Genes for ash tree resistance to an insect pest identified via comparative genomics

Genome-wide discovery of candidate genes for functional traits within a species typically involves the sequencing of large samples of phenotyped individuals, or linkage analysis through multiple generations. When a trait occurs repeatedly among phylogenetically independent lineages within a genus, a more efficient approach may be to identify genes via detection of amino acid residues shared by species possessing that trait. Here, by taking this approach, we identify candidate loci in the genus Fraxinus (ash trees) for resistance to the emerald ash borer beetle (EAB; Agrilus planipennis), a pest species that appears innocuous to otherwise healthy ash in its native East Asian range but is highly destructive in North America and poses a threat to ash trees in Europe. Assembling whole genome sequences for 24 diploid species and subspecies of ash, and estimating resistance to EAB for 26 taxa from egg bioassays, we find 53 genes containing amino acid variants shared between two or more independent Fraxinus lineages with EAB-resistant species, that are unlikely to be due to chance or undetected paralogy. Of these, seven genes have putative roles relating to the phenylpropanoid biosynthesis pathway and 17 are potentially connected to herbivore recognition, defence signalling or programmed cell death. We also find that possible loss-of-function mutations among our 53 candidate genes are more frequent in susceptible species, than in resistant ones. Patterns of polymorphism for the EAB-associated amino acid variants in ash trees representing different European populations suggest that selection may be able to enhance their resistance to EAB.