Origin and evolution of the octoploid strawberry genome

Abstract

Cultivated strawberry emerged from the hybridization of two wild octoploid species, both descendants from the merger of four diploid progenitor species into a single nucleus more than 1 million years ago. Here we report a near-complete chromosome-scale assembly for cultivated octoploid strawberry (Fragaria × ananassa) and uncovered the origin and evolutionary processes that shaped this complex allopolyploid. We identified the extant relatives of each diploid progenitor species and provide support for the North American origin of octoploid strawberry. We examined the dynamics among the four subgenomes in octoploid strawberry and uncovered the presence of a single dominant subgenome with significantly greater gene content, gene expression abundance, and biased exchanges between homoeologous chromosomes, as compared with the other subgenomes. Pathway analysis showed that certain metabolomic and disease-resistance traits are largely controlled by the dominant subgenome. These findings and the reference genome should serve as a powerful platform for future evolutionary studies and enable molecular breeding in strawberry.

Fig. 1. Collinearity of the diploid and octoploid strawberry genomes.

a, Macrosyntenic comparison of the entire Fragaria × ananassa and diploid F. vesca genomes, with each homoeologous chromosome set colored according to its diploid progenitor species (F. vesca in red, F. nipponica in purple, F. iinumae in blue, and F. viridis in green). Details are provided in Supplementary Table 8. F. vesca and F. ananassa chromosomes are shown on the y axis and x axis, respectively. b, Gene-retention patterns among the four homoeologous copies of chromosome 1, with color coding as in a. The relative distance along the F. vesca chromosome is shown on the x axis with the total number of analyzed genes. The percentage of genes retained is shown on the y axis, as estimated with sliding windows of 100 genes. The chromosomes of F. vesca are named Fvb1 through Fvb7. c, A microsyntenic comparison of a region on chromosome 1 between diploid F. vesca and the four homoeologous regions in Fragaria × ananassa. Gray lines indicate shared syntenic gene pairs, and relative orientation is shown in blue (forward) or orange (reverse). The four subgenomes of Fragaria × ananassa are labeled with corresponding diploid species names of potential origins.

Fig. 2. The evolutionary history of the octoploid strawberry.

North-polar projection of present day. Geographic distributions of extant relatives of the diploid (2×) progenitors of Fragaria × ananassa, the putative intermediate tetraploid (4×) and hexaploid (6×) progenitors of Fragaria × ananassa, and extant wild octoploid (8×) species in North America. The colors associated with each diploid progenitor are as in Fig. 1. Map data were obtained from Google Maps (see URLs).

Fig. 3. Subgenome expression dominance.

Homoeolog expression bias (HEB) for all testable homoeolog pairs, shown in gray histograms. Testable homoeolog pairs (n) are those that could confidently be identified as homoeologous on the basis of synteny and assigned to a subgenome with phylogenetic support (>80% bootstrap), and that had at least one read in each transcriptome dataset. Homoeolog pairs significantly biased toward the F. vesca homoeolog are shown in red, and pairs significantly biased toward the ‘other’ homoeolog from one of the other three diploid progenitors are shown in black.