A secreted protease-like protein in Zymoseptoria triticiis responsible for avirulence on Stb9resistance 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 factor AvrStb9using association mapping and functional validation approaches. Pathotyping AvrStb9transgenic strains on Stb9cultivars, near isogenic lines and wheat mapping populations, showed that AvrStb9interacts with Stb9resistance gene, triggering an 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 global Z. 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.

Author Summary

Fungal avirulence ( Avr) genes are involved in gene-for-gene relationships with host resistance genes. Avrgenes may at the same time target host defenses to allow infection and be recognized by a host resistance gene triggering a defense response. The fungus Zymoseptoria triticicauses Septoria tritici blotch, a major disease of wheat worldwide. Z. triticipopulations rapidly adapt to selection pressures such as host resistance, leading to resistance breakdown. We report the identification of the avirulence gene AvrStb9based on genetic mapping, sequence polymorphisms and allele swapping. AvrStb9is involved in the interaction with Stb9resistance gene following the gene-for-gene model, and its recognition hinders disease symptoms in hosts carrying the corresponding resistance gene. Unlike other known Z. tritici Avreffectors, AvrStb9encodes for an unusually large Avr protein with a predicted protease S41 domain conserved among diverse ascomycete lineages. We also highlight several gene mutations likely involved in escaping Stb9-mediated recognition.