SlWRKY45 interacts with jasmonate-ZIM domain proteins to negatively regulate defense against the root-knot nematode Meloidogyne incognita in tomato

Abstract

Parasitic root-knot nematodes (RKNs) cause a severe reduction in crop yield and seriously threaten agricultural production. The phytohormones jasmonates (JAs) are important signals regulating resistance to multiple biotic and abiotic stresses. However, the molecular mechanism for JAs-regulated defense against RKNs in tomato remains largely unclear. In this study, we found that the transcription factor SlWRKY45 interacted with most JA-ZIM domain family proteins (JAZs), key repressors of the JA signaling. After infection by the RKN Meloidogyne incognita, the slwrky45 mutants exhibited lower gall numbers and egg numbers per gram of roots than wild type, whereas overexpression of SlWRKY45 attenuated resistance to Meloidogyne incognita. Under M. incognita infection, the contents of jasmonic acid (JA) and JA-isoleucine (JA-Ile) in roots were repressed by SlWRKY45-overexpression. Furthermore, SlWRKY45 bound to and inhibited the promoter of the JA biosynthesis gene ALLENE OXIDE CYCLASE (AOC), and repressed its expression. Overall, our findings revealed that the SlJAZ-interaction protein SlWRKY45 attenuated RKN-regulated JA biosynthesis and repressed defense against the RKN M. incognita in tomato.

References

[1] El-Sappah AH, Yan S, Qi S et al. Tomato natural resistance genes in controlling the root-knot nematode. Genes (Basel). 2019; 10: 925.

[2] Gheysen G, Mitchum MG . How nematodes manipulate plant development pathways for infection. Curr Opin Plant Biol. 2011; 14: 415-21.

[3] Favery B, Quentin M, Jaubert-Possamai S et al. Gall-forming root-knot nematodes hijack key plant cellular functions to induce multinucleate and hypertrophied feeding cells. J Insect Physiol. 2016; 84: 60-9.

[4] Bird DM . Signaling between nematodes and plants. Curr Opin Plant Biol. 2004; 7: 372-6.

[5] Siddique S, Grundler FM . Parasitic nematodes manipulate plant development to establish feeding sites. Curr Opin Microbiol. 2018; 46: 102-8.

[6] Abad P, Favery B, Rosso MN et al. Root-knot nematode parasitism and host response: molecular basis of a sophisticated interaction. Mol Plant Pathol. 2003; 4: 217-24.

[7] Browse J. Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol. 2009; 60: 183-205.

[8] Xie DX, Feys BF, James S et al. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Sci. 1998; 280: 1091-4.

[9] Xu L, Liu F, Lechner E et al. The SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell. 2002; 14: 1919-35.

[10] Chini A, Fonseca S, Fernández G et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature. 2007; 448: 666-71.

[11] Thines B, Katsir L, Melotto M et al. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature. 2007; 448: 661-5.

[12] Yan Y, Stolz S, Chételat A et al. A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell. 2007; 19: 2470-83.

[13] Chini A, Gimenez-Ibanez S, Goossens A et al. Redundancy and specificity in jasmonate signalling. Curr Opin Plant Biol. 2016; 33: 147-56.

[14] Howe GA, Major IT, Koo AJ . Modularity in Jasmonate Signaling for multistress resilience. Annu Rev Plant Biol. 2018; 69: 387-415.

[15] Yan J, Yao R, Chen L et al. Dynamic perception of Jasmonates by the F-box protein COI1. Mol Plant. 2018; 11: 1237-47.

[16] Yan J, Zhang C, Gu M et al. The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell. 2009; 21: 2220-36.

[17] Sheard LB, Tan X, Mao H et al. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature. 2010; 468: 400-5.

[18] Fonseca S, Chini A, Hamberg M et al. (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol. 2009; 5: 344-50.

[19] Wasternack C, Song S . Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. J Exp Bot. 2017; 68: 1303-21.

[20] Cooper WR, Jia L, Goggin L . Effects of jasmonate-induced defenses on root-knot nematode infection of resistant and susceptible tomato cultivars. J Chem Ecol. 2005; 31: 1953-67.

[21] Fan J, Hu CL, Zhang LN et al. Jasmonic acid mediates tomato’s response to root knot nematodes. J Plant Growth Regul. 2015; 34: 196-205.

[22] Sun Y, Cao H, Yin J et al. Elevated CO2 changes the interactions between nematode and tomato genotypes differing in the JA pathway. Plant Cell Environ. 2010; 33: 729-39.

[23] Zhao W, Li Z, Fan J et al. Identification of jasmonic acid-associated microRNAs and characterization of the regulatory roles of the miR319/TCP4 module under root-knot nematode stress in tomato. J Exp Bot. 2015; 66: 4653-67.

[24] Xu X, Fang P, Zhang H et al. Strigolactones positively regulate defense against root-knot nematodes in tomato. J Exp Bot. 2019; 70: 1325-37.

