Reticulate evolution of the rye genome

Abstract

Rye (Secale cereale) is closely related to wheat (Triticum aestivum) and barley (Hordeum vulgare). Due to its large genome (~8 Gb) and its regional importance, genome analysis of rye has lagged behind other cereals. Here, we established a virtual linear gene order model (genome zipper) comprising 22,426 or 72% of the detected set of 31,008 rye genes. This was achieved by high-throughput transcript mapping, chromosome survey sequencing, and integration of conserved synteny information of three sequenced model grass genomes (Brachypodium distachyon, rice [Oryza sativa], and sorghum [Sorghum bicolor]). This enabled a genome-wide high-density comparative analysis of rye/barley/model grass genome synteny. Seventeen conserved syntenic linkage blocks making up the rye and barley genomes were defined in comparison to model grass genomes. Six major translocations shaped the modern rye genome in comparison to a putative Triticeae ancestral genome. Strikingly dissimilar conserved syntenic gene content, gene sequence diversity signatures, and phylogenetic networks were found for individual rye syntenic blocks. This indicates that introgressive hybridizations (diploid or polyploidy hybrid speciation) and/or a series of whole-genome or chromosome duplications played a role in rye speciation and genome evolution.

Figure 1.

Rye Consensus Transcript Map. Comparison of the integrated genetic map of chromosome 1R with the 1R maps of four individual mapping populations (Lo7xLo225, P87xP105, Lo90xLo115, and L2039-NxDH). Colored lines connect markers between the integrated map and each individual genetic linkage map. Complete collinearity could be observed between all individual maps and the integrated consensus. Centromere position in the consensus map is indicated by green triangles.

Figure 2.

Conserved Synteny between Rye, Barley, and B. distachyon. Collinearity of the rye and barley genomes is depicted by the inner circle of the diagram. Rye (1R to 7R) and barley (1H to 7H) chromosomes were scaled according to the rye genetic and barley physical map, respectively. Lines (colored according to barley chromosomes) within the inner circle connect putatively orthologous rye and barley genes. The outer partial circles of heat map colored bars illustrate the density of B. distachyon genes hit by the 454 chromosome survey sequencing reads of the corresponding rye chromosomes. Conserved syntenic blocks are highlighted by yellow-red-colored regions of the heat maps. Putatively orthologous genes between rye and B. distachyon are connected with lines (colored according to rye chromosomes), and centromere positions are highlighted by gray rectangles.

Figure 3.

Rye Genome Reorganization and Translocation Events. Rye genome reorganizations occurring in the common ancestor of rye and wheat (translocation between chromosomes 4 and 5) and divergence of the two lineages are postulated. Three of the five translocations that occurred after the split of wheat can be ordered, while for two the order cannot be deduced. They may have occurred in parallel or consecutively.

Figure 4.

Conserved Synteny Statistics of Rye Chromosome 3R and the Corresponding Barley Regions to Reference Genomes. Venn diagrams show the absolute number of conserved syntenic rye (yellow) and barley (gray) genes in comparison to the reference grass genomes of B. distachyon, rice, and sorghum. The bars below depict the percentage of distribution of reference genes shared by barley and rye (white), or rye (yellow) and barley alone (gray), respectively. While the 3R.1 fragment shows a balanced conserved syntenic pattern, the second fragment 3R.2 showed 10-fold less conserved syntenic genes in comparison to the corresponding barley segment.

Figure 5.

Sequence Conservation between Rye and Barley in 17 Conserved Syntenic Genome Segments. (A) Rye gene-based chromosome survey sequences of the 17 conserved syntenic genome segments were compared with the putative barley orthologs (on the basis of fl-cDNAs) and the distribution of percentage of sequence identity is depicted by heat maps for each conserved block (max = highest no. of reads per segment with the given identity value; each block has its own maximum). The segments showed nonuniform sequence conservation patterns. (B) The obtained sequence identity values were grouped by hierarchical clustering (average linkage, Euclidean distance) with the aim to find similarities between segments that could indicate their origin from the same progenitor genome and translocation or introgression event.