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Open Access Highly Accessed Research article

Novel genomic approaches unravel genetic architecture of complex traits in apple

Satish Kumar1*, Dorian J Garrick2, Marco CAM Bink3, Claire Whitworth1, David Chagné4 and Richard K Volz1

Author Affiliations

1 The New Zealand Institute for Plant & Food Research Limited, Private Bag 1401, Havelock North 4157, New Zealand

2 Department of Animal Science, Iowa State University, Ames, IA, 50011, USA

3 Biometris, Wageningen University and Research Centre, PO Box 100, Wageningen, 6700AC, Netherlands

4 The New Zealand Institute for Plant & Food Research Limited, Private Bag 11600, Palmerston North, New Zealand

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BMC Genomics 2013, 14:393  doi:10.1186/1471-2164-14-393

Published: 12 June 2013

Abstract

Background

Understanding the genetic architecture of quantitative traits is important for developing genome-based crop improvement methods. Genome-wide association study (GWAS) is a powerful technique for mining novel functional variants. Using a family-based design involving 1,200 apple (Malus × domestica Borkh.) seedlings genotyped for an 8K SNP array, we report the first systematic evaluation of the relative contributions of different genomic regions to various traits related to eating quality and susceptibility to some physiological disorders. Single-SNP analyses models that accounted for population structure, or not, were compared with models fitting all markers simultaneously. The patterns of linkage disequilibrium (LD) were also investigated.

Results

A high degree of LD even at longer distances between markers was observed, and the patterns of LD decay were similar across successive generations. Genomic regions were identified, some of which coincided with known candidate genes, with significant effects on various traits. Phenotypic variation explained by the loci identified through a whole-genome scan ranged from 3% to 25% across different traits, while fitting all markers simultaneously generally provided heritability estimates close to those from pedigree-based analysis. Results from ‘Q+K’ and ‘K’ models were very similar, suggesting that the SNP-based kinship matrix captures most of the underlying population structure. Correlations between allele substitution effects obtained from single-marker and all-marker analyses were about 0.90 for all traits. Use of SNP-derived realized relationships in linear mixed models provided a better goodness-of-fit than pedigree-based expected relationships. Genomic regions with probable pleiotropic effects were supported by the corresponding higher linkage group (LG) level estimated genetic correlations.

Conclusions

The accuracy of artificial selection in plants species can be increased by using more precise marker-derived estimates of realized coefficients of relationships. All-marker analyses that indirectly account for population- and pedigree structure will be a credible alternative to single-SNP analyses in GWAS. This study revealed large differences in the genetic architecture of apple fruit traits, and the marker-trait associations identified here will help develop genome-based breeding methods for apple cultivar development.

Keywords:
GWAS; Linkage disequilibrium; Genetic architecture; Allele substitution effect; Pleiotropy; Malus × domestica