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J Exp Bot. 2019 Aug 27. pii: erz332. doi: 10.1093/jxb/erz332. [Epub ahead of print]

Gene-set association and epistatic analyses reveal complex gene interaction networks affecting flowering time in a worldwide barley collection.

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Western Barley Genetics Alliance, Western Australian State Agricultural Biotechnology Centre, College of Science, Health, Engineering and Education, Murdoch University, Murdoch, WA, Australia.
SAGI-WEST, Faculty of Science and Engineering, Curtin University, Bentley, WA, Australia.
InterGrain Pty Ltd WA, Australia.
Australian Grain Technologies Pty Ltd (AGT), SA, Australia.
Agriculture and Food, Department of Primary Industries and Regional Development, South Perth, WA, Australia.
Hubei Collaborative Innovation Centre for Grain Industry, Yangtze University, Hubei Jingzhou, China.


Single-marker genome-wide association studies (GWAS) have successfully detected associations between single nucleotide polymorphisms (SNPs) and agronomic traits such as flowering time and grain yield in barley. However, the analysis of individual SNPs can only account for a small proportion of genetic variation, and can only provide limited knowledge on gene network interactions. Gene-based GWAS approaches provide enormous opportunity both to combine genetic information and to examine interactions among genetic variants. Here, we revisited a previously published phenotypic and genotypic data set of 895 barley varieties grown in two years at four different field locations in Australia. We employed statistical models to examine gene-phenotype associations, as well as two-way epistasis analyses to increase the capability to find novel genes that have significant roles in controlling flowering time in barley. Genetic associations were tested between flowering time and corresponding genotypes of 174 putative flowering time-related genes. Gene-phenotype association analysis detected 113 genes associated with flowering time in barley, demonstrating the unprecedented power of gene-based analysis. Subsequent two-way epistasis analysis revealed 19 pairs of gene√ógene interactions involved in controlling flowering time. Our study demonstrates that gene-based association approaches can provide higher capacity for future crop improvement to increase crop performance and adaptation to different environments.


Barley; GWAS; epistasis; flowering time; gene-set association analysis; heritability; next-generation sequencing; phenology; target capture; target enrichment


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