A LlWRKY33-LlHSFA4-LlCAT2 module confers resistance to Botrytis cinerea in lily

Liping Ding , Ze Wu , Jun Xiang , Xing Cao , Sujuan Xu , Yinyi Zhang , Dehua Zhang , Nianjun Teng

Horticulture Research ›› 2024, Vol. 11 ›› Issue (1) : 254

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Horticulture Research ›› 2024, Vol. 11 ›› Issue (1) :254 DOI: 10.1093/hr/uhad254
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A LlWRKY33-LlHSFA4-LlCAT2 module confers resistance to Botrytis cinerea in lily
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Abstract

Gray mold caused by Botrytis cinerea is one of the major threats in lily production. However, limited information is available about the underlying defense mechanism against B. cinerea in lily. Here, we characterized a nuclear-localized class A heat stress transcription factor (HSF)-LlHSFA4 from lily (Lilium longiflorum), which positively regulated the response to B. cinerea infection. LlHSFA4 transcript and its promoter activity were increased by B. cinerea infection in lily, indicating its involvement in the response to B. cinerea. Virus-induced gene silencing (VIGS) of LlHSFA4 impaired the resistance of lily to B. cinerea. Consistent with its role in lily, overexpression of LlHSFA4 in Arabidopsis (Arabidopsis thaliana) enhanced the resistance of transgenic Arabidopsis to B. cinerea infection. Further analysis showed that LlWRKY33 directly activated LlHSFA4 expression. We also found that both LlHSFA4 and LlWRKY33 positively regulated plant response to B. cinerea through reducing cell death and H2O2 accumulation and activating the expression of the reactive oxygen species (ROS) scavenging enzyme gene LlCAT2 (Catalase 2) by binding its prompter, which might contribute to reducing H2O2 accumulation in the infected area. Taken together, our data suggested that there may be a LlWRKY33-LlHSFA4-LlCAT2 regulatory module which confers B. cinerea resistance via reducing cell death and the ROS accumulation.

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Liping Ding, Ze Wu, Jun Xiang, Xing Cao, Sujuan Xu, Yinyi Zhang, Dehua Zhang, Nianjun Teng. A LlWRKY33-LlHSFA4-LlCAT2 module confers resistance to Botrytis cinerea in lily. Horticulture Research, 2024, 11(1): 254 DOI:10.1093/hr/uhad254

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Acknowledgements

This research was supported by the National Key R&D Program of China (2023YFD2300900), the Project for Crop Germplasm Resources Conservation of Jiangsu (2021-SJ-011), and the Modern Agricultural Industry Technology System in Jiangsu [JATS (2023) 007].

Author contributions

N.T. and Z.W. designed the research; L.D. and Z.W. conducted the experiments and data processing under the supervision of N.T.; L.D. wrote the manuscript; J.X. S.X., Y.Z., and D.Z. provided technological assistance; X.C. isolated and provided strains of Botrytis cinerea. All authors read and revised the article.

Data availability

The data and figures in this study can be found within the article and its supporting materials.

Conflict of interest statement

All authors state that they have no conflict of interest in relation to this research.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1]

van Kan JAL. Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci. 2006;11:247-53

[2]

Dean R, Van Kan JAL, Pretorius ZA. et al. The top 10 fun-gal pathogens in molecular plant pathology. Mol Plant Pathol. 2012;13:414-30

[3]

Mengiste T. Plant immunity to Necrotrophs. Annu Rev Phy-topathol. 2012;50:267-94

[4]

AbuQamar S, Moustafa K, Tran LS. Mechanisms and strategies of plant defense against Botrytis cinerea. Crit Rev Biotechnol. 2017;37: 262-74

[5]

Andersen EJ, Ali S, Byamukama E. et al. Disease resistance mech-anisms in plants. Genes (Basel). 2018;9:339

[6]

Moore JW, Loake GJ, Spoel SH. Transcription dynamics in plant immunity. Plant Cell. 2011;23:2809-20

