The organization and rate of evolution of wheat genomes are correlated with recombination rates along chromosome arms

Abstract

Genes detected by wheat expressed sequence tags (ESTs) were mapped into chromosome bins delineated by breakpoints of 159 overlapping deletions. These data were used to assess the organizational and evolutionary aspects of wheat genomes. Relative gene density and recombination rate increased with the relative distance of a bin from the centromere. Single-gene loci present once in the wheat genomes were found predominantly in the proximal, low-recombination regions, while multigene loci tended to be more frequent in distal, high-recombination regions. One-quarter of all gene motifs within wheat genomes were represented by two or more duplicated loci (paralogous sets). For 40 such sets, ancestral loci and loci derived from them by duplication were identified. Loci derived by duplication were most frequently located in distal, high-recombination chromosome regions whereas ancestral loci were most frequently located proximal to them. It is suggested that recombination has played a central role in the evolution of wheat genome structure and that gradients of recombination rates along chromosome arms promote more rapid rates of genome evolution in distal, high-recombination regions than in proximal, low-recombination regions.

Figure 1.

Estimates of recombination rates (cM/Mb) within individual bins in relation to the position of bin midpoints on the centromere-telomere axis of wheat chromosome arms. On the horizontal axis, 0.0 represents the centromere and 1.0 represents the telomere. The curve and its equation best fitting the data are shown.

Figure 2.

Relative gene density along chromosome arms. On the horizontal axis, 0.0 represents the centromere and 1.0 represents the telomere. Relative gene density is estimated by the number of restriction fragments per Mb. The curve and its equation best fitting the data are shown.

Figure 3.

Relationship between relative frequencies of single-gene loci (S/T ratio) per bin and the bin relative distance from the centromere. On the horizontal axis, 0.0 represents the centromere and 1.0 represents the telomere. The curve and its equation best fitting the data are shown.

Figure 4.

Frequencies of EST unigenes detecting the indicated numbers of loci within a genome. The curve and the exponential equation best fitting the data are shown.

Figure 5.

Synteny between wheat chromosome 3B and rice chromosome 1 and wheat chromosome 7D and rice chromosomes 6 and 8. The boundaries of the bins delineated by deletion breakpoints on chromosomes 3B and 7D are indicated by horizontal lines across chromosomes. The distances of the breakpoints from the centromere, expressed as the fraction of arm length, are shown to the left of the breakpoints. The numbers to the right of the wheat chromosomes indicate the numbers of loci detected by ESTs per bin that had orthologous genes on rice homoeologous chromosomes. Numbers of wheat/rice orthologous loci that are members of wheat paralogous sets are indicated in parentheses. Wheat bins and rice contigs (indicated by brackets) containing two or more orthologous loci are connected by dotted lines. Rice contigs containing only a single putative ortholog are unconnected. The numbers of wheat/rice orthologs within each rice contig are indicated to the left of rice chromosomes. The black circles indicate centromeres.

Figure 6.

The distribution of loci derived by duplication of ancestral loci on W3, the ancestral loci, and the rest of W3 loci with orthologs on rice chromosome 1 along wheat chromosome arms (A) and the distribution of loci derived by duplication of ancestral loci on W7, ancestral loci, and the rest of W7 loci with orthologs on rice chromosome 6 plus 8 along wheat chromosome arms (B). The horizontal axes, on which 0.0 represents the centromere and 1.0 represents the telomere, show grouping of bin midpoints in which loci reside on the centromere-telomere axis into five equal intervals.

Figure 7.

Differentiation rice chromosome 1 (R1) from between wheat chromosome 3B. The boundaries of bins (breakpoints) are indicated by horizontal lines across the chromosome. Their distances from the centromere, expressed as the fraction of arm length, are shown to the left of the breakpoints. The estimates of differentiation, di, of R1 from individual bins of 3B are to the right of the chromosome.