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

Authors: XIAO, SHENGHUA - Huazhong Agricultural University; MING, YUQING - Huazhong Agricultural University; HU, QIN - Huazhong Agricultural University; YE, ZHENGXIU - Huazhong Agricultural University; SI, HUAN - Huazhong Agricultural University; LIU, SHIMING - Huazhong Agricultural University; ZHANG, XIAOJUN - Huazhong Agricultural University; WANG, WEIRAN - Xinjiang Academy Of Agricultural And Reclamation Science; YU, YU - Xinjiang Academy Of Agricultural And Reclamation Science; KONG, JIE - Xinjiang Academy Of Agricultural And Reclamation Science; Klosterman, Steven; LINDSEY, KEITH - University Of Durham; ZHANG, XIANLONG - Huazhong Agricultural University; AIERXI, ALIFU - Xinjiang Academy Of Agricultural And Reclamation Science; ZHU, LONGFU - Huazhong Agricultural University

Submitted to: Plant Biotechnology Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/24/2022
Publication Date: 1/12/2023
Citation: Xiao, S., Ming, Y., Hu, Q., Ye, Z., Si, H., Liu, S., Zhang, X., Wang, W., Yu, Y., Kong, J., Klosterman, S.J., Lindsey, K., Zhang, X., Aierxi, A., Zhu, L. 2023. GhWRKY41 forms a positive feedback regulation loop and increases cotton defense response against Verticillium dahliae by regulating phenylpropanoid metabolism. Plant Biotechnology Journal. 21(5):961-978. https://doi.org/10.1111/pbi.14008.
DOI: https://doi.org/10.1111/pbi.14008

Interpretive Summary: The soilborne fungus Verticillium dahliae causes vascular wilt disease on important food and fiber crop species worldwide. Developing plant resistance to wilt diseases is necessary for their control, especially with recent limitations on fumigants, and the increased demand for organically produced crops. This study identified a gene in several cotton cultivars that is expressed in response to V. dahliae. The results indicate that the gene encodes a transcription factor that regulates the expression of many defense genes and promotes cell wall strengthening in the plant. The work provides additional tools for more quickly developing Verticillium wilt resistance in cotton and other crops that contain this gene.

Technical Abstract: 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.