Population genomic and genome-wide association studies of agroclimatic traits in sorghum

Abstract

Accelerating crop improvement in sorghum, a staple food for people in semiarid regions across the developing world, is key to ensuring global food security in the context of climate change. To facilitate gene discovery and molecular breeding in sorghum, we have characterized ~265,000 single nucleotide polymorphisms (SNPs) in 971 worldwide accessions that have adapted to diverse agroclimatic conditions. Using this genome-wide SNP map, we have characterized population structure with respect to geographic origin and morphological type and identified patterns of ancient crop diffusion to diverse agroclimatic regions across Africa and Asia. To better understand the genomic patterns of diversification in sorghum, we quantified variation in nucleotide diversity, linkage disequilibrium, and recombination rates across the genome. Analyzing nucleotide diversity in landraces, we find evidence of selective sweeps around starch metabolism genes, whereas in landrace-derived introgression lines, we find introgressions around known height and maturity loci. To identify additional loci underlying variation in major agroclimatic traits, we performed genome-wide association studies (GWAS) on plant height components and inflorescence architecture. GWAS maps several classical loci for plant height, candidate genes for inflorescence architecture. Finally, we trace the independent spread of multiple haplotypes carrying alleles for short stature or long inflorescence branches. This genome-wide map of SNP variation in sorghum provides a basis for crop improvement through marker-assisted breeding and genomic selection.

Fig. 1.

Germplasm origin and genetic relationships among worldwide sorghum accessions. (A) Geographic origin for 469 of 971 worldwide accessions, for which source location is known, color-coded by morphological type. (B) Genetic relatedness among the same 469 accessions assessed by neighboring joining method, with the predominant region of origin for each cluster noted, or in one case, the cluster containing guinea margaritiferum types. Worldwide sorghum populations show structuring by morphological type within regions.

Fig. 2.

Genome-wide patterns of SNP variation. (A) Genome-wide variation of expected heterozygosity for sorghum landraces, smoothed with a 2000 SNP moving average. The location of the centromeres are noted by the gray bars. Dotted vertical lines indicate the Shattering1 (Sh1) domestication locus and two orthologs of starch-related domestication loci from maize (opaque2 and brittle endosperm2) that colocalize with regions of reduced diversity. (B) The relative heterozygosity in sorghum conversion lines compared with landraces. The reduction in heterozygosity in conversion lines is due to introgressions of short stature and early maturity alleles, with known dwarfing (dw) and maturity (ma) loci noted. (C) Genome-wide variation in historical recombination rates averaged across 10 subpopulations. Wider regions of reduced heterozygosity occur in regions near centromeres with low recombination rates.

Fig. 3.

GWAS of preflag leaf height using landraces and introgression lines. (A) Manhattan plot for compressed mixed linear model with known dwarfing loci indicated. (B–D) GWAS peaks for height colocalize with reductions in heterozygosity in the sorghum association panel due to introgression of short stature and early maturity alleles. (E–G) Geographic distribution of alleles at dw2, dw3, and dw1/SbHT9.1, respectively, color-coded by allele (A, green; C, blue; T, red; G, orange).

Fig. 4.

GWAS on inflorescence branch-length and geographic distribution QTL alleles. (A) Compressed mixed linear model using first three principal components of population structure as covariates. Candidate genes at peaks are indicated (Table S2), with association peaks in the given gene denoted by black triangles and outside the given gene by gray triangles. (B–D) Worldwide distribution of alleles at three branch-length QTL illustrate the spread of haplotypes associated with variation in branch length, color-coded by allele (A, green; C, blue; T, red; G, orange).