Molecular convergence analyses identify candidate genes for low susceptibility to the ash dieback pathogen

Abstract

Non-native pests and pathogens increasingly threaten global forest ecosystems. An understanding of the genomic basis of low susceptibility in the natural hosts of such pests and pathogens, with which they share a coevolutionary history, can enhance restoration efforts by facilitating the selection of individuals carrying beneficial alleles. Within the genus Fraxinus (ash trees) low susceptibility to the fungal pathogen Hymenoscyphus fraxineus, the causative agent of the ash dieback disease (ADB) epidemic, is observed in three independent lineages of known or plausible natural hosts. Here, we seek to elucidate the genetic basis of this trait, which is key to the future survival of Fraxinus excelsior populations in Europe, using a molecular convergence approach. We analysed 4,300 protein-coding loci for amino acid convergence between lineages with low susceptibility. After filtering for potential false positives, we find 62 genes that have a signal of excess convergence between Fraxinus lineages with low ADB susceptibility. Eleven of these loci have additional evidence for a role in defence against fungal pathogens, with a further 17 linked to more general immunity or defence, or other functions relevant to the response against ADB such as cell wall biogenesis. The candidate loci discovered here complement those reported by previous genomic studies of F. excelsior, and can be targeted in efforts to mitigate the devastation caused by this deadly disease by informing breeding programmes involving hybridisation and marker-assisted back-crossing. Our study demonstrates the benefit of genomic analyses incorporating natural hosts, when seeking to tackle biotic threats to naive host populations. Significance StatementKnowledge of the genomic basis of variation in susceptibility to emerging forest pests and pathogens can provide the foundation for interventions to mitigate such threats, but studies restricted to the analysis of naive host populations may miss relevant genomic loci that could be present in coevolved hosts. Using comparative genomic analyses for the detection of molecular convergence between lineages of ash trees with low susceptibility to ash dieback, incorporating known and plausible natural hosts, we detect novel candidate loci for defence against this disease. Our findings can be used to support efforts to tackle one of the worlds worst forest pathogens and demonstrate the value of integrating genomic data from coevolved hosts when aiming to identify the basis of low susceptibility to biotic threats.