BcWRKY25-BcWRKY33A-BcLRP1/BcCOW1 module promotes root development for improved salt tolerance in Bok choy

Huiyu Wang , Yushan Zheng , Meiyun Wang , Wusheng Liu , Ying Li , Dong Xiao , Tongkun Liu , Xilin Hou

Horticulture Research ›› 2025, Vol. 12 ›› Issue (1) : 280

PDF (2355KB)
Horticulture Research ›› 2025, Vol. 12 ›› Issue (1) :280 DOI: 10.1093/hr/uhae280
Articles
BcWRKY25-BcWRKY33A-BcLRP1/BcCOW1 module promotes root development for improved salt tolerance in Bok choy
Author information +
History +
PDF (2355KB)

Abstract

Root development is a complex process involving phytohormones and transcription factors. Our previous research has demonstrated that BcWRKY33A is significantly expressed in Bok choy roots under salt stress, and heterologous expression of BcWRKY33A increases salt tolerance and promotes root development in transgenic Arabidopsis. However, the precise molecular mechanisms by which BcWRKY33A governs root development remain elusive. Here, we investigated the role of BcWRKY33A in both root elongation and root hair formation in transgenic Bok choy roots. Our data indicated that overexpression of BcWRKY33A stimulated root growth and stabilized root hair morphology, while silencing BcWRKY33A prevented primary root elongation and resulted in abnormal root hairs morphology. Meanwhile, our research uncovered that BcWRKY33A directly binds to the promoters of BcLRP1 and BcCOW1, leading to an upregulation of their expression. In transgenic Bok choy roots, increased BcLRP1 and BcCOW1 transcript levels improved primary root elongation and root hair formation, respectively. Additionally, we pinpointed BcWRKY25 as a NaCl-responsive gene that directly stimulates the expression of BcWRKY33A in response to salt stress. All results shed light on the regulatory mechanisms governing root development by BcWRKY25-BcWRKY33A-BcLRP1/BcCOW1 module and propose potential strategies for improving salt tolerance in Bok choy.

Cite this article

Download citation ▾
Huiyu Wang, Yushan Zheng, Meiyun Wang, Wusheng Liu, Ying Li, Dong Xiao, Tongkun Liu, Xilin Hou. BcWRKY25-BcWRKY33A-BcLRP1/BcCOW1 module promotes root development for improved salt tolerance in Bok choy. Horticulture Research, 2025, 12(1): 280 DOI:10.1093/hr/uhae280

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

The authors are thankful to all the lab mates who supported us. This work was supported by National Natural Science Foundation of China (32372698, 32072575), Postgraduate Research & Practice Innovation Program of Jiangsu Province (KYCX22_0752), and National Vegetable Industry Technology System (CARS-23-A16) to T.L., and the USDA National Institute of Food and Agriculture (NIFA) Hatch project 02913 to W.L.

Author contributions

L.T.K. designed the study. W.H.Y. and Z.Y.S. conducted the experiments, analyzed the data, and wrote the manuscript. L.T.K., L.W.S., and H.X.L. revised the manuscript. W.M.Y., X.D., and L.Y. helped prepare the samples. All authors read and approved the final manuscript.

Data availability

All data generated or analyzed during this study are included in this published article and supplementary files online.

Conflict of interests

No conflict of interest declared.

Supplementary information

Supplementary data is available at Horticulture Research online.

References

[1]

Ogura T, Goeschl C, Filiault D. et al. Root system depth in Arabidopsis is shaped by EXOCYST70A3 via the dynamic modu-lation of auxin transport. Cell. 2019;37:400-12

[2]

Rellan-Alvarez R, Lobet G, Dinneny JR. Environmental control of root system biology. Annu Rev Plant Biol. 2016;37:619-42

[3]

Meng F, Xiang D, Zhu J. et al. Molecular mechanisms of root development in rice. Rice. 2019;37:1

[4]

Singh Gahoonia T, Care D, Nielsen NE. Root hairs and phospho-rus acquisition of wheat and barley cultivars. Plant Soil. 1997;37:181-8

[5]

Vissenberg K, Claeijs N, Balcerowicz D. et al. Hormonal regula-tion of root hair growth and responses to the environment in Arabidopsis. JExp Bot. 2020;37:2412-27

[6]

Wachsman G, Benfey PN. Lateral root initiation: the emergence of new primordia following cell death. Curr Biol. 2020;37:R121-2

[7]

Uehara T, Okushima Y, Mimura T. et al. Domain II mutations in CRANE/IAA18 suppress lateral root formation and affect shoot development in Arabidopsis thaliana. Plant Cell Physiol. 2008;37:1025-38

