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

Authors: SINGH, JUGPREET - Cornell University; SUN, MANYI - Nanjing Agricultural University; Cannon, Steven; WU, JUN - Nanjing Agricultural University; KHAN, AWAIS - Cornell University

Submitted to: Tree Genetics and Genomes
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/21/2021
Publication Date: 5/2/2021
Citation: Singh, J., Sun, M., Cannon, S.B., Wu, J., Khan, A. 2021. An accumulation of genetic variation and selection across the disease-related genes during apple domestication. Tree Genetics and Genomes. 17. Article 29. https://doi.org/10.1007/s11295-021-01510-1.
DOI: https://doi.org/10.1007/s11295-021-01510-1

Interpretive Summary: Apple, an important crop in the U.S. and worldwide, faces many disease challenges. Its genetics are also complex, and breeding is made more difficult due to the many years required to evaluate a new variety grown from seed. This study describes a set of several hundred genes associated with disease resistance, identified in the sequenced genome of the Golden Delicious variety. Genetic variation was also assessed between these genes and the corresponding genes tested in other cultivated varieties and related wild species. Greater variety was observed in the disease resistance genes in cultivated apple than in wild relatives. This may be due to the complex history of domesticated apple, which involved crosses and contributions from several wild species, as apple developed as a crop over many centuries in Asia and Europe. This study also finds particular disease resistance genes associated with genetic locations previously identified for resistance to several serious apple diseases: apple scab, fire blight, powdery mildew and blue mold. This work will help apple breeders and geneticists to more quickly and effectively select new, disease-resistant apple varieties.

Technical Abstract: Although human imposed selection has altered plant traits during crop domestication, the effect of selection on host susceptibility or resistance is not well understood. Moreover, unlike annual crops, the domestication of tree fruit crops was driven by hybridization, selection of desirable phenotypes, and clonal propagation. This work describes the effects of domestication on disease-related NLR (nucleotide binding–leucine-rich repeat) genes by combining phylogenetic, haplotype, and selection signature analysis in apples. The NLR gene family in the Golden Delicious double haploid (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, are also evident in the NLR genes. The NLR genes are found in genomic regions associated with previously detected disease-related 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 greater diversity than the wild M. sieversii and Malus sylvestris groups, suggesting evidence of selection for disease resistance associated with domestication. An increased diversity across NLR genes in the domesticated Malus germplasm may be attributed to the diverse geographical origins and genetic contributions in the genetic background of domesticated apple, together with selection for disease resistance during domestication. The results from this study are useful to study the role of NLR genes in disease resistance in apples.