SlWRKY30 and SlWRKY81 synergistically modulate tomato immunity to Ralstonia solanacearum by directly regulating SlPR-STH2

Fengfeng Dang , Jinhui Lin , Yajing Li , Ruoyun Jiang , Yudong Fang , Fei Ding , Shuilin He , Yanfeng Wang

Horticulture Research ›› 2023, Vol. 10 ›› Issue (5) : 050

PDF (3846KB)
Horticulture Research ›› 2023, Vol. 10 ›› Issue (5) :050 DOI: 10.1093/hr/uhad050
Article
research-article
SlWRKY30 and SlWRKY81 synergistically modulate tomato immunity to Ralstonia solanacearum by directly regulating SlPR-STH2
Author information +
History +
PDF (3846KB)

Abstract

Bacterial wilt is a devastating disease of tomato (Solanum lycopersicum) caused by Ralstonia solanacearum that severely threatens tomato production. Group III WRKY transcription factors (TFs) are implicated in the plant response to pathogen infection; however, their roles in the response of tomato to R. solanacearum infection (RSI) remain largely unexplored. Here, we report the crucial role of SlWRKY30, a group III SlWRKY TF, in the regulation of tomato response to RSI. SlWRKY30 was strongly induced by RSI. SlWRKY30 overexpression reduced tomato susceptibility to RSI, and also increased H2O2 accumulation and cell necrosis, suggesting that SlWRKY30 positively regulates tomato resistance to RSI. RNA sequencing and reverse transcription–quantitative PCR revealed that SlWRKY30 overexpression significantly upregulated pathogenesis-related protein (SlPR-STH2) genes SlPR-STH2a, SlPR-STH2b, SlPR-STH2c, and SlPR-STH2d (hereafter SlPR-STH2a/ b/ c/ d) in tomato, and these SlPR-STH2 genes were directly targeted by SlWRKY30. Moreover, four group III WRKY proteins (SlWRKY52, SlWRKY59, SlWRKY80, and SlWRKY81) interacted with SlWRKY30, and SlWRKY81 silencing increased tomato susceptibility to RSI. Both SlWRKY30 and SlWRKY81 activated SlPR-STH2a/ b/ c/ d expression by directly binding to their promoters. Taking these results together, SlWRKY30 and SlWRKY81 synergistically regulate resistance to RSI by activating SlPR-STH2a/ b/ c/ d expression in tomato. Our results also highlight the potential of SlWRKY30 to improve tomato resistance to RSI via genetic manipulations.

Cite this article

Download citation ▾
Fengfeng Dang, Jinhui Lin, Yajing Li, Ruoyun Jiang, Yudong Fang, Fei Ding, Shuilin He, Yanfeng Wang. SlWRKY30 and SlWRKY81 synergistically modulate tomato immunity to Ralstonia solanacearum by directly regulating SlPR-STH2. Horticulture Research, 2023, 10 (5) : 050 DOI:10.1093/hr/uhad050

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This work was supported by the Guangdong Basic and Applied Basic Research Foundation (2019A1515110239), the China Postdoctoral Science Foundation (2020 M682732), and the Key Project of Biology Discipline Construction of Yan’an University (301200085).

Author contributions

F.F.D. and Y.F.W. conceived and designed the research; F.F.D., J.H.L., Y.J.L., R.Y.J., Y.D.F., and F.D. performed the experiments; F.F.D., F.D., S.L.H., and Y.F.W. analyzed the data; F.F.D., F.D., and S.L.H. wrote the manuscript; all the authors revised the manuscript.

Data availability

All relevant data supporting our findings are available in the manuscript file or from the corresponding author upon request.

Conflict of interest

The authors declare no competing interests.

References

[1]

Boller T, He SY . Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science. 2009; 324: 742-4.

[2]

Jones JDG, Dangl JL . The plant immune system. Nature. 2006; 444: 323-9.

[3]

Köster P, DeFalco TA, Zipfel C . Ca 2+ signals in plant immunity . EMBO J. 2022; 41: e110741.

