Genomic consequences of apple improvement

Authors: MIGICOVSKY, ZOE - Dalhousie University; GARDNER, KYLE - Dalhousie University; Richards, Christopher; CHAO, THOMAS - Former ARS Employee; SCHWANINGER, HEIDI - Former ARS Employee; Fazio, Gennaro; Zhong, Gan-Yuan; MYLES, SEAN - Dalhousie University

Submitted to: Horticulture Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/9/2020
Publication Date: 1/1/2021
Citation: Migicovsky, Z., Gardner, K., Richards, C.M., Chao, T., Schwaninger, H., Fazio, G., Zhong, G., Myles, S. 2021. Genomic consequences of apple improvement. Horticulture Research. https://doi.org/10.1038/s41438-020-00441-7.
DOI: https://doi.org/10.1038/s41438-020-00441-7

Interpretive Summary: Apple is one of the most economically important fruit crops, with a worldwide production value exceeded only by tomatoes and grapes. Where and how apples were originated are still a subject of wide interest to many apple researchers, because understanding these questions will help breeders identify important genetic variation or diversity (or genes) for breeding new or improving existing apples. While there is an immense amount of genetic variation available in apple, most commercial production focuses on a limited number of elite cultivars. In 2017, over 50% of the commercial apple production in the European Union consisted of only five apple cultivars. The repeated use of a small number of elite cultivars during breeding reduces genetic diversity, especially among commercial cultivars. In addition, clonal propagation allows successful cultivars to persist for long periods of time, such as the ‘McIntosh’ apple which is still in widespread production after 200 years. The ability of the apple industry to respond to pests, pathogens, and a changing climate will rely on comprehensive evaluations of apple variation, and the subsequent introgression of desirable genetic variants into apple breeding material. In this study, we investigated the domestication history of apples by examining its relationship to the progenitor species M. sieversii and M. sylvestris, identified signatures of positive changes during domestication and improvement, and elucidated the improvement history of cultivated apples by examining the relationships among modern cultivars in the USDA apple germplasm collection preserved in Geneva, New York, USA. Our work significantly advanced our knowledge in apple domestication, improvement history and genetic diversity.

Technical Abstract: The apple (Malus domestica) is one of the world’s most commercially important perennial crops and its improvement has been the focus of human effort for thousands of years. Here we genetically characterize over 1,000 apple accessions from the United States Department of Agriculture (USDA) germplasm collection using over 30,000 single nucleotide polymorphisms (SNPs). We confirm the close genetic relationship between modern apple cultivars and their primary progenitor species, M. sieversii from Central Asia, and find that cider apples derive more of their ancestry from the European crabapple, M. sylvestris, than do dessert apples. We determined that most of the USDA collection is a large complex pedigree: over half of the collection is inter-connected by a series of first-degree relationships. In addition, 15% of the accessions have a first-degree relationship with one of the top 10 cultivars sold in the USA. With the exception of ‘Honeycrisp’, the 10 top-selling cultivars are also inter-connected to each other via pedigree relationships. The cultivars ‘Golden Delicious’ and ‘Red Delicious’ were found to have over 60 first-degree relatives, consistent with their repeated use by apple breeders. We detected a signature of intense selection for red skin and provide evidence that breeders also selected for increased firmness. Our results suggest that Americans are eating apples largely from a single family tree and that the apple’s future improvement will benefit from increased exploitation of its tremendous natural genetic diversity.