AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home The Crop Journal Article
PDF (2.5 MB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

ZmWRKY104 positively regulates salt tolerance by modulating ZmSOD4 expression in maize

Jingwei Yana,b,1, Jing Lia,1, Heping Zhanga, Ya Liua, Aying Zhanga,b( )
College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, Jiangsu, China
State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing 210095, Jiangsu, China

1 These authors contributed equally to this work.

Show Author Information

Abstract

Salinity impairs plant growth, limiting agricultural development. It is desirable to identify genes responding to salt stress and their mechanism of action. We identified a function of the Zea mays WRKY transcription factor, ZmWRKY104, in salt stress response. ZmWRKY104 was localized in the nucleus and showed transcriptional activation activity. Phenotypic and physiological analysis showed that overexpression of ZmWRKY104 in maize increased the tolerance of maize to salt stress and alleviated salt-induced increases in O2− accumulation, malondialdehyde (MDA) content, and percent of electrolyte leakage. Further investigation showed that ZmWRKY104 increased SOD activity by regulating ZmSOD4 expression. Yeast one-hybrid, electrophoretic mobility shift test, and chromatin immunoprecipitation–quantitative PCR assay showed that ZmWRKY104 bound directly to the promoter of ZmSOD4 by recognizing the W-box motif in vivo and in vitro. Phenotypic, physiological, and biochemical analysis showed that ZmSOD4 increased salt tolerance by alleviating salt-induced increases in O2− accumulation, MDA content, and percent of electrolyte leakage under salt stress. Taken together, our results indicate that ZmWRKY104 positively regulates ZmSOD4 expression to modulate salt-induced O2− accumulation, MDA content, and percent of electrolyte leakage, thus affecting salt stress response in maize.

Keywords

Salt tolerance Zea mays ZmWRKY104ZmSOD4

References

[1]

J.K. Zhu, Abiotic stress signaling and responses in plants, Cell 167 (2016) 313–324.
Crossref Google Scholar
[2]

Y. Yang, Y. Guo, Unraveling salt stress signaling in plants, J. Integr. Plant Biol. 60 (2018) 796–804.
Crossref Google Scholar
[3]

J. Wu, Y. Jiang, Y. Liang, L. Chen, W. Chen, B. Cheng, Expression of the maize MYB transcription factor ZmMYB3R enhances drought and salt stress tolerance in transgenic plants, Plant Physiol. Biochem. 137 (2019) 179–188.
Crossref Google Scholar
[4]

Y.L. Ju, X.F. Yue, Z. Min, X.H. Wang, Y.L. Fang, J.X. Zhang, VvNAC17, a novel stress-responsive grapevine (Vitis vinifera L.) NAC transcription factor, increases sensitivity to abscisic acid and enhances salinity, freezing, and drought tolerance in transgenic Arabidopsis, Plant Physiol. Biochem. 146 (2020) 98–111.
Crossref Google Scholar
[5]

R. Cai, W. Dai, C. Zhang, Y. Wang, M. Wu, Y. Zhao, Q. Ma, Y. Xiang, B. Cheng, The maize WRKY transcription factor ZmWRKY17 negatively regulates salt stress tolerance in transgenic Arabidopsis plants, Planta 246 (2017) 1215–1231.
Crossref Google Scholar
[6]

J. Yan, Y. Liu, L. Yang, H. He, Y. Huang, L. Fang, H.V. Scheller, M. Jiang, A. Zhang, Cell Wall β-1, 4-galactan regulated by the BPC1/BPC2-GALS1 module aggravates salt sensitivity in Arabidopsis thaliana, Mol. Plant 46 (2021) 411–425.
Crossref Google Scholar
[7]

F. Chen, Y. Hu, A. Vannozzi, K. Wu, H. Cai, Y. Qin, A. Mullis, Z. Lin, L. Zhang, The WRKY transcription factor family in model plants and crops, Crit. Rev. Plant Sci. 36 (2017) 311–335.
Crossref Google Scholar
[8]