[4]

Pieterse CM, Van der Does D, Zamioudis C et al. Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol. 2012; 28: 489-521.

[5]

Lewis LA, Polanski K, de Torres-Zabala M et al. Transcriptional dynamics driving MAMP-triggered immunity and pathogen effector-mediated immunosuppression in Arabidopsis leaves following infection with Pseudomonas syringae pv tomato DC3000 . Plant Cell. 2015; 27: 3038-64.

[6]

Buscaill P, Rivas S . Transcriptional control of plant defence responses. Curr Opin Plant Biol. 2014; 20: 35-46.

[7]

Birkenbihl RP, Liu S, Somssich IE . Transcriptional events defining plant immune responses. Curr Opin Plant Biol. 2017; 38: 1-9.

[8]

Tsuda K, Somssich IE . Transcriptional networks in plant immunity. New Phytol. 2015; 206: 932-47.

[9]

Eulgem T, Rushton PJ, Robatzek S et al. The WRKY superfamily of plant transcription factors. Trends Plant Sci. 2000; 5: 199-206.

[10]

Kalde M, Barth M, Somssich IE et al. Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways . Mol Plant-Microbe Interact. 2003; 16: 295-305.

[11]

Huang Y, Li MY, Wu P et al. Members of WRKY group III transcription factors are important in TYLCV defense signaling pathway in tomato (Solanum lycopersicum). BMC Genomics. 2016; 17: 788.

[12]

Ding Y, Sun T, Ao K et al. Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity. Cell. 2018; 173: 1454-1467.e15.

[13]

Chen SY, Ding YL, Tian HN et al. WRKY54 and WRKY70 positively regulate SARD1 and CBP60g expression in plant immunity . Plant Signal Behav. 2021; 16: 1932142.

[14]

Zavaliev R, Mohan R, Chen TY et al. Formation of NPR1 condensates promotes cell survival during the plant immune response. Cell. 2020; 182: 1093-1108.e18.

[15]

Dang FF, Wang YN, Yu L et al. CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection . Plant Cell Environ. 2013; 36: 757-74.

[16]

Yang S, Cai W, Shen L et al. A CaCDPK29-CaWRKY27b module promotes CaWRKY40-mediated thermotolerance and immunity to Ralstonia solanacearum in pepper . New Phytol. 2022; 233: 1843-63.

[17]

Wang Y, Dang F, Liu Z et al. CaWRKY58, encoding a group I WRKY transcription factor of Capsicum annuum, negatively regulates resistance to Ralstonia solanacearum infection . Mol Plant Pathol. 2013; 14: 131-44.

[18]

Eulgem T, Somssich IE . Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol. 2007; 10: 366-71.

[19]

Hayward AC . Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu Rev Phytopathol. 1991; 29: 65-87.

[20]

Kim SG, Hur OS, Ro NY et al. Evaluation of resistance to Ralstonia solanacearum in tomato genetic resources at seedling stage . Plant Pathol J. 2016; 32: 58-64.

[21]

Huang SG, Gao Y, Liu J et al. Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol Gen Genomics. 2012; 287: 495-513.

[22]

Bai YL, Sunarti S, Kissoudis C et al. The role of tomato WRKY genes in plant responses to combined abiotic and biotic stresses . Front Plant Sci. 2018; 9: 801.

[23]

Chinnapandi B, Bucki P, Fitoussi N et al. Tomato SlWRKY3 acts as a positive regulator for resistance against the root-knot nematode Meloidogyne javanica by activating lipids and hormone-mediated defense-signaling pathways . Plant Signal Behav. 2019; 14: 1601951.

[24]

Atamian HS, Eulgem T, Kaloshian I . SlWRKY70 is required for Mi-1-mediated resistance to aphids and nematodes in tomato . Planta. 2012; 235: 299-309.

[25]

Glazebrook J . Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol. 2005; 43: 205-27.

