Comparative population genomics of maize domestication and improvement

Abstract

Domestication and plant breeding are ongoing 10,000-year-old evolutionary experiments that have radically altered wild species to meet human needs. Maize has undergone a particularly striking transformation. Researchers have sought for decades to identify the genes underlying maize evolution, but these efforts have been limited in scope. Here, we report a comprehensive assessment of the evolution of modern maize based on the genome-wide resequencing of 75 wild, landrace and improved maize lines. We find evidence of recovery of diversity after domestication, likely introgression from wild relatives, and evidence for stronger selection during domestication than improvement. We identify a number of genes with stronger signals of selection than those previously shown to underlie major morphological changes. Finally, through transcriptome-wide analysis of gene expression, we find evidence both consistent with removal of cis-acting variation during maize domestication and improvement and suggestive of modern breeding having increased dominance in expression while targeting highly expressed genes.

Figure 1. Neighbor-joining tree and changing morphology of domesticated maize and its wild relatives

Taxa in the neighbor-joining tree (right) are represented by different colors: parviglumis (green), landraces (red), improved lines (blue), mexicana (yellow), and Tripsacum (brown). Morphological changes (left) are shown for female inflorescences and plant architecture during domestication and improvement.

Figure 2. Genome-wide analysis of nucleotide diversity and selection

(a) LOWESS curves of nucleotide diversity (π) along chromosome 1 in parviglumis (green), landraces (red), and improved lines (blue). Genome-wide likelihood values (XP-CLR) for selection during domestication (b) and improvement (c) with chromosome number indicated along the x-axis. Distributions of feature size (d) and gene counts within features (e) in domestication and improvement scans.

Figure 3. Domestication (a–c) and improvement (d–f) candidate genes in relation to two pathways in rice

Zea mays genes are on a grey background (candidates) or boxed (in selected regions) above their rice orthologs. (a) The flowering-time pathway, including GRMZM2G448355 and zagl1. (b) Seedling expression pattern of GRMZM2G448355 in parviglumis and maize inbreds. (c) XP-CLR and relative diversity near GRMZM2G448355; gene orientation is indicated with arrows. (d) The gibberellin biosynthesis pathway. (e) and (f) XP-CLR near the improvement candidates GRMZM2G152354 and dwarf1. The high-yielding rice variety IR8 has a mutation in GA20ox.