Characterization of three Fusarium graminearum effectors and their roles during Fusarium head blight

Authors: Hao, Guixia; McCormick, Susan; Usgaard, Thomas; Tiley, Helene; Vaughan, Martha

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/6/2020
Publication Date: 11/30/2020
Citation: Hao, G., McCormick, S., Usgaard, T., Tiley, H., Vaughan, M.M. 2020. Characterization of three Fusarium graminearum effectors and their roles during Fusarium head blight. Frontiers in Plant Science. 11. Article 579553. https://doi.org/10.3389/fpls.2020.579553.
DOI: https://doi.org/10.3389/fpls.2020.579553

Interpretive Summary: The plant fungal pathogen Fusarium graminearum causes Fusarium head blight (FHB) on wheat and barley in the US and worldwide. The disease results in severe yield loss, and more importantly, contaminates grains with mycotoxins that are harmful to humans and animals. To develop novel and effective control methods, it is important to understand how F. graminearum causes FHB. The goal of this study was to discover critical factors involved in initial infection. We found that multiple fungal genes are expressed during the initial stages of FHB development and investigated the role of three of these genes in FHB development. Although these fungal genes only had a minor effect on disease spread, knockout mutants of one gene limited the ability of F. graminearum strains to cause initial infection. This study also demonstrated that multiple genes with minor cumulative roles or functional redundancy contribute to disease development. This knowledge improves our understanding of why it has been so difficult to control FHB and provides valuable information on FHB development and molecular targets for disease and mycotoxin controls.

Technical Abstract: Fusarium graminearum causes Fusarium head blight (FHB) on wheat, barley, and other grains. During infection, F. graminearum produces deoxynivalenol (DON), which contaminates grain and functions as a virulence factor to promote FHB spread throughout the wheat head. F. graminearum secretes hundreds of putative effectors, which can interfere with plant immunity to promote disease development. However, the function of most of these putative effectors remains unknown. In this study, we investigated the expression profiles of 23 F. graminearum effector-coding genes during the early stage of wheat head infection. Gene expression analyses revealed that three effectors, FGSG_01831, FGSG_03599 and FGSG_12160, were highly induced around 272, 170 and 4,300-fold respectively. We generated deletion mutants for these effector genes and performed FHB virulence assays on wheat and barley. The deletion mutants, '01831, '03599 and '12160 reduced FHB spread in wheat heads, but the reductions were not statistically significant. In contrast, '01831 significantly reduced FHB initial infection on wheat and barley, produced significantly less DON on wheat and barley heads. To investigate their potential functions, these three effectors were transiently expressed in Nicotiana benthamiana leaves. N. benthamiana leaves expressing these individual effectors had significantly reduced production of reactive oxygen species (ROS) induced by chitin, but not by flg22. Furthermore, FGSG_01831 and FGSG_03599 suppressed Bax-induced cell death when co-expressed with Bax in N. benthamiana leaves. Our study provides new insights into the functions of these effectors and suggests they play minor cumulative or functionally redundant roles that likely ensure the successful infection against plant resistance.