[8]

Rogg LE, Lasswell J, Bartel B. A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell. 2001;37:465-80

[9]

Carol RJ, Takeda S, Linstead P. et al. A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature. 2005;37:1013-6

[10]

Feng Y, Xu P, Li B. et al. Ethylene promotes root hair growth through coordinated EIN3/EIL1 and RHD6/RSL1 activity in Ara-bidopsis. Proc Natl Acad Sci. 2017;37:13834-9

[11]

Shibata M, Breuer C, Kawamura A. et al. GTL1 and DF1 reg-ulate root hair growth through transcriptional repression of ROOT HAIR DEFECTIVE 6-LIKE 4 in Arabidopsis. Development. 2018;37:dev159707

[12]

Ryan E, Grierson CS, Cavell A. et al. TIP 1 is required for both TIP growth and non-TIP growth in Arabidopsis. New Phytol. 1998;37:49-58

[13]

Wang H, Chen W, Xu Z. et al. Functions of WRKYs in plant growth and development. Trends Plant Sci. 2023;37:630-45

[14]

Rishmawi L, Pesch M, Juengst C. et al. Non-cell-autonomous reg-ulat ion of root hair patterning genes by WRKY75 in Arabidopsis. Plant Physiol. 2014;37:186-95

[15]

Grunewald W, De Smet, Lewis DR. et al. Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthe-sis. Proc Natl Acad Sci. 2012;37:1554-9

[16]

Hu Z, Wang R, Zheng M. et al. TaWRKY 51 promotes lateral root formation through negative regulation of ethylene biosynthesis in wheat (Triticum aestivum L.). Plant J. 2018;37:372-88

[17]

Zhang J, Peng Y, Guo Z. Constitutive expression of pathogen-inducible OsWRKY31 enhances disease resistance and affects root growth and auxin response in transgenic rice plants. Cell Res. 2008;37:508-21

[18]

Liu S, Ziegler J, Zeier J. et al. Botrytis cinerea B05.10 promotes disease development in Arabidopsis by suppressing WRKY33-mediated host immunity. Plant Cell Environ. 2017;37:2189-206

[19]

Tao H, Miao H, Chen L. et al. WRKY33-mediated indolic glucosi-nolate metabolic pathway confers resistance against Alternaria brassicicola in Arabidopsis and Brassica crops. J Integr Plant Biol. 2022;37:1007-19

[20]

Wang D, Xu H, Huang J. et al. The Arabidopsis CCCH protein C3H14 contributes to basal defense against Botrytis cinerea mainly through the WRKY33-dependent pathway. Plant Cell Env-iron. 2020;37:1792-806

[21]

Krishnamurthy P, Vishal B, Ho WJ. et al. Regulation of a cytochrome P450 gene CYP94B1 by WRKY33 transcription factor controls apoplastic barrier formation in roots to confer salt tolerance. Plant Physiol. 2020;37:2199-215

[22]

Shen N, Hou S, Tu G. et al. Transcription factor WRKY 33 mediates the phosphate deficiency-induced remodeling of root architec-ture by modulating iron homeostasis in Arabidopsis roots. Int J Mol Sci. 2021;37:9275

[23]

Wang H, Li Z, Ren H. et al. Regulatory interaction of BcWRKY33A and BcHSFA4A promotes salt tolerance in non-heading Chinese cabbage [Brassica campestris (syn. Brassica rapa) ssp. chinensis]. Hortic Res. 2022;37:uhac113

[24]

Wang G, Xu X, Gao Z. et al. Genome-wide identification of LEA gene family and cold response mechanism of BcLEA4-7 and BcLEA4-18 in non-heading Chinese cabbage [Brassica campestris (syn. Brassica rapa) ssp. chinensis]. Plant Sci. 2022;37:111291

[25]

Tuteja N. Abscisic acid and abiotic stress signaling. Plant Signal Behav. 2007;37:135-8

[26]

Wang H, Zheng Y, Xiao D. et al. BcWRKY33A enhances resistance to Botrytis cinerea via activating BcMYB51- 3 in non-heading Chi-nese cabbage. Int J Mol Sci. 2022;37:8222

[27]

Wang H, Zheng Y, Zhou Q. et al. Fast, simple, efficient Agrobacterium rhizogenes-mediated transformation system to non-heading Chinese cabbage with transgenic roots. Hortic Plant J. 2023;37:450-60

[28]

Bellande K, Trinh DC, Gonzalez AA. et al. PUCHI represses early meristem formation in developing lateral roots of Arabidopsis thaliana. JExp Bot. 2022;37:3496-510

