research was supported by Science and Technology Development Plan of Jilin Province, China (20210302008NC) and National Natural Science Foundation of China (31701396 and 32101664).
Funding
National Natural Science Foundation of China, 31701396, Tao Wu, 32101664, Shuangzhan Huang, Jilin Scientific and Technological Development Program, 20210302008NC, Xinglin Du
Author information
Authors and Affiliations
Contributions
TW and XD designed the study; ZM, RZ, HW, SR, LS, ZW, BG, and JJ executed the experiments; SH, YZ and MC analyzed the data; ZM and RZ wrote the manuscript; XD, TW, and WJ modified the manuscript. All authors have read and agreed to the published version of the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors claim no conflicts of interest.
Additional information
Communicated by Zheng-Yi Xu.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, M., Zhao, R., Wang, H. et al. OsWRKY28 positively regulates salinity tolerance by directly activating OsDREB1B expression in rice. Plant Cell Rep 42, 223–234 (2023). https://doi.org/10.1007/s00299-022-02950-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-022-02950-2