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

Abstract

Knowledge of genetic determinism and evolutionary dynamics mediating host-pathogen interactions is essential to manage fungal plant diseases. However, the genetic architecture of fungal pathogenicity remains poorly understood, and studies often focus on large-effect effector genes triggering strong, qualitative resistance. It is not clear how this translates to predominately quantitative pathogens. Here, we used the Zymoseptoria tritici-wheat model to elucidate the genetic architecture of quantitative pathogenicity and mechanisms mediating host adaptation. Z. tritici is a globally occurring pathogen that causes severe yield losses on wheat. We perform whole-genome sequencing of 103 isolates and quantified pathogenicity traits on 12 cultivars harbouring different resistance genes. We perform a multi-host GWAS and identified 58 candidate genes associated with pathogenicity, of which nineteen are highly expressed and/or differentially expressed in planta. Two of these had large effects and three were shared in more than one cultivar, suggesting that Z. tritici pathogenicity is predominantly quantitative and host-specific. Analysis of genetic diversity revealed that sequence polymorphism is the main evolutionary process mediating differences in quantitative pathogenicity, a process that is likely facilitated by genetic recombination and transposable elements dynamics. We found signatures of positive diversifying selection in ~68% of the candidate genes acting on specific amino acid substitutions, likely responsible for evasion of host recognition. Finally, we used functional approaches to confirm the role of an effector-like gene and a methyltransferase in quantitative pathogenicity. This study highlights the complex genetic architecture of quantitative pathogenicity, extensive diversifying selection and plausible mechanisms facilitating pathogen adaptation.

Population-level whole genome sequencing ofAscochyta rabieiidentifies genomic loci associated with isolate aggressiveness

“…Classic genome-wide association studies, which are commonly used for identification of loci associated with target phenotypic traits in fungal plants pathogens with frequent cycles of sexual reproduction (63)(64)(65), are only relevant in the presence of recombination (66). Such methods are not appropriate for identifying associations of phenotype and genotypes in strongly clonal populations with long-range linkage disequilibrium and population stratification.…”

Septoria tritici blotch resistance geneStb15encodes a lectin receptor-like kinase

“…effector 44 , which may also be the case for Stb15. A candidate gene for AvrStb15 encoding a small secreted protein (SSP) has been suggested 45 , but further work will be needed to determine the nature of its interaction with Stb15. There is thus far no evidence of a direct interaction between Stb6 and AvrStb6, also encoding a cysteine-rich SSP 3,46,47 .…”

A novel genome-wide association approach reveals wheat pathogen genes involved in host specialization

“…The utilization of GWAS to identify microbial pathogenicity factors lags far behind compared to plants 7 . In microbes, GWAS has primarily been used to discover genomic traits involved in pathogenicity and fungicide resistance, but these advances required prior knowledge regarding the host or fungicide phenotypes [8][9][10][11][12][13][14] . One reason for the relative lack of GWAS applications to plant pathogenic microbes is the scarcity of extensive collections of genome-sequenced pathogen strains.…”