GhWRKY41 forms a positive feedback regulation loop and increases cotton defence response against Verticillium dahliae by regulating phenylpropanoid metabolism

Abstract

Summary Despite the established significance of WRKY proteins and phenylpropanoid metabolism in plant immunity, how WRKY proteins modulate aspects of the phenylpropanoid pathway remains undetermined. To understand better the role of WRKY proteins in plant defence, we identified a cotton (Gossypium hirsutum) protein, GhWRKY41, that is, universally and rapidly induced in three disease‐resistant cotton cultivars following inoculation with the plant pathogenic fungus, Verticillium dahliae. We show that overexpression of GhWRKY41 in transgenic cotton and Arabidopsis enhances resistance to V. dahliae, while knock‐down increases cotton more susceptibility to the fungus. GhWRKY41 physically interacts with itself and directly activates its own transcription. A genome‐wide chromatin immunoprecipitation and high‐throughput sequencing (ChIP‐seq), in combination with RNA sequencing (RNA‐seq) analyses, revealed that 43.1% of GhWRKY41‐binding genes were up‐regulated in cotton upon inoculation with V. dahliae, including several phenylpropanoid metabolism master switches, receptor kinases, and disease resistance‐related proteins. We also show that GhWRKY41 homodimer directly activates the expression of GhC4H and Gh4CL, thereby modulating the accumulation of lignin and flavonoids. This finding expands our understanding of WRKY‐WRKY protein interactions and provides important insights into the regulation of the phenylpropanoid pathway in plant immune responses by a WRKY protein.

An Oxidoreductase-like Protein is Required for Verticillium dahliae Infection and Participates in the Metabolism of Host Plant Defensive Compounds

“…This adaptation increases the host’s resilience to changes in external environments. , The inhibitory effects of phenylpropanoids, such as caffeic acid, ferulic acid, naringin, and quercetin, on V. dahliae have been observed. , Plant organic heterocyclic compounds are another kind of secondary metabolite that exhibit antimicrobial activity. , In this study, metabolomic analysis revealed that the levels of 10 organic heterocyclic compounds and 4 phenylpropanoids were significantly increased in Δ VdOrlp -infected plants than in wild-type plants. Gayoso et al showed that the levels of phenylpropanoid metabolic products, including ferulic acid, vanillin, and p -coumaric acid, were significantly increased in tomato resistant to V.…”

“…35,36 The inhibitory effects of phenylpropanoids, such as caffeic acid, ferulic acid, naringin, and quercetin, on V. dahliae have been observed. 37,38 Plant organic heterocyclic compounds are another kind of secondary metabolite that exhibit antimicrobial activity. 39,40 In this study, metabolomic analysis revealed that the levels of 10 organic heterocyclic compounds and 4 phenylpropanoids were significantly increased in ΔVdOrlp-infected plants than in wild-type plants.…”

Transcriptome analysis reveals defense-related genes and pathways during dodder (Cuscuta australis) parasitism on white clover (Trifolium repens)

“…Accumulation studies have shown that WRKYs are responsible for plant defense response to abiotic and biotic stresses ( Wani et al, 2021 ). For example, in cotton, GhWRKY41 directly activates the expression of GhC4H and Gh4CL , thereby contributing to the accumulation of flavonoids and lignin and enhancing the defense against Verticillium dahlia ( Xiao et al, 2023 ). In a recent report, the resistant tomato cultivar Heinz showed a lignin-based resistance against field dodder parasitism ( Jhu et al, 2022 ), which was regulated by a CC-NBS-LRR gene and three transcription factors, SIWRKY16 , SIMYB55, and an AP2 transcription factor LIF1 .…”

Interactions between Verticillium dahliae and cotton: pathogenic mechanism and cotton resistance mechanism to Verticillium wilt

“…Luo et al found that the biosynthetic pathway of flavonoids was activated under phosphatedeficient conditions, thereby enhancing the resistance of cotton to V. dahliae (Luo et al, 2021). Moreover, GhWRKY41 positively regulated the cotton resistance to V. dahliae by enhancing the accumulation of flavonoids (Xiao et al, 2023). Molecular mechanisms of cotton resistance to V. dahliae infection.…”

“…Knock-down of GbTSA1 (tryptophan synthase a) and GbTSB1 (tryptophan synthase b) enhanced the accumulation of indole, thereby activating SA biosynthesis and defense signaling pathways and improving cotton resistance to V. dahliae (Miao et al, 2019). Moreover, the miR530-GhSAP6 module in cotton leaves responded remotely to V. dahliae infection from roots via SAR, and then enlarged SA signaling at locations farther from the injection sites, leading to enhanced resistance of cotton plants to V. dahliae (Hu et al, 2023).…”