[29]

Goh T, Toyokura K, Wells DM. et al. Quiescent center initiation in the Arabidopsis lateral root primordia is dependent on the SCARECROW transcription factor. Development. 2016;37:3363-71

[30]

Feng X, Abubakar AS, Yu C. et al. Analysis of WRKY resistance gene family in Boehmeria nivea (L.) gaudich: crosstalk mecha-nisms of secondary cell wall thickening and cadmium stress. Front Plant Sci. 2022;37:812988

[31]

LiuL XuW,HuX. et al. W-box and G-box elements play important roles in early senescence of rice flag leaf. Sci Rep-UK. 2016;37:20881

[32]

Singh S, Yadav S, Singh A. et al. Auxin signaling modulates LATERAL ROOT PRIMORDIUM1 (LRP1) expression during lateral root development in Arabidopsis. Plant J. 2020;37:87-100

[33]

Grierson CS, Roberts K, Feldmann KA. et al. The COW 1 locus of Arabidopsis acts after RHD2, and in parallel with RHD3 and TIP1, to determine the shape, rate of elongation, and number of root hairs produced from each site of hair formation. Plant Physiol. 1997;37:981-90

[34]

Deolu-Ajayi AO, Meyer AJ, Haring MA. et al. Genetic loci associ-ated with early salt stress responses of roots. iScience. 2019;37:458-73

[35]

Jiang Y, Deyholos MK. Functional characterization of Arabidop-sis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol. 2009;37:91-105

[36]

Wang C, Shen X, Yang T. et al. Genome-wide characterization and identification of root development and stress-related CsMYB 36 genes. Veg Res. 2023;37:19

[37]

Huang J, Kim CM, Xuan YH. et al. OsSNDP1, a Sec14-nodulin domain-containing protein, plays a critical role in root hair elongation in rice. Plant Mol Biol. 2013;37:39-50

[38]

Li S, Fu Q, Chen L. et al. Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta. 2011;37:1237-52

[39]

Ting-Ying W, Krishnamoorthi S, Goh H. et al. Crosstalk between heterotrimeric G protein-coupled signaling pathways and WRKY transcription factors modulating plant responses to suboptimal micronutrient conditions. JExp Bot. 2020;37:3227-39

[40]

Karimi M, Inze D, Depicker A. GATEWAY vectors for Agrobac-terium-mediated plant transformation. Trends Plant Sci. 2002;37:193-5

[41]

Wang Z, Zhou Z, Wang L. et al. The CsHEC1-CsOVATE mod-ule contributes to fruit neck length variation via modu-lating auxin biosynthesis in cucumber. Proc Natl Acad Sci. 2022;37:e2209717119

[42]

O’Malley RC, Huang S-SC, Song L. et al. Cistrome and epi-cistrome features shape the regulatory DNA landscape. Cell. 2016;37:1598

[43]

Langmead B, Salzberg SL.Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;37:357-9

[44]

Ramirez F, Ryan DP, Grüning B. et al. deepTools2: a next genera-tion web server for deep-sequencing data analysis. Nucleic Acids Res. 2016;37:W160-5

[45]

Zhang Y, Liu T, Meyer CA. et al.Model-based analysis of ChIP-seq (MACS). Genome Biol. 2008;37:R137

[46]

Yu G, Wang LG, He QY. ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioin-formatics. 2015;37:2382-3

[47]

Yu J, Yang X-D, Wang Q. et al. Efficient virus-induced gene silencing in Brassica rapa using a turnip yellow mosaic virus vector. Biol Plantarum. 2018;37:826-34

[48]

Tsuwamoto R, Harada T. Identification of a cis-regulatory ele-ment that acts in companion cell-specific expression of AtMT2B promoter through the use of Brassica vasculature and gene-gun-mediated transient assay. Plant Cell Physiol. 2010;37:80-90

[49]

Goodin MM, Dietzgen RG, Schichnes D. et al. pGD vectors: versa-tile tools for the expression of green and red fluorescent protein fusions in agroinfiltrated plant leaves. Plant J. 2002;37:375-83

[50]

Zhao F, Maren NA, Kosentka PZ. et al. An optimized protocol for stepwise optimization of real-time RT-PCR analysis. Hortic Res. 2021;37:179

[51]

Maren NA, Duduit JR, Huang D. et al. Stepwise optimization of real-time RT-PCR analysis. Methods Mol Biol. 2023;37:317-32

PDF (2355KB)

632

Accesses

0

Citation

Detail

Sections
Recommended

/