Mechanisms of infection and response of the fungal wheat pathogen Zymoseptoria tritici during compatible, incompatible and non-host interactions

Authors: GOMEZ, SANDRA - PURDUE UNIVERSITY; MILLION, CASSIDY - U.S. DEPARTMENT OF AGRICULTURE (USDA); JAISWAL, NAMRATA; GRIBSKOV, MICHAEL - PURDUE UNIVERSITY; Helm, Matthew; Goodwin, Stephen - Steve

Submitted to: Fungal Genetics Conference Proceedings
Publication Type: Abstract Only
Publication Acceptance Date: 2/1/2024
Publication Date: 3/12/2024
Citation: Gomez, S.V., Million, C.R., Jaiswal, N., Gribskov, M., Helm, M.D., Goodwin, S.B. 2024. Mechanisms of infection and response of the fungal wheat pathogen Zymoseptoria tritici during compatible, incompatible and non-host interactions. Fungal Genetics Conference Proceedings. ABSTRACT.

Interpretive Summary: N/A

Technical Abstract: Zymoseptoria tritici causes Septoria tritici blotch (STB) on wheat. Despite the importance of this disease, our understanding of the infection strategy and the arsenal of candidate effectors that are activated by the pathogen, is currently limited. To investigate the infection phase-specific gene expression in Z. tritici, we analyzed the transcriptome activation response 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). We observed dramatic differences in pathogen gene expression at 10 DPI in the compatible compared to both incompatible interactions. A total of 275 and 226 genes in Z. tritici were expressed at 10 DPI during the compatible interaction compared to the incompatible interactions with Veranopolis and Israel 493, respectively. This correlates with the initiation of the necrotrophic lifestyle of the pathogen. We observed a significant up-regulation of genes at 10 DPI that encode carbohydrate-active enzymes (CAZymes). The largest differences in pathogen gene expression occurred at 3 DPI in both compatible and incompatible interactions compared to the non-host interaction. Of the Z. tritici genes that were significantly expressed at 1 and 3 DAI in the compatible interaction, we identified thirty-one putative effectors. Subsequent subcellular localization studies using Agrobacterium-mediated transient expression in Nicotiana benthamiana revealed two candidate effectors that localize 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. We found that the genome of Z. tritici encodes four CAP-domain-containing PR-1-like proteins. Two of them contain a predicted signal peptide. However, only Mycgr3109710 is predicted as an effector. Mycgr3109710 contains three CAP signature motifs and a conserved CNY motif, which is important for the immunity activity of PR-1s in plants and is present in PR-1-like proteins with confirmed virulence activity in other fungal pathogens. We are investigating the evolution of PR-1-like proteins in the genomes of 19 Z. tritici isolates, four sister Zymoseptoria species, and selected Dothideomycetes species through comparative genomics and phylogenetic reconstruction.