[26]

Yang S, Cai W, Shen L et al. Solanaceous plants switch to cytokinin-mediated immunity against Ralstonia solanacearum under high temperature and high humidity . Plant Cell Environ. 2022; 45: 459-78.

[27]

Mansfield J, Genin S, Magori S et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol. 2012; 13: 614-29.

[28]

Du MM, Zhao J, DTW T et al. MYC2 orchestrates a hierarchical transcriptional cascade that regulates jasmonate-mediated plant immunity in tomato. Plant Cell. 2017; 29: 1883-906.

[29]

Liu YY, Du M, Deng L et al. MYC2 regulates the termination of jasmonate signaling via an autoregulatory negative feedback loop. Plant Cell. 2019; 31: 106-27.

[30]

Jaiswal N, Liao CJ, Mengesha B et al. Regulation of plant immunity and growth by tomato receptor-like cytoplasmic kinase TRK1. New Phytol. 2022; 233: 458-78.

[31]

Chi Y, Yang Y, Zhou Y et al. Protein-protein interactions in the regulation of WRKY transcription factors. Mol Plant. 2013; 6: 287-300.

[32]

Yoshioka H, Numata N, Nakajima K et al. Nicotiana benthamiana gp91 phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. Plant Cell. 2003; 15: 706-18.

[33]

Yuan MH, Ngou BPM, Ding PT et al. PTI-ETI crosstalk: an integrative view of plant immunity. Curr Opin Plant Biol. 2021; 62: 102030.

[34]

Tsuda K, Katagiri F . Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol. 2010; 13: 459-65.

[35]

Tenhaken R, Rubel C . Salicylic acid is needed in hypersensitive cell death in soybean but does not act as a catalase inhibitor. Plant Physiol. 1997; 115: 291-8.

[36]

Feng DX, Tasset C, Hanemian M et al. Biological control of bacterial wilt in Arabidopsis thaliana involves abscissic acid signalling . New Phytol. 2012; 194: 1035-45.

[37]

Besseau S, Li J, Palva ET . WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. J Exp Bot. 2012; 63: 2667-79.

[38]

Xu X, Chen C, Fan B et al. Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors . Plant Cell. 2006; 18: 1310-26.

[39]

Yang S, Zhang Y, Cai W et al. CaWRKY28 Cys249 is required for interaction with CaWRKY40 in the regulation of pepper immunity to Ralstonia solanacearum. Mol Plant-Microbe Interact. 2021; 34: 733-45.

[40]

Wang WD, Chen L, Fengler K et al. A giant NLR gene confers broad-spectrum resistance to Phytophthora sojae in soybean . Nat Commun. 2021; 12: 6263.

[41]

Du M et al. Closely related NAC transcription factors of tomato differentially regulate stomatal closure and reopening during pathogen attack. Plant Cell. 2014; 26: 3167-84.

[42]

Dang FF, Lin J, Chen Y et al. A feedback loop between CaWRKY41 and H2O2 coordinates the response to Ralstonia solanacearum and excess cadmium in pepper . J Exp Bot. 2019; 70: 1581-95.

[43]

Liu Y, Wu G, Zhao Y et al. DWARF53 interacts with transcription factors UB2/UB3/TSH4 to regulate maize tillering and tassel branching. Plant Physiol. 2021; 187: 947-62.

[44]

Dang FF, Li Y, Wang Y et al. ZAT10 plays dual roles in cadmium uptake and detoxification in Arabidopsis. Front Plant Sci. 2022; 13: 994100.

[45]

Yoo SD, Cho YH, Sheen J . Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis . Nat Protoc. 2007; 2: 1565-72.

[46]

Liu YL, Schiff M, Dinesh-Kumar SP . Virus-induced gene silencing in tomato. Plant J. 2002; 31: 777-86.

[47]

Hellens RP, Allan AC, Friel EN et al. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods. 2005; 1: 13.

[48]

Chen H, Zou Y, Shang Y et al. Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol. 2008; 146: 368-76.

PDF (3846KB)

82

Accesses

0

Citation

Detail

Sections
Recommended

/