[7]

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

[8]

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

[9]

Scharf KD, Berberich T, Ebersberger I. et al. The plant heat stress transcription factor (HSF) family: structure, function and evolu-tion. Biochim Biophys Acta Gene Regul Mech. 2012;1819:104-19

[10]

Liu HC, Liao HT, Charng YY. The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Ara-bidopsis. Plant Cell Environ. 2011;34:738-51

[11]

Yoshida T, Ohama N, Nakajima J. et al. Arabidopsis HSFA1 tran-scription factors function as the main positive regulators in heat shock-responsive gene expression. Mol Gen Genomics. 2011;286: 321-32

[12]

Albertos P, Duendar G, Schenk P. et al. Transcription factor BES1 interacts with HSFA1 to promote heat stress resistance of plants. EMBO J. 2022;41:e108664

[13]

Wang N, Liu W, Yu L. et al. Heatshock factor A8a modu-lates flavonoid synthesis and drought tolerance. Plant Physiol. 2020;184:1273-90

[14]

Li F, Zhang H, Zhao H. et al. Chrysanthemum CmHSFA4 gene positively regulates salt stress tolerance in transgenic chrysan-themum. Plant Biotechnol J. 2018;16:1311-21

[15]

Chen S, Yu M, Li H. et al. SaHsfA4c from Sedum alfredii Hanceen-hances cadmium tolerance by regulating ROS-scavenger activ-ities and heat shock proteins expression. Front Plant Sci. 2020;11:142

[16]

Kumar M, Busch W, Birke H. et al. Heat shock factors HSFB1 and HSFB2b are involved in the regulation of Pdf1.2 expression and pathogen resistance in Arabidopsis. Mol Plant. 2009;2:152-65

[17]

Pick T, Jaskiewicz M, Peterhaensel C. et al. Heat shock factor HSFB1 primes gene transcription and systemic acquired resis-tance in Arabidopsis. Plant Physiol. 2012;159:52-5

[18]

Yang W, Ju Y, Zuo L. et al. OsHsfB4d binds the promoter and regulates the expression of OsHsp18.0-CI to resistant against Xanthomonas Oryzae. Rice. 2020;13:28

[19]

Mao G, Meng X, Liu Y. et al. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell. 2011;23: 1639-53

[20]

Zhou J, Wang X, He Y. et al. Differential phosphorylation of the transcription factor WRKY33 by the protein kinases CPK5/CPK6 and MPK3/MPK6 cooperatively regulates camalexin biosynthe-sis in Arabidopsis. Plant Cell. 2020;32:2621-38

[21]

Birkenbihl RP, Diezel C, Somssich IE. Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection. Plant Physiol. 2012; 159:266-85

[22]

Liu S, Kracher B, Ziegler J. et al. Negative regulation of ABA sig-naling by WRKY 33 is critical for Arabidopsis immunity towards Botrytis cinerea 2100. elife. 2015;4:4

[23]

Zhou J, Wang J, Zheng Z. et al. Characterization of the promoter and extended C-terminal domain of Arabidopsis WRKY33 and functional analysis of tomato WRKY33 homologues in plant stress responses. JExp Bot. 2015;66:4567-83

[24]

Zheng Z, Abu Qamar S, Chen Z. et al. Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J. 2006;48:592-605

[25]

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;40:2189-206

[26]

Xue GP, Drenth J, McIntyre CL. TaHSFA6f is a transcriptional activator that regulates a suite of heat stress protection genes in wheat (Triticum aestivum L.) including previously unknown HSF targets. JExp Bot. 2015;66:1025-39

[27]

Xie DL, Huang HM, Zhou CY. et al. HSFA1a confers pollen ther-motolerance through upregulating antioxidant capacity, protein repair, and degradation in Solanum lycopersicum L. Hortic Res. 2022;9:uhad163

[28]

