Fruit Quality Traits Have Played Critical Roles in Domestication of the Apple

With its long history of cultivation, the domesticated apple, Malus × domestica Borkh., is an excellent model for studying domestication in long-lived perennial plants. As apples have been transported from their center of origin in the Tian Shan region in central Asia and moved along the famous Silk Road trading path, they have undergone selection for distinct phenotypic traits. In this study, a high-throughput single nucleotide polymorphism (SNP) genotyping assay is used to investigate relationships of Malus species, draw inferences on the domestication history, identify traits critical for domestication, and assess potential genetic loci under selection. A total of 160 Malus accessions, including wild species, old and new apple cultivars, and advanced selections, were genotyped. Of 1536 SNPs from GoldenGate oligonucleotide pool assays (OPAs), 901 SNPs fulfilled filtering criteria. A principal component analysis (PCA) revealed that most M. × domestica accessions grouped together. A total of 67 loci, including 13 genomic SNPs and 54 genic SNPs, have been identified as potential targets for selection during evolution of the apple genome from its wild progenitor M. sieversii. Genes introgressed from local wild species into M. × domestica are associated with adaptation to local environments, while genes for fruit quality traits are derived from M. sieversii. Since ancient times, plants have been undergoing selection for desirable traits through the process of domestication. During domestication, wild species of plants and animals undergo intensive artificial selection based on desirable morphological characters that eventually fixes beneficial alleles derived from wild species or from new mutations (Paran and Van der Knaap, 2007), collectively referred to as the “domestication syndrome” (Hammer, 1984). Over many centuries, selection for traits of interest has gone on both intentionally, with targeted desired traits, and unintentionally, by propagating favorable phenotypes of each generation (Gepts, 2004). Domestication of species provides not only insights into cultures and lifestyles of human civilizations, but also serves as a well-designed natural experiment to gain new knowledge about evolution, and allows us to pursue studies on the influence of selection on modifying functions of genes controlling desirable traits (Purugganan and Fuller, 2009; Olsen and Wendel, 2013). To date, several studies have focused on the genetics and genomics of the Published in The Plant Genome 7 doi: 10.3835/plantgenome2014.04.0018 © Crop Science Society of America 5585 Guilford Rd., Madison, WI 53711 USA An open-access publication All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher. M.A. Khan, and S.S. Korban, Dep. of Natural Resources & Environmental Sciences, and V. Sovero and M. M. Kushad, Dep. of Crop Sciences, Univ. of Illinois, Urbana, IL 61801; K.M. Olsen, Dep. of Biology, Washington Univ., St. Louis, MO 63130-4899; S.S. Korban, Dep. of Biology, Univ. of Massachusetts-Boston, Boston 02125. M.A. Khan, current address, International Potato Center (CIP), La Molina, Lima, Peru. Received 25 Apr. 2014. *Corresponding author ([email protected]). Abbreviations: EST, expressed sequence tag; Fst, subpopulation relative to the total variance; GWAS, Genome-Wide Association Study in Genome Association and Prediction Integrated Tool, an R package; IBS, identity-by-state matrix; K, number of subpopulations; LD, linkage disequilibrium; LG, linkage group; NADP, nicotinamide adenine dinucleotide phosphate; NCBI, National Center for Biotechnology Information; OPA, oligonucleotide pool assay; PC, principal component; PCA, principal component analysis; QTL, quantitative trait locus; SNP, single nucleotide polymorphism. Published October 31, 2014