An accumulation of genetic variation and selection across the disease-related genes during apple domestication

Although human-imposed selection is known to have altered plant traits during crop domestication, the effect of selection on host susceptibility or resistance is not well understood. Moreover, the domestication of perennial tree fruit crops, unlike annual crops, was driven by hybridization, clonal propagation, and selection of desirable phenotypes, which could confound the accurate assessment of domestication-associated effects on host resistance or susceptibility genes. We studied the effects of domestication on disease-related nucleotide-binding leucine-rich repeat (NLR) genes by combining phylogenetic, haplotype, and selection signature analysis using sequence data from Golden Delicious double haploid (GDDH13 v.1.1) apple genome and 80 resequenced domesticated and wild Malus accessions. The NLR gene family in the GDDH13 v.1.1 apple genome constituted 546 genes that showed expansion mainly through proximal (39.1%) and dispersed (29.5%) duplications. The genome duplication (WGD) within Rosaceae, affecting the Malus lineage, is also evident in the NLR genes. The NLR genes are found in genomic regions associated with previously detected disease resistance-related quantitative trait loci (QTL) for apple scab, fire blight, powdery mildew, and blue mold. A genomic diversity analysis identified that the NLR genes in domesticated apples (Malus domestica) have more variation (average πdom=4.01 × 10−3) than their main progenitor, wild M. sieversii (average πsie=2.95 × 10−3) and M. sylvestris (average πsyl=2.11 × 10−3), which hybridized with M. domestica during the domestication process. These results suggest evidence of selection on disease-related genes associated with domestication of apple. An increased diversity across NLR genes in the domesticated germplasm may be attributed to their diverse geographical origins and distinct pedigrees, together with selection for disease resistance during domestication. The NLR genes under selection can provide opportunities to explore their role in disease resistance in apples.