Dramatic changes in genetic diversity of the avirulence effector AvrStb6 in global populations of the wheat pathogen Zymoseptoria tritici

Septoria tritici blotch (STB), caused by the pathogenic fungus Zymoseptoria tritici, is one of the most commercially important diseases of wheat globally. Recently, both genetic factors of the previously characterised gene-for-gene interaction between Z. tritici and wheat have been identified: the wheat receptor-like kinase Stb6 and the Z. tritici secreted effector protein AvrStb6. Genetic diversity analysis of AvrStb6 in historic collections of Z. tritici from global populations has been carried out and recently published. However, the prevalence of AvrStb6 haplotypes that may allow evasion of Stb6-mediated defence in modern Z. tritici isolates is currently unknown. We therefore analysed genetic diversity of AvrStb6 in 2016-2017 Z. tritici field populations from the UK, Western Europe, USA, South America, and Australia.
This study revealed that, whilst AvrStb6 is present in all modern isolates tested, remarkably, a small number of haplotypes - encoding the same protein isoform conditioning virulence on Stb6-containing wheat - currently predominate in different parts of the world. The “original”, avirulence isoform of AvrStb6 was not detected. This contrasts with the data collected in a study focused on the analysis of a largely French Z. tritici population, sampled between 2009-2010, in which this avirulent isoform of AvrStb6 was found to be present in 20% of isolates in the collection (Zhong et al. 2017). Data collected on a global Z. tritici population sampled from 1990-2001 (Brunner & McDonald, 2018) also suggested a higher diversity of AvrStb6 haplotypes than we have found. Therefore, it appears that in recent years there has been a significant shift in the global Z. tritici populations towards haplotypes encoding a single Stb6 resistance-breaking isoform of Avrstb6. On one hand, evolutionary pressure to evade recognition by Stb6 - found to be present in over 50% of current commercial UK wheat cultivars (Saintenac et al., 2018) - may explain the elimination of avirulence isoforms of AvrStb6. On the other hand, emergence of a particular virulence isoform of this effector protein may contribute to fungal pathogenicity, fitness, or other important traits. This hypothesis will be tested by transgenic introduction of different AvrStb6 haplotypes into an AvrStb6 deletion mutant of Z. tritici followed by characterisation of the resulting fungal strains, including pathoassays on wheat plants possessing or lacking the functional resistance allele of Stb6.
This knowledge would help build an understanding of the relative importance of Stb6 in conferring genetic resistance to modern Z. tritici strains, as well as help identify the mutations that allow evasion of Stb6 detection, helping to further elucidate the function of AvrStb6 in pathogenicity.