Partial resistance in wheat is triggered upon recognition of an avirulence gene

Lukas Meile 1 Clémence Plissonneau 1 Fanny E. Hartmann 3 Patrick C. Brunner 1 Parvathy Krishnan 1 Daniel Croll 2 Bruce A. McDonald 1 Andrea Sánchez-Vallet 1
1Environmental Systems Science, ETH, Zurich, Switzerland
2Laboratory of Evolutionary Genetics, University of Neuchâtel, Neuchatel, Switzerland
3Ecologie Systématique Evolution, University Paris Sud, Orsay, France

Adaptation of fungal pathogens to colonize a plant often involves escape from host surveillance. This can be mediated by sequence polymorphism of avirulence genes that evolve to prevent recognition by host resistance genes. Despite the ubiquity and importance of avirulence genes for the infection outcome, the mechanisms behind their evolution remain undetermined. The causal agent of Septoria Tritici Blotch on wheat, Zymoseptoria tritici, is a necrotrophic pathogen that is globally distributed. Resistance is mediated by 21 mapped major resistance genes, of which many lead to partial resistance. It still remains unknown what components are recognized by these particular resistance genes. In order to elucidate the genetic basis of quantitative virulence, a genetic mapping approach was undertaken. Differences between two isolates were mapped to a transposable element-rich and highly dynamic genomic region that included a cluster of four genes encoding putative effectors. We confirmed that one of the genes, Avr3D1, encodes an avirulence protein that is specifically recognized by some wheat cultivars. Disruption of Avr3D1 in the avirulent isolate led to an increase in virulence on the resistant hosts. Complementation experiments demonstrated that polymorphism in the coding sequence is responsible for the differences in virulence between the two isolates. Population genetics analyses showed that Avr3D1 is present in all of 132 investigated isolates from around the world and that it has evolved under diversifying selection. In contrast, the transposable elements and the putative effector genes surrounding Avr3D1 are under presence/absence polymorphism. Genes in the cluster were shown to be silenced in vitro but highly up-regulated during infection. Thus, we identified a novel avirulence gene whose recognition leads to partial resistance. Its high controlled gene expression regulation, its clear signs of diversifying selection and its localization in a highly dynamic genomic environment provide us with evidences of the evolution of this avirulence gene to escape recognition.