Comparative transcriptomic analysis of Zymoseptoriatritici reveals interaction-speci¿c gene expression patterns during susceptible, resistant, and nonhost interactions

Authors: GOMEZ, SANDRA - Purdue University; MILLION, CASSIDY - US Department Of Agriculture (USDA); Jaiswal, Namrata; GRIBSKOV, MICHAEL - Purdue University; Helm, Matthew; Goodwin, Stephen

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/25/2025
Publication Date: 12/19/2025
Citation: Gomez-Gutierrez, S.V., Million, C.R., Jaiswal, N., Gribskov, M., Helm, M.D., Goodwin, S.B. 2025. Comparative transcriptomic analysis of Zymoseptoriatritici reveals interaction-speci¿c gene expression patterns during susceptible, resistant, and nonhost interactions. Molecular Plant-Microbe Interactions. https://doi.org/10.1094/MPMI-07-25-0090-R.
DOI: https://doi.org/10.1094/MPMI-07-25-0090-R

Interpretive Summary: Septoria tritici blotch (STB) is one of the most important diseases of wheat worldwide, yet the exact steps taken by the pathogen to cause disease are not known. To begin to unravel this process, we compared pathogen gene expression differences during susceptible and resistant interactions with wheat and barley. The pathogen was inoculated onto a highly susceptible wheat cultivar, two resistant wheat cultivars, and barley, which is not susceptible to STB. RNA samples were collected at six timepoints from 1-23 days after inoculation. Comparison of the pathogen sequences showed large differences in gene expression between infection of wheat versus barley at 3 days after inoculation, and between the susceptible and resistant interactions on wheat at ten days. Thirty-one genes were identified that are likely to be involved in causing disease. Proteins from two of these genes interacted at specific locations in plant cells that indicate possible roles in regulation of host gene expression or defense signaling. These results will help plant pathologists better understand the infection process and identify pathogen genes that may be targeted in strategies for improving resistance to STB.

Technical Abstract: Zymoseptoria tritici incites Septoria tritici blotch, a disease causing significant annual yield losses in wheat. To investigate infection phase-specific gene expression in the pathogen we analyzed gene expression during infection of susceptible (Taichung 29) and resistant (Veranopolis and Israel 493) wheat cultivars, plus the non-host species barley at 1, 3, 6, 10, 17 and 23 days post-inoculation (DPI). There were dramatic differences in pathogen gene expression at 10 DPI in the compatible compared to both incompatible interactions. The largest differences in pathogen gene expression occurred at 3 DPI in both compatible and incompatible interactions compared to the non-host interaction. Thirty-one putative effectors had early expression in the compatible interaction. Subsequent subcellular localization studies using Agrobacterium-mediated transient expression in Nicotiana benthamiana revealed that most candidate effectors localized to the nucleus and cytosol, and two localized to mobile cytosolic bodies, suggesting involvement in intracellular signaling or host gene regulation. Mycgr3109710, which localized to cytosolic bodies, belongs to the non-plant PR-1-like protein family implicated in virulence in other pathogens. Comparison of pathogen gene expression in resistant and susceptible hosts, in which an initial colonization is established, versus in the non-host species, allowed us to identify genes involved in establishing infection. Comparison of the compatible and incompatible interactions identified pathogen genes involved in transition from biotrophic to necrotrophic growth at 10 DPI. In addition, we contribute to the understanding of candidate effectors that are activated early during infection and might be involved in the initial plant immunity suppression.