GWAS-based population genetic analysis identifies bZIP29 as a heterotic gene in maize

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Understanding the role of heterotic genes in contributing to heterosis is essential for advancing hybrid breeding. We analyzed plant height (PH), ear height (EH), and transcriptomic data from a maize hybrid population. Genome-wide association studies (GWASs) revealed that dominance effects of quantitative trait loci (QTLs) play a significant role in hybrid traits and mid-parent heterosis. By integrating GWAS, expression GWAS (eGWAS), and module eGWAS analysis, we prioritized six candidate heterotic genes underlying six QTLs, including one QTL that spans the bZIP29 gene. In the hybrid population, bZIP29 exhibits additive expression and dominance effects for both hybrid traits and mid-parent heterosis, with its favorable allele correlating positively with PH and EH. bZIP29 demonstrates dominance or over-dominance patterns in hybrids derived from crosses between transgenic and wild-type lines, contingent upon its expression. A tsCUT&Tag assay revealed that bZIP29 protein binds directly to a gene regulated by its associated expression QTL (eQTL) and six genes within expression modules governed by its associated module-eQTLs (meQTLs). Regulatory networks involving bZIP29 are more extensive in hybrid subpopulations than in the parental population. This study offers insights into key heterotic genes and networks that underpin the robust growth of hybrid maize.

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