P.J. Rushton, I.E. Somssich, P. Ringler, Q.J. Shen, WRKY transcription factors, Trends Plant Sci. 15 (2010) 247–258.
Crossref Google Scholar
[9]

Z.J. Ding, J.Y. Yan, C.X. Li, G.X. Li, Y.R. Wu, S.J. Zheng, Transcription factor WRKY 46 modulates the development of Arabidopsis lateral roots in osmotic/salt stress conditions via regulation of ABA signaling and auxin homeostasis, Plant J. 84 (2015) 56–69.
Crossref Google Scholar
[10]

X. Cheng, Y. Zhao, Q. Jiang, J. Yang, W. Zhao, I.A. Taylor, Y.L. Peng, D. Wang, J. Liu, Structural basis of dimerization and dual W-box DNA recognition by rice WRKY domain, Nucl. Acids Res. 47 (2019) 4308–4318.
Crossref Google Scholar
[11]

C.Q. Zhang, Y. Xu, Y. Lu, H.X. Yu, M.H. Gu, Q.Q. Liu, The WRKY transcription factor OsWRKY78 regulates stem elongation and seed development in rice, Planta 234 (2011) 541–554.
Crossref Google Scholar
[12]

Y. Wang, Y. Li, S.P. He, Y.A. Gao, N.N. Wang, R. Lu, X.B. Li, A cotton (Gossypium hirsutum) WRKY transcription factor (GhWRKY22) participates in regulating anther/pollen development, Plant Physiol. Biochem. 141 (2019) 231–239.
Crossref Google Scholar
[13]

T. Tian, L. Ma, Y. Liu, D.I. Xu, Q. Chen, G. Li, Arabidopsis FAR-RED ELONGATED HYPOCOTYL3 integrates age and light signals to negatively regulate leaf senescence, Plant Cell 32 (2020) 1574–1588.
Crossref Google Scholar
[14]

T. Eulgem, P.J. Rushton, S. Robatzek, I.E. Somssich, The WRKY superfamily of plant transcription factors, Trends Plant Sci. 5 (2000) 199–206.
Crossref Google Scholar
[15]

L. Chen, Y.U. Song, S. Li, L. Zhang, C. Zou, D. Yu, The role of WRKY transcription factors in plant abiotic stresses, Biochim. Biophys. Acta 1819 (2012) 120–128.
Crossref Google Scholar
[16]

L. Satapathy, D. Kumar, M. Kumar, K. Mukhopadhyay, Functional and DNA-protein binding studies of WRKY transcription factors and their expression analysis in response to biotic and abiotic stress in wheat (Triticum aestivum L.), 3 Biotech 8 (2018) 40.
Crossref Google Scholar
[17]

V. Albrecht, S. Weinl, D. Blazevic, C. D'Angelo, O. Batistic, Ü. Kolukisaoglu, R. Bock, B. Schulz, K. Harter, J. Kudla, The calcium sensor CBL1 integrates plant responses to abiotic stresses, Plant J. 36 (2003) 457–470.
Crossref Google Scholar
[18]

Z.J. Ding, J.Y. Yan, X.Y. Xu, D.Q. Yu, G.X. Li, S.Q. Zhang, S.J. Zheng, Transcription factor WRKY 46 regulates osmotic stress responses and stomatal movement independently in Arabidopsis, Plant J. 79 (2014) 13–27.
Crossref Google Scholar
[19]

S. Vanderauwera, K. Vandenbroucke, A. Inze, B. van de Cotte, P. Muhlenbock, R. de Rycke, N. Naouar, T. van Gaever, M.C.E. van Montagu, F. van Breusegem, AtWRKY15 perturbation abolishes the mitochondrial stress response that steers osmotic stress tolerance in Arabidopsis, Proc. Natl. Acad. Sci. U. S. A. 109 (2012) 20113–20118.
Crossref Google Scholar
[20]

