Construction and annotation for a near-complete genome assembly of the cultivated octoploid strawberry, Fragaria×ananassa, revealed its four diploid progenitors and subgenome dominance phenomenon which occurred during the construction of such allopolyploid.
Fragrant and tasty – the cultivated garden strawberry, Fragaria×ananassa, is an octoploid cultivar (2n = 8× = 56) developed from a human-facilitated cross between Fragaria virginiana (from North America) and Fragaria chiloensis (from South America). Though the strain has been extremely popular on commercial markets, little was known for its fundamental genome. Its evolutionary history was largely blurred by our limited genetic data, which contained only fragmented and incomplete assemblies. In fact, it is understandable why previous researchers felt reluctant doing the work: Fragaria×ananassa’s complex allopolyploid genome and its high heterozygosity not only render it difficult to distinguish between homoeologous and paralogous copies, but also bring huge workloads (Folta and Barbey 2019). Nevertheless, as sequencing technologies develop over time, in