Decreased Nucleotide and Expression Diversity and Modified Coexpression Patterns Characterize Domestication in the Common Bean

Abstract

Using RNA sequencing technology and de novo transcriptome assembly, we compared representative sets of wild and domesticated accessions of common bean (Phaseolus vulgaris) from Mesoamerica. RNA was extracted at the first true-leaf stage, and de novo assembly was used to develop a reference transcriptome; the final data set consists of ∼190,000 single nucleotide polymorphisms from 27,243 contigs in expressed genomic regions. A drastic reduction in nucleotide diversity (∼60%) is evident for the domesticated form, compared with the wild form, and almost 50% of the contigs that are polymorphic were brought to fixation by domestication. In parallel, the effects of domestication decreased the diversity of gene expression (18%). While the coexpression networks for the wild and domesticated accessions demonstrate similar seminal network properties, they show distinct community structures that are enriched for different molecular functions. After simulating the demographic dynamics during domestication, we found that 9% of the genes were actively selected during domestication. We also show that selection induced a further reduction in the diversity of gene expression (26%) and was associated with 5-fold enrichment of differentially expressed genes. While there is substantial evidence of positive selection associated with domestication, in a few cases, this selection has increased the nucleotide diversity in the domesticated pool at target loci associated with abiotic stress responses, flowering time, and morphology.

Figure 1.

Multidimensional Scaling Analysis Representing the Genetic Relationships among the 21 Common Bean Genotypes.

Figure 2.

Within-Population Genetic Diversity Comparison between MW and MD Populations. Box plots of the number of segregating sites (per base pair), the expected heterozygosity, the number of haplotypes, and the nucleotide diversity in the MW versus the MD population, evaluated over all of the contigs. The statistical significance was computed with the Wilcoxon signed rank test for paired data (P value: above each box plot).

Figure 3.

Estimated Density Functions for the Coefficients of Variation in MD and MW as a Reference. Comparison of the density functions of the CVs considering: all contigs (n = 27,217 CVs of finite value in MW; 27,114 CVs of finite value in MD) (A), subdivision in PN contigs (n = 24,854 CVs of finite value in MW; 24,759 CVs of finite value in MD) (B), and PS contigs (n = 2363 CVs of finite value in MW; 2355 CVs of finite value in MD) (C), where N denotes the number of contigs with CVs of finite values in MW as a reference.

Figure 4.

Distributions of the Pearson Correlation Coefficients Obtained from the Expression Profiles in the MW and MD Populations. Distributions of the MW (A) and MD (B) populations resemble normal distributions, with the PCCs in MD showing greater values than those in MW.

Figure 5.

Proximity Networks of MW and MD and Their Community Structure. Nodes are color-coded according to their participation in one of the seven and five communities in the MW (A) and MD (B) proximity networks, respectively, containing a single connected component. Nodes of bigger size correspond to contigs under selective pressure.