Liu X, Chen H, Li S. et al. Natural variations of HSFA2 enhance thermotolerance in grapevine. Hortic Res. 2023;10:uhac250

[29]

Xin H, Zhang H, Chen L. et al. Cloning and characterization of HSFA2 from lily (Lilium longiflorum). Plant Cell Rep. 2010;29:875-85

[30]

Gong B, Yi J, Wu J. et al. LlHSFA1, a novel heat stress transcription factor in lily (Lilium longiflorum), can interact with LlHSFA2 and enhance the thermotolerance of transgenic Arabidopsis thaliana. Plant Cell Rep. 2014;33:1519-33

[31]

Xin H, Zhang H, Zhong X. et al. Over-expression of LlHSFA2b,a lily heat shock transcription factor lacking trans-activation activity in yeast, can enhance tolerance to heat and oxidative stress in transgenic Arabidopsis seedlings. Plant Cell Tissue Organ Cult. 2017;130:617-29

[32]

Wu Z, Liang J, Wang C. et al. Overexpression of lily HSFA3s in Ara-bidopsis confers increased thermotolerance and salt sensitivity via alterations in proline catabolism. JExp Bot. 2018;69:2005-21

[33]

Wang C, Zhou Y, Yang X. et al. The heat stress transcription factor LlHSFA4 enhanced basic thermotolerance through regu-lating ROS metabolism in lilies (Lilium longiflorum). Int J Mol Sci. 2022;23:572

[34]

Davletova S, Schlauch K, Coutu J. et al. The zinc-finger protein ZAT12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol. 2005;139:847-56

[35]

Shim D, Hwang JU, Lee J. et al. Orthologs of the class A4 heat shocktranscription factor HSFA4a confer cadmium tolerance in wheat and rice. Plant Cell. 2009;21:4031-43

[36]

Personat JM, TejedorCano J, PrietoDapena P. et al. Co-overexpression of two heat shock factors results in enhanced seed longevity and in synergistic effects on seedling tolerance to severe dehydration and oxidative stress. BMC Plant Biol. 2014;14:56

[37]

Perez-Salamo I, Papdi C, Rigo G. et al. The heat shock factor A4A confers salt tolerance and is regulated by oxidative stress and the mitogen-activated protein kinases MPK3 and MPK6. Plant Physiol. 2014;165:319-34

[38]

Ciolkowski I, Wanke D, Birkenbihl RP. et al. Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol Biol. 2008;68:81-92

[39]

Li S, Fu Q, Chen L. et al. Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta. 2011;233:1237-52

[40]

Zhou J, Wang J, Yu JQ. et al. Role and regulation of autophagy in heat stress responses of tomato plants. Front Plant Sci. 2014;5:174

[41]

He GH, Xu JY, Wang YX. et al. Drought-responsive WRKY tran-scription factor genes TaWRKY1 and TaWRKY33 from wheat confer drought and/or heat resistance in Arabidopsis. BMC Plant Biol. 2016;16:116

[42]

Sewelam N, Oshima Y, Mitsuda N. et al. A step towards under-standing plant responses to multiple environmental stresses: a genome-wide study. Plant Cell Environ. 2014;37:2024-35

[43]

Ramegowda V, Senthil-Kumar M. The interactive effects of simultaneous biotic and abiotic stresses on plants: mechanistic understanding from drought and pathogen combination. JPlant Physiol. 2015;176:47-54

[44]

Zhao Y, Yu W, Hu X. et al. Physiological and transcriptomic anal-ysis revealed the involvement of crucial factors in heat stress response of Rhododendron hainanense. Gene. 2018;660:109-19

[45]

Wang L, Wen R, Wang J. et al. Arabidopsis UBC13 differentially regulates two programmed cell death pathways in responses to pathogen and low-temperature stress. New Phytol. 2019;221: 919-34

[46]

Desaint H, Aoun N, Deslandes L. et al. Fight hard or die try-ing: when plants face pathogens under heat stress. New Phytol. 2021;229:712-34

