Whole genome comparisons of Fragaria, Prunus and Malus reveal different modes of evolution between Rosaceous subfamilies

Abstract

Background: Rosaceae include numerous economically important and morphologically diverse species. Comparative mapping between the member species in Rosaceae have indicated some level of synteny. Recently the whole genome of three crop species, peach, apple and strawberry, which belong to different genera of the Rosaceae family, have been sequenced, allowing in-depth comparison of these genomes.

Results: Our analysis using the whole genome sequences of peach, apple and strawberry identified 1399 orthologous regions between the three genomes, with a mean length of around 100 kb. Each peach chromosome showed major orthology mostly to one strawberry chromosome, but to more than two apple chromosomes, suggesting that the apple genome went through more chromosomal fissions in addition to the whole genome duplication after the divergence of the three genera. However, the distribution of contiguous ancestral regions, identified using the multiple genome rearrangements and ancestors (MGRA) algorithm, suggested that the Fragaria genome went through a greater number of small scale rearrangements compared to the other genomes since they diverged from a common ancestor. Using the contiguous ancestral regions, we reconstructed a hypothetical ancestral genome for the Rosaceae 7 composed of nine chromosomes and propose the evolutionary steps from the ancestral genome to the extant Fragaria, Prunus and Malus genomes.

Conclusion: Our analysis shows that different modes of evolution may have played major roles in different subfamilies of Rosaceae. The hypothetical ancestral genome of Rosaceae and the evolutionary steps that lead to three different lineages of Rosaceae will facilitate our understanding of plant genome evolution as well as have a practical impact on knowledge transfer among member species of Rosaceae.

Figure 1

Orthology map identified between three Rosaceous genera based on whole genome sequence analysis. The lines link one to one orthologous regions, identified using Mercator program [25]. A. Comparison between Prunus and Fragaria, B. Comparison between Prunus and Malus. Data were plotted using Circos [42]. Colors for plots A and B follow the same pattern based on Prunus chromosomes.

Figure 2

Comparison of orthologous regions (OR) from two-species analyses and those from the three-species analysis. A. ORs between PC2 and chromosomes of Fragaria and Malus, detected from two separate analyses. B. The same ORs shown in A as well as ORs that are shared by all three species. Blue lines link the ORs shared by all three species, red lines link ORs between Prunus and Fragaria only, and green lines link ORs between Prunus and Malus only. Data were plotted using Circos [42].

Figure 3

The chromosomes of Prunus, Fragaria, and Malus, with the colors represent the origin from the 49 contiguous ancestral regions (CARs). The spaces with a black line represent chromosomal regions where the ancestral origin was not assigned. CARs that existed before the split of Prunus, Fragaria and Malus, were detected by MGRA (Multiple Genome Rearrangments and Ancestors) algorithm [32]. The figure was drawn using R program (Hornik 2011).

Figure 4

Hypothetical evolutionary steps from the nine Rosaceae ancestral chromosomes to Fragaria, Prunus and Malus lineage. Each color represent distinct CARs detected by MGRA algorithm. Chromosomal rearrangements specific for Rosoideae (contains Fragaria) and Spireaoideae (contains Malus and Prunus) are depicted. Also shown are chromosomal rearragenments specific for Prunus, Malus, and subgenome of Malus after the WGD.

Figure 5

The Concentric circle of Rosaceae genomes. The innermost circle represents the putative nine chromosomes of Rosaceae ancestral genome. Next sets of circles represent eight, 17 and seven chromosomes of Prunus, Malus and Fragaria, respectively. The regions originated from each Rosaceae ancestral chromosome are highlighted with corresponding color in Figure S3. The Data were plotted using Circos [42].