Domestication Shapes Recombination Patterns in Tomato

Abstract

Meiotic recombination is a biological process of key importance in breeding, to generate genetic diversity and develop novel or agronomically relevant haplotypes. In crop tomato, recombination is curtailed as manifested by linkage disequilibrium decay over a longer distance and reduced diversity compared with wild relatives. Here, we compared domesticated and wild populations of tomato and found an overall conserved recombination landscape, with local changes in effective recombination rate in specific genomic regions. We also studied the dynamics of recombination hotspots resulting from domestication and found that loss of such hotspots is associated with selective sweeps, most notably in the pericentromeric heterochromatin. We detected footprints of genetic changes and structural variants, among them associated with transposable elements, linked with hotspot divergence during domestication, likely causing fine-scale alterations to recombination patterns and resulting in linkage drag.

Keywords: domestication; heterochromatin; recombination; selective sweeps; structural variants; transposable elements.

Fig. 1.

Recombination landscape and transformation from wild to domesticated tomato. (A) Recombination landscape in chromosome 1 of wild (SP), early-domesticated (SLC), and vintage (SLL) tomato. This ρ/kb landscape is intended to show overall landscape only; r_e is used to compare populations in other analyses. Gray vertical lines mark heterochromatin boundaries. (B) Effective recombination rate (r_e) in 1-Mb windows of both wild and domesticated tomato. (C) Change in effective recombination rate in 50-kb regions during domestication (SLC r_e–SP r_e) and improvement (SLL r_e–SLC r_e). (D) Resulting change in r_e for chromosome 1 after the domestication process or between the wild and vintage population. Gray vertical lines mark the heterochromatin boundaries and the colors correspond to the colors in (C).

Fig. 2.

Historical recombination hotspots. (A) Number of hotspots in each chromosome of the wild and domesticated populations. (B) Small but significant numbers of hotspots are shared between populations. (C) Effective recombination rates of hotspots in euchromatic and heterochromatic regions. (D) Recombination hotspots in chromosome 2. Gray lines mark the heterochromatin boundaries.

Fig. 3.

Recombination hotspots in genes. (A) Enrichment of euchromatin hotspots in UTRs and promoter regions (1-kb upstream of genes) in all three populations. (B) Recombination rates of domestication (DSG) and nondomestication (nDSG) sweep genes overlapping and not overlapping S. pimpinellifolium hotspots. h and nh mean hotspots and nonhotspots, respectively. (C–D) Recombination rate upstream (<1 kb) of genes with excised promoters due to (C) domestication and (D) improvement.

Fig. 4.

Recombination and genomic variants. Using permutation tests, we identified (A) specific TE families with an excess or depletion of recombination hotspots. TE families are grouped into repeat elements (gray), retrotransposons (brown), and DNA transposons (yellow). (B) Scatter plots of effective recombination rate and deletion size (n = 1,255) per population. (C–D) Significance of overlap between (C) hotspots and deletions in SP and (D) empirical COs and deletions segregating between SP and SLL. The black and red vertical lines indicate the average number of overlaps found in 10,000 permutation sets and the number of overlaps at P = 0.05, respectively. The green vertical line indicates the observed number of overlaps. (E) Recombination rates (violin) and allele frequencies (red boxplot) of Gypsy, Copia, and L1 elements.