A secreted protease-like protein inZymoseptoria triticiis responsible for avirulence onStb9resistance gene in wheat

Abstract

Zymoseptoria triticiis the fungal pathogen responsible for Septoria tritici blotch on wheat. Disease outcome in this pathosystem is partly determined by isolate-specific resistance, where wheat resistance genes recognize specific fungal factors triggering an immune response. Despite the large number of known wheat resistance genes, fungal molecular determinants involved in such cultivar-specific resistance remain largely unknown. We identified the avirulence factorAvrStb9using association mapping and functional validation approaches. PathotypingAvrStb9transgenic strains onStb9cultivars, near isogenic lines and wheat mapping populations, showed thatAvrStb9interacts withStb9resistance gene, triggering a strong immune response.AvrStb9encodes an unusually large avirulence gene with a predicted secretion signal and a protease domain. It belongs to a S41 protease family conserved across different filamentous fungi in the Ascomycota class and may constitute a core effector.AvrStb9is also conserved among a globalZ. triticipopulation and carries multiple amino acid substitutions caused by strong positive diversifying selection. These results demonstrate the contribution of an ′atypical′ conserved effector protein to fungal avirulence and the role of sequence diversification in the escape of host recognition, adding to our understanding of host-pathogen interactions and the evolutionary processes underlying pathogen adaptation.

Quantitative pathogenicity and host adaptation in a fungal plant pathogen revealed by whole-genome sequencing

“…To date, three Z. tritici pathogenicity genes encoding avirulence factors have been cloned. These include AvrStb6 and AvrStb9 that are recognized by the R genes Stb6 and Stb9, respectively, and lead to a strong qualitative resistance response (Amezrou et al, 2022;Kema et al, 2018;Zhong et al, 2017), and Avr3D1 which triggers quantitative resistance on cultivars harbouring Stb7 or Stb12 (Meile et al, 2018). In addition to the above-mentioned R genes, 18 other race-specific Stb resistance genes and numerous quantitative resistance loci have been genetically mapped in wheat (Brown et al, 2015), but only Stb6 and Stb16q have been cloned to date (Saintenac et al, 2018(Saintenac et al, , 2021).…”

“…In the case of antagonistic host-pathogen interactions, the fate of genetic variation is determined partly by the selection pressure exerted by host R proteins. This is especially true when R genes and effectors are involved in a gene-for-gene (GFG) relationship [9][10][11][12] . Moreover, the diversity of host genotypes in Rgene content exerts heterogeneous selection pressure on pathogen populations, giving rise to the comaintenance of multiple pathogen variants better adapted to specific subsets of hosts 3,13 .…”

Sas3-mediated histone acetylation regulates effector gene activation in a fungal plant pathogen

“…We hypothesized that histone acetylation might be required for effector gene upregulation. We determined the expression levels of 4 effector genes ( Avr3D1 (3D7.g7883 reannotated in (24)), AvrStb6 (3D7.g5586), AvrStb9 (3D7.g741 ; (32)), and Mycgr3G76589 (3D7.g10118) ) by qRT-PCR during plant infection in KAT knockouts (Figure 6). The expression levels of Avr3D1 and AvrStb6 were higher in Δ Ngs1 and Δ Gcn5 , while AvrStb6 expression was reduced in Δ Sas2 and Δ Sas3 at 10 dpi (Figures 6A and 6B).…”

Multiplexed effector screening for recognition by endogenous resistance genes using positive defense reporters in wheat protoplasts

“…(formerly known as Blumeria graminis f. sp. tritici) Avr genes (Praz et al, 2017;Bourras et al, 2019;Hewitt et al, 2021;M€ uller et al, 2022), three for Zymoseptoria tritici (Zhong et al, 2017;Meile et al, 2018;Amezrou et al, 2023), and five for Puccinia graminis f. sp. tritici (Pgt; Chen et al, 2017;Salcedo et al, 2017;Upadhyaya et al, 2021;Arndell et al, 2023).…”