C.T. Wang, J.N. Ru, Y.W. Liu, M. Li, D. Zhao, J.F. Yang, J.D. Fu, Z.S. Xu, Maize WRKY transcription factor ZmWRKY106 confers drought and heat tolerance in transgenic plants, Int. J. Mol. Sci. 19 (2018) 3046.
Crossref Google Scholar
[21]

K.F. Wei, J. Chen, Y.F. Chen, L.J. Wu, D.X. Xie, Molecular phylogenetic and expression analysis of the complete WRKY transcription factor family in maize, DNA Res. 19 (2012) 153–164.
Crossref Google Scholar
[22]

H. Li, Y. Gao, H.U. Xu, Y.I. Dai, D. Deng, J. Chen, ZmWRKY33, a WRKY maize transcription factor conferring enhanced salt stress tolerances in Arabidopsis, Plant Growth Regul. 70 (2013) 207–216.
Crossref Google Scholar
[23]

C. Bo, H. Chen, G. Luo, W. Li, X. Zhang, Q. Ma, B. Cheng, R. Cai, Maize WRKY114 gene negatively regulates salt-stress tolerance in transgenic rice, Plant Cell Rep. 39 (2020) 135–148.
Crossref Google Scholar
[24]

R. Cai, Y. Zhao, Y. Wang, Y. Lin, X. Peng, Q. Li, Y. Chang, H. Jiang, Y. Xiang, B. Cheng, Overexpression of a maize WRKY58 gene enhances drought and salt tolerance in transgenic rice, Plant Cell Tissue Organ Cult. 119 (2014) 565–577.
Crossref Google Scholar
[25]

J. Yan, Y. Huang, H. He, T. Han, P. Di, J. Sechet, L. Fang, Y. Liang, H.V. Scheller, J.C. Mortimer, Xyloglucan endotransglucosylase-hydrolase30 negatively affects salt tolerance in Arabidopsis, J. Exp. Bot. 70 (2019) 5495–5506.
Crossref Google Scholar
[26]

M.G. Kibria, M. Hossain, Y. Murata, M.A. Hoque, Antioxidant defense mechanisms of salinity tolerance in rice genotypes, Rice Sci. 24 (2017) 155–162.
Crossref Google Scholar
[27]

Z.B. Liu, W.J. Zhang, X.D. Gong, Q. Zhang, L.R. Zhou, A Cu/Zn superoxide dismutase from Jatropha curcas enhances salt tolerance of Arabidopsis thaliana, Genet. Mol. Res. 14 (2015) 2086–2098.
Crossref Google Scholar
[28]

Q. Guan, X.U. Liao, M. He, X. Li, Z. Wang, H. Ma, S. Yu, S. Liu, J.S. Zhang, Tolerance analysis of chloroplast OsCu/Zn-SOD overexpressing rice under NaCl and NaHCO3 stress, PLoS ONE 12 (2017) e0186052.
Crossref Google Scholar
[29]

A. Shafi, A.K. Pal, V. Sharma, S. Kalia, S. Kumar, P.S. Ahuja, A.K. Singh, Transgenic potato plants overexpressing SOD and APX exhibit enhanced lignification and starch biosynthesis with improved salt stress tolerance, Plant Mol. Biol. Rep. 35 (2017) 504–518.
Crossref Google Scholar
[30]

Y. Xing, W.h. Chen, W. Jia, J. Zhang, Mitogen-activated protein kinase kinase 5 (MKK5)-mediated signalling cascade regulates expression of iron superoxide dismutase gene in Arabidopsis under salinity stress, J. Exp. Bot. 66 (2015) 5971–5981.
Crossref Google Scholar
[31]

D. Verma, N. Lakhanpal, K. Singh, Genome-wide identification and characterization of abiotic-stress responsive SOD (superoxide dismutase) gene family in Brassica juncea and B. rapa, BMC Genomics 20 (2019) 227.
Crossref Google Scholar
[32]

