Convergent molecular evolution among ash species resistant to the Emerald Ash Borer

Authors: KELLEY, LAURA - University Of London; PLUMB, WILLIAM - University Of London; CAREY, DAVID - Us Forest Service (FS); MASON, MARY - The Ohio State University; COOPER, ENDYMION - University Of London; CROWTHER, WILLIAM - University Of London; Whittemore, Alan; ROSSITER, STEPHEN - University Of London; KOCH, JENNIFER - Us Forest Service (FS); BUGGS, RICHARD - University Of London

Submitted to: Nature Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/16/2020
Publication Date: 5/25/2020
Citation: Kelley, L.J., Plumb, W.J., Carey, D.W., Mason, M.E., Cooper, E.D., Crowther, W., Whittemore, A.T., Rossiter, S.J., Koch, J.L., Buggs, R.J. 2020. Convergent molecular evolution among ash species resistant to the Emerald Ash Borer. Nature Ecology and Evolution. 4:1116-1128. https://doi.org/10.1038/s41559-020-1209-3.
DOI: https://doi.org/10.1038/s41559-020-1209-3

Interpretive Summary: Over the past twenty years, ash trees (Fraxinus species) in the U.S. have been decimated by a highly destructive insect pest, the emerald ash borer (EAB), native to east Asia. EAB has now spread across much of eastern North America and caused significant ecological and economic impact, with the effects of damage to ash trees estimated in the tens of billions of dollars. An international team of scientists compared sequences of genes in resistant and susceptible ash species and identified 53 genes whose structure is correlated with EAB resistance in multiple unrelated groups of ash. This is the first study that used genome-wide analysis to identify the types of genes involved in resistance to EAB in ash species. This data will be useful to target genes that could increase resistance of ash species to EAB through breeding or gene editing.

Technical Abstract: 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. Assembling whole genome sequences for 25 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.