Historical genomics of North American maize

Abstract

Since the advent of modern plant breeding in the 1930s, North American maize has undergone a dramatic adaptation to high-input agriculture. Despite the importance of genetic contributions to historical yield increases, little is known about the underlying genomic changes. Here we use high-density SNP genotyping to characterize a set of North American maize lines spanning the history of modern breeding. We provide a unique analysis of genome-wide developments in genetic diversity, ancestry, and selection. The genomic history of maize is marked by a steady increase in genetic differentiation and linkage disequilibrium, whereas allele frequencies in the total population have remained relatively constant. These changes are associated with increasing genetic separation of breeding pools and decreased diversity in the ancestry of individual lines. We confirm that modern heterotic groups are the product of ongoing divergence from a relatively homogeneous landrace population, but show that differential landrace ancestry remains evident. Using a recent association approach, we characterize signals of directional selection throughout the genome, identifying a number of candidate genes of potential agronomic relevance. However, overall we find that selection has had limited impact on genome-wide patterns of diversity and ancestry, with little evidence for individual lines contributing disproportionately to the accumulation of favorable alleles in today's elite germplasm. Our data suggest breeding progress has mainly involved selection and recombination of relatively common alleles, contributed by a representative but limited set of ancestral lines.

Fig. 1.

(A) Genetic structure described by the first three genetic PCs obtained from PCA on the whole sample. Era 0 landraces are shown in yellow; remaining colors indicate heterotic groups (red, SS; green, IDT; blue, NSS) with darker tones representing later eras (e.g., light red, era 1; red, era 2; dark red, era 3). Colored labels indicate the position of the three historically important era 2 lines within each heterotic group. (B) First three genetic PCs obtained from PCA on Corn Belt Dent landraces; different genetic groups are shown in different colors (green, Yellow Dents; red, Lancaster; blue, Midland; yellow, Minnesota 13; purple, Southern Dents).

Fig. 2.

Historical developments in genetic differentiation and ancestry. (A) Mean differentiation among genetic groups in eras 0–3. (B) Changes in ancestral composition from era 1–3 (colors as in Fig. 1A, with era 0 in yellow and tones from light to dark for eras 1–3). (C) Average number of differences between ancestral haplotypes within individual inbred lines. (D) Weighted average of the effective number of direct ancestors contributing to individual inbred lines. (E) Differential assignment of era 3 heterotic groups to different era 0 landraces.

Fig. 3.

Evidence for directional selection (Top), basal ancestry distortion (Middle), and ancestral haplotype diversity (Bottom) across the genome. Colors indicate the separate chromosomes with red vertical lines marking the centromeres. Green dashed horizontal line marks the 99th percentile of Bayes factors; purple dashed horizontal lines indicate median values of ancestry distortion and effective number of basal ancestors. Black vertical ticks mark selected features. Gray dots mark candidate SNPs. Black circles mark candidates that coincide with sites of low ancestral diversity.

Fig. 4.

Analysis of disproportionate ancestral contributions of individual era 1 lines to favorable alleles in era 3. Left: Overrepresentation of individual era 1 lines in the ancestry of favorable alleles, estimated by plotting the average ancestry proportion at favorable alleles against the genome-wide proportion. Right: Enrichment (as defined by the log probability ratio (LPR) with respect to noncandidate SNP) of favorable alleles in era 1 lines as a function of their average ancestral contribution to era 3. Black dotted lines represent the 1:1 diagonal and 0 horizontal, respectively. Gray dotted lines are regression lines (slope/r²: 1.15/0.85 and −0.1/0.00). Line names on the Right are shown for lines with LPR values higher than 4 or ancestry proportion above 0.03. Labels in boldface mark breeding lines of known historic popularity.