A reference genome for common bean and genome-wide analysis of dual domestications

Abstract

Common bean (Phaseolus vulgaris L.) is the most important grain legume for human consumption and has a role in sustainable agriculture owing to its ability to fix atmospheric nitrogen. We assembled 473 Mb of the 587-Mb genome and genetically anchored 98% of this sequence in 11 chromosome-scale pseudomolecules. We compared the genome for the common bean against the soybean genome to find changes in soybean resulting from polyploidy. Using resequencing of 60 wild individuals and 100 landraces from the genetically differentiated Mesoamerican and Andean gene pools, we confirmed 2 independent domestications from genetic pools that diverged before human colonization. Less than 10% of the 74 Mb of sequence putatively involved in domestication was shared by the two domestication events. We identified a set of genes linked with increased leaf and seed size and combined these results with quantitative trait locus data from Mesoamerican cultivars. Genes affected by domestication may be useful for genomics-enabled crop improvement.

Figure 1. Structure of the P. vulgaris genome and synteny with the G. max genome.

(a) Gray lines connect duplicated genes. (b) Chromosome structure with centromeric and pericentromeric regions in black and gray, respectively (scale is in Mb). (c) Gene density in sliding windows of 1 Mb at 200-kb intervals. (d) Repeat density in sliding windows of 1 Mb at 200-kb intervals. (e) Recombination rate based on the genetic and physical mapping of 6,945 SNPs and SSRs. (f,g) First syntenic region (f) and second G. max syntenic region (g) due to a lineage-specific duplication resulting in two chromosome segments for every segment in P. vulgaris.

Figure 2

Geographic distribution of sampled genotypes.

Figure 3. Evolution and domestication of common bean.

(a) Divergence of the wild Mesoamerican and Andean common bean pools. The wild Andean gene pool diverged from the wild Mesoamerican gene pool ∼165,000 years ago, with a small founding population and a strong bottleneck that lasted ∼76,000 years. The bottleneck was followed by an exponential growth phase extending to the present day. Asymmetric gene flow between the two pools had a key role in maintaining genetic diversity, especially in the Andean population, with average migration rates M₂₁ = 0.135 (wild Mesoamerican to wild Andean) and M₁₂ = 0.087 (wild Andean to wild Mesoamerican). This scenario conforms to the Mesoamerican origin model of the common bean, with an Andean bottleneck that predated domestication. (n_anc, size of ancestral population; t_div, start of bottleneck; n_b, size of bottleneck population; t_b, length of bottleneck) (b) Population genomic analysis based on SNP data from the resequencing of DNA pools for common bean. The size of the circle for each pool is proportional to the π value for the pool. For a reference, π = 0.0061 for the wild Mesoamerican (MA) pool. F_ST statistics, representing the differentiation of any two pools, are noted on the lines (not proportional) connecting pools. Data are average statistics across all 10-kb/2-kb sliding/discarding windows with <50% called bases. Land, landrace; N, north; S, south; C, central. (c) Variation in seed size in common bean. The seeds of wild Mesoamerican and Andean beans (two each) are smaller than the seeds corresponding to the reference genotype (G19833) and the multiple market classes of common beans grown in the United States (navy to light red kidney).

Figure 4. Differentiation and reduction in diversity during the domestication of common bean.

(a,b) Genome-wide view in 10-kb/2-kb sliding windows of differentiation (F_ST) and reduction in diversity (π ratio) statistics associated with domestication within the common bean Mesoamerican (a) and Andean (b) gene pools. Log₁₀ π ratios less than zero are not shown. Lines represent the 90%, 95% and 99% tails for the empirical distribution of each statistic.

Figure 5. Genome-wide association analysis of seed weight.

(a) A 280-member panel of Mesoamerican cultivars was grown in 4 locations in the United States. Phenotypic data were coupled with 34,799 SNP markers and analyzed using a mixed-model analysis that controlled for population structure and genotype relatedness. (b) A close-up view of the GWAS results for seed weight and linkage disequilibrium (r²) around a 1.23-Mb Mesoamerican sweep window on Pv07. The positions of candidate genes for domestication are noted by asterisks above the GWAS display. The candidates range from Phvul.007G094299 to Phvul.007G.99700 (Supplementary Note).