Idiosyncratic Patterns of Disease Resistance Gene Adaptation in Three Species in the Rosaceae Detected Using the RosaR80 Framework

Progress in identifying plant disease resistance genes is facilitated by the availability of high-quality reference genomes. We characterized the R gene composition of the apple (Malus × domestica), peach (Prunus persica) and woodland strawberry (Fragaria vesca) genomes using the RosaR80 framework, an analytical pipeline we developed as a community resource for comparative analysis in the Rosaceae. We detected species-specific patterns of NB-encoding gene adaptation: while woodland strawberry has wide representation of lineages from several ancient clades, peach and apple exhibit expansion of species-specific R gene lineages and large chromosomal gene clusters. We suggest an anthropogenic intensification of the molecular arms race as a driver of R gene lineage diversification. Compared to the wild woodland strawberry genome, the genomes of apple and peach represent varieties with prolonged cultivation as monocultures outside their native range. Domestication history influences R gene composition, and repeated selection for resistance to agriculturally relevant pathogens has driven expansion of these R gene lineages. We uncovered evidence for rapid adaptive diversification in response to pathogen pressure in the apple genome, where cloned and candidate genes affording resistance to apple scab (Venturia inaequalis) were derived from large, highly diversified, species-specific R gene lineages. Additionally, the RosaR80 framework revealed five lineages remarkably conserved between all three rosaceous species as well as phylogenetically distant plant species. Future research efforts will expand the RosaR80 framework, providing improved resolution for generating new evolutionary hypotheses, linking specific R gene lineages with specific putative functions, and informing evaluation of genebank collections for R allele discovery.