Y. Zhu, J. Yan, W. Liu, L. Liu, Y.u. Sheng, Y. Sun, Y. Li, H.V. Scheller, M. Jiang, X. Hou, L. Ni, A. Zhang, Phosphorylation of a NAC transcription factor by a Calcium/Calmodulin-dependent protein kinase regulates abscisic acid-induced antioxidant defense in maize, Plant Physiol. 171 (2016) 1651–1664.
Crossref Google Scholar
[33]

K.J. Livak, T.D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2-△△CT method, Methods 25 (2001) 402–408.
Crossref Google Scholar
[34]

Y. Xiang, X. Sun, X. Bian, T. Wei, T. Han, J. Yan, A. Zhang, The transcription factor ZmNAC49 reduces stomatal density and improves drought tolerance in maize, J. Exp. Bot. (2020) 1399–1410.
Crossref Google Scholar
[35]

J. Yan, L. Guan, Y. Sun, Y. Zhu, L. Liu, R. Lu, M. Jiang, M. Tan, A. Zhang, Calcium and ZmCCaMK are involved in brassinosteroid-induced antioxidant defense in maize leaves, Plant Cell Physiol. 56 (2015) 883–896.
Crossref Google Scholar
[36]

L.I. Li, F. Wang, P. Yan, W. Jing, C. Zhang, J. Kudla, W. Zhang, A phosphoinositide-specific phospholipase C pathway elicits stress-induced Ca2+ signals and confers salt tolerance to rice, New Phytol. 214 (2017) 1172–1187.
Crossref Google Scholar
[37]

S. Adhikari, S. Ghosh, I. Azahar, A. Adhikari, A.K. Shaw, S. Konar, S. Roy, Z. Hossain, Sulfate improves cadmium tolerance by limiting cadmium accumulation, modulation of sulfur metabolism and antioxidant defense system in maize, Environ. Exp. Bot. 153 (2018) 143–162.
Crossref Google Scholar
[38]

J. Yan, L. Fang, L. Yang, H. He, Y. Huang, Y. Liu, A. Zhang, Abscisic acid positively regulates L-arabinose metabolism to inhibit seed germination through ABSCISIC ACID INSENSITIVE4-mediated transcriptional promotions of MUR4 in Arabidopsis thaliana, New Phytol. 225 (2020) 823–834.
Crossref Google Scholar
[39]

A.D. de Azevedo Neto, J.T. Prisco, J. Enéas-Filho, C.E.B. de Abreu, E. Gomes-Filho, Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes, Environ. Exp. Bot. 56 (2006) 87–94.
Crossref Google Scholar
[40]

C.S. Johnson, B. Kolevski, D.R. Smyth, TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor, Plant Cell 14 (2002) 1359–1375.
Crossref Google Scholar
[41]

Y. Miao, T. Laun, P. Zimmermann, U. Zentgraf, Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis, Plant Mol. Biol. 55 (2004) 853–867.
Crossref Google Scholar
[42]

M. Luo, E.S. Dennis, F. Berger, W.J. Peacock, A. Chaudhury, MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis, Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 17531–17536.
Crossref Google Scholar
[43]

C.I. Rinerson, E.D. Scully, N.A. Palmer, T. Donze-Reiner, R.C. Rabara, P. Tripathi, Q.J. Shen, S.E. Sattler, J.S. Rohila, G. Sarath, P.J. Rushton, The WRKY transcription factor family and senescence in switchgrass, BMC Genomics 16 (2015) 912.
Crossref Google Scholar
[44]

L. Yang, X. Zhao, F. Yang, D. Fan, Y. Jiang, K. Luo, PtrWRKY19, a novel WRKY transcription factor, contributes to the regulation of pith secondary wall formation in Populus trichocarpa, Sci. Rep. 6 (2016) 18643.
Crossref Google Scholar
[45]