[47]

Webb KM, Ona I, Bai J. et al. A benefit of high temperature: increased effectiveness of a rice bacterial blight disease resis-tance gene. New Phytol. 2010;185:568-76

[48]

Li T, Zhou J, Li J. Combined effects of temperature and humidity on the interaction between tomato and Botrytis cinerea revealed by integration of histological characteristics and transcriptome sequencing. Hortic Res. 2023;10:uhad257

[49]

Eden MA, Hill RA, Beresford R. et al. The influence of inoculum concentration, relative humidity, and temperature on infection of greenhouse tomatoes by Botrytis cinerea. Plant Pathol. 1996;45: 795-806

[50]

Benito EP, ten Have A, van ’t Klooster JW. et al. Fungal and plant gene expression during synchronized infection of tomato leaves by Botrytis cinerea. Eur J Plant Pathol. 1998;104:207-20

[51]

Amselem J, Cuomo CA, van Kan JAL. et al. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 2011;7, e1002230

[52]

Gupta R, Leibman-Markus M, Marash I. et al. Root zone warming represses foliar diseases in tomato by inducing systemic immu-nity. Plant Cell Environ. 2021;44:2277-89

[53]

Qayoum A, Line RF. High-temperature, adult-plant resistence to stripe rust of wheat. Phytopathology. 1985;75:1121-5

[54]

Elad Y, David DR, Israeli L. et al. Passive heat treatment of sweet basil crops suppresses white mould and grey mould. Plant Pathol. 2017;66:105-14

[55]

Elad Y, Omer C, Nisan Z. et al. Passive heat treatment of sweet basil crops suppresses Peronospora belbahrii downy mildew. Ann Appl Biol. 2016;168:373-89

[56]

Ding L, Wu Z, Teng R. et al. LlWRKY39 is involved in thermotol-erance by activating LlMBF1c and interacting with LlCaM3 in lily (Lilium longiflorum). Hortic Res. 2021;8:36

[57]

Cao X, Shi S, Zhang Z. First report of botrytis leaf blight on lily (Lilium longiflorum)causedbyBotrytis cinerea in Beijing, China. Plant Dis. 2018;102:1033-4

[58]

Liu YG, Chen Y. High-efficiency thermal asymmetric interlaced PCR for amplification of unknown flanking sequences. BioTech-niques. 2007;43:649-56

[59]

Hwang SM, Kim DW, Woo MS. et al. Functional characterization of Arabidopsis HSFA6a as a heat-shock transcription factor under high salinity and dehydration conditions. Plant Cell Env-iron. 2014;37:1202-22

[60]

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆CT method. Methods. 2001;25:402-8

[61]

Bachan S, Dinesh-Kumar SP. Tobacco rattle virus (TRV)-based virus-induced gene silencing. Methods Mol Biol. 2012;894:83-92

[62]

Xiang J, Lei X, Wu Z. et al. An efficient and novel method to screen Botrytis cinerea resistance genes based on TRV-induced gene silencing with lily petal discs. Physiol Mol Plant Pathol. 2022;122:101923

[63]

Choi DS, Hwang IS, Hwang BK. Requirement of the cytoso-lic interaction between pathogenesis-related protein10 and leucine-rich1 for cell death and defense signaling in pepper. Plant Cell. 2012;24:1675-90

[64]

Dang F, Wang Y, She J. et al. Overexpression of CaWRKY27,a subgroup IIe WRKY transcription factor of Capsicum annuum, positively regulates tobacco resistance to Ralstonia solanacearum infection. Physiol Plant. 2014;150:397-411

[65]

Clough SJ, Bent AF. Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16:735-43

[66]

Gietz RD, Schiestl RH. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc. 2007;2: 31-4

[67]

Xu S, Wu Z, Hou H. et al. The transcription factor CmLEC1 pos-itively regulates the seed-setting rate in hybridization breeding of chrysanthemum. Hortic Res. 2021;8:191

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