GhMYB4 downregulates lignin biosynthesis and enhances cotton resistance to Verticillium dahliae

Authors: XIAO, SHENGHUA - Huazhong Agricultural University; HU, QIN - Hubei University; SHEN, JILI - Shihezi University; LIU, SHIMING - Huazhong Agricultural University; YANG, ZHAOGUANG - Huazhong Agricultural University; CHEN, KUN - Huazhong Agricultural University; Klosterman, Steven; JAVORNIK, BRANKA - University Of Ljubljana; ZHANG, XIANLONG - Huazhong Agricultural University; ZHU, LONGFU - Huazhong Agricultural University

Submitted to: Plant Cell Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/3/2021
Publication Date: 2/27/2021
Citation: Xiao, S., Hu, Q., Shen, J., Liu, S., Yang, Z., Chen, K., Klosterman, S.J., Javornik, B., Zhang, X., Zhu, L. 2021. GhMYB4 downregulates lignin biosynthesis and enhances cotton resistance to Verticillium dahliae. Plant Cell Reports. 40:735-751. https://doi.org/10.1007/s00299-021-02672-x.
DOI: https://doi.org/10.1007/s00299-021-02672-x

Interpretive Summary: The soil-borne fungus Verticillium dahliae causes wilt disease of economically important crops worldwide, including on cotton. Typically, the research literature indicates plant defenses against pathogens are bolstered by increased lignification of plant tissues. Interestingly, in this study, a gene named GhMYB4 which suppresses lignin synthesis in cotton, was overexpressed in cotton and Arabidopsis plants and led to increased disease resistance to V. dahliae. This may be explained by the accompanying alterations in plant cell wall integrity and increases in oligosaccharide or sugar molecules detected in the GhMYB4 overexpressing plants. We hypothesized that the oligosaccharides released from the plants act as damage-associated molecular patterns elicit plant defense responses and this is supported by the evidence presented in this study. This work increases our understanding of the complexities of the roles of lignin and its biosynthesis in plant defense responses.

Technical Abstract: Verticillium wilt of cotton (Gossypium hirsutum) caused by the soil-borne fungus Verticillium dahliae (V. dahliae) represents one of the most important constraints of cotton production worldwide. Mining of the genes involved in disease resistance and illuminating the molecular mechanisms that underlie this resistance is of great importance in cotton breeding programs. Defense-induced lignification in plants is necessary for innate immunity, and there are reports of a correlation between increased lignification and disease resistance. In this study, we present an example in cotton whereby plants with reduced lignin content also exhibit enhanced disease resistance. We identified a negative regulator of lignin synthesis, in cotton encoded in GhMYB4. Overexpression of GhMYB4 in cotton and Arabidopsis enhanced resistance to V. dahliae with reduced lignin deposition. Moreover, GhMYB4 could bind the promoters of several genes involved in lignin synthesis, such as GhC4H-1, GhC4H-2, Gh4CL-4, and GhCAD-3, and impair their expression. The reduction of lignin content in GhMYB4-overexpressing cotton led to alterations of cell wall integrity (CWI) and released more oligogalacturonides (OGs) which may act as damage-associated molecular patterns (DAMPs) to stimulate plant defense responses. In support of this hypothesis, exogenous application with polygalacturonic acid (PGA) in cotton activated biosynthesis of jasmonic acid (JA) and JA-mediated defense against V. dahliae, similar to that described for cotton plants overexpressing GhMYB4. This study provides a new candidate gene for cotton disease-resistant breeding and an increased understanding of the relationship between lignin synthesis, OG release, and plant immunity.