X. Wang, J. Li, J. Guo, Q. Qiao, X. Guo, Y. Ma, The WRKY transcription factor PlWRKY65 enhances the resistance of Paeonia lactiflora (herbaceous peony) to Alternaria tenuissima, Hortic. Res. 7 (2020) 1–12.
Crossref Google Scholar
[46]

Z. Zheng, S.A. Qamar, Z. Chen, T. Mengiste, Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens, Plant J. 48 (2006) 592–605.
Crossref Google Scholar
[47]

Y. Miao, T.M. Laun, A. Smykowski, U. Zentgraf, Arabidopsis MEKK1 can take a short cut: it can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter, Plant Mol. Biol. 65 (2007) 63–76.
Crossref Google Scholar
[48]

Z.Q. Liu, L. Yan, Z. Wu, C. Mei, K. Lu, Y.T. Yu, S. Liang, X.F. Zhang, X.F. Wang, D.P. Zhang, Cooperation of three WRKY-domain transcription factors WRKY18, WRKY40, and WRKY60 in repressing two ABA-responsive genes ABI4 and ABI5 in Arabidopsis, J. Exp. Bot. 63 (2012) 6371–6392.
Crossref Google Scholar
[49]

S. Robatzek, I.E. Somssich, Targets of AtWRKY6 regulation during plant senescence and pathogen defense, Gene Dev. 16 (2002) 1139–1149.
Crossref Google Scholar
[50]

R. Sunkar, A. Kapoor, J.K. Zhu, Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance, Plant Cell 18 (2006) 2051–2065.
Crossref Google Scholar
[51]

Y. Wang, C. Deng, P. Ai, X. Cui, Z. Zhang, ALM1, encoding a Fe-superoxide dismutase, is critical for rice chloroplast biogenesis and drought stress response, Crop J. 9 (2021) 1018–1029.
Crossref Google Scholar
[52]

X. Luo, Y. Dai, C. Zheng, Y. Yang, W. Chen, Q. Wang, U. Chandrasekaran, J. Du, W. Liu, K. Shu, The ABI4-RbohD/VTC2 regulatory module promotes reactive oxygen species (ROS) accumulation to decrease seed germination under salinity stress, New Phytol. 229 (2021) 950–962.
Crossref Google Scholar
[53]

Y. Yu, J. Wang, S. Li, X. Kakan, Y. Zhou, Y. Miao, F. Wang, H. Qin, R. Huang, Ascorbic acid integrates the antagonistic modulation of ethylene and abscisic acid in the accumulation of reactive oxygen species, Plant Physiol. 179 (2019) 1861–1875.
Crossref Google Scholar
[54]

X. Kakan, Y. Yu, S. Li, X. Li, R. Huang, J. Wang, Ascorbic acid modulation by ABI4 transcriptional repression of VTC2 in the salt tolerance of Arabidopsis, BMC Plant Biol. 21 (2021) 112.
Crossref Google Scholar
[55]

Y. Xing, Q. Cao, Q. Zhang, L. Qin, W. Jia, J. Zhang, MKK5 regulates high light-induced gene expression of Cu/Zn superoxide dismutase 1 and 2 in Arabidopsis, Plant Cell Physiol 54 (2013) 1217–1227.
Crossref Google Scholar
The Crop Journal
Volume 10 Issue 2,
April 2022
Pages 555-564
DOI: 10.1016/j.cj.2021.05.010
Cite this article:
Yan J, Li J, Zhang H, et al. ZmWRKY104 positively regulates salt tolerance by modulating ZmSOD4 expression in maize. The Crop Journal, 2022, 10(2): 555-564. https://doi.org/10.1016/j.cj.2021.05.010

255

Views

4

Downloads

20

Crossref

19

Web of Science

25

Scopus

5

CSCD

Altmetrics
Received: 18 March 2021
Revised: 04 May 2021
Accepted: 11 June 2021
Published: 01 July 2021
© 2021 Crop Science Society of China and Institute of Crop Science, CAAS.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Return