[25] Shang Y, Wang K, Sun S et al. COP9 Signalosome CSN4 and CSN5 subunits are involved in jasmonate-dependent defense against root-knot nematode in tomato. Front Plant Sci. 2019; 10: 1223.

[26] Li W, Pang S, Lu Z et al. Function and mechanism of WRKY transcription factors in abiotic stress responses of plants. Plants (Basel). 2020; 9: 1515.

[27] Wani SH, Anand S, Singh B et al. WRKY transcription factors and plant defense responses: latest discoveries and future prospects. Plant Cell Rep. 2021; 40: 1071-85.

[28] Rushton PJ, Somssich IE, Ringler P et al. WRKY transcription factors. Trends Plant Sci. 2010; 15: 247-58.

[29] Karkute SG, Gujjar RS, Rai A et al. Genome wide expression analysis of WRKY genes in tomato (Solanum lycopersicum) under drought stress. Plant Gene. 2018; 13: 8-17.

[30] 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.

[31] 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.

[32] Chinnapandi B, Bucki P, Braun Miyara S . SlWRKY45, nematode-responsive tomato WRKY gene, enhances susceptibility to the root knot nematode M. javanica infection. Plant Signal Behav. 2017; 12: e1356530.

[33] Wang G, Hu C, Zhou J et al. Systemic root-shoot signaling drives jasmonate-based root defense against nematodes. Curr Biol. 2019; 29: 3430-3438.e4.

[34] Jiang Y, Liang G, Yang S et al. Arabidopsis WRKY57 functions as a node of convergence for jasmonic acid- and auxin-mediated signaling in jasmonic acid-induced leaf senescence. Plant Cell. 2014; 26: 230-45.

[35] Yan C, Fan M, Yang M et al. Injury activates Ca(2+)/Calmodulin-dependent phosphorylation of JAV1-JAZ8-WRKY51 complex for Jasmonate biosynthesis. Cell. 2018; 70: 136-149.e7.

[36] Huang H, Zhao W, Li C et al. SlVQ15 interacts with Jasmonate-ZIM domain proteins and SlWRKY31 to regulate Defense response in tomato. Plant Physiol. 2022; 190: 828-42.

[37] Hussain RMF, Sheikh AH, Haider I et al. Arabidopsis WRKY50 and TGA transcription factors synergistically activate expression of PR1. Front Plant Sci. 2018; 9: 930.

[38] Chen J, Wang H, Li Y et al. Arabidopsis VQ10 interacts with WRKY8 to modulate basal defense against Botrytis cinerea. J Integr Plant Biol. 2018; 60: 956-69.

[39] Hu Y, Chen L, Wang H et al. Arabidopsis transcription factor WRKY8 functions antagonistically with its interacting partner VQ9 to modulate salinity stress tolerance. Plant J. 2013; 74: 730-45.

[40] Ma Z, Li W, Wang H et al. WRKY transcription factors WRKY12 and WRKY13 interact with SPL10 to modulate age-mediated flowering. J Integr Plant Biol. 2020; 62: 1659-73.

[41] Kim KC, Lai Z, Fan B et al. Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell. 2008; 20: 2357-71.

[42] Jiang Y, Yu D . The WRKY57 transcription factor affects the expression of jasmonate ZIM-domain genes transcriptionally to compromise Botrytis cinerea resistance. Plant Physiol. 2016; 171: 2771-82.

[43] Turck F, Zhou A, Somssich IE . Stimulus-dependent, promoter-specific binding of transcription factor WRKY1 to its native promoter and the defense-related gene PcPR1-1 in parsley. Plant Cell. 2004; 16: 2573-85.

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

[45] Min D, Li F, Zhang X et al. SlMYC2 involved in methyl jasmonate-induced tomato fruit chilling tolerance. J Agric Food Chem. 2018; 66: 3110-7.

[46] Min D, Li F, Cui X et al. SlMYC2 are required for methyl jasmonate-induced tomato fruit resistance to Botrytis cinerea. Food Chem. 2020; 310: 125901.

[47] Shu P, Li Z, Min D et al. CRISPR/Cas9-mediated SlMYC2 mutagenesis adverse to tomato plant growth and meja-induced fruit resistance to Botrytis cinerea. J Agric Food Chem. 2020; 68: 5529-38.

[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.

[49] Qi T, Song S, Ren Q et al. The Jasmonate-ZIM-domain proteins interact with the WD-repeat/bHLH/MYB complexes to regulate Jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell. 2011; 23: 1795-814.

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

[51] Hussey RS, Barker KR . Comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Dis Rep. 1973; 57: 1025-8.

[52] Pan X, Welti R, Wang X . Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc. 2010; 5: 986-92.

[53] Saleh A, Alvarez-Venegas R, Avramova Z . An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat Protoc. 2008; 3: 1018-25.

[54] Yamaguchi N, Winter CM, Wu MF et al. PROTOCOLS: chromatin Immunoprecipitation from Arabidopsis tissues. Arabidopsis Book. 2014; 12: e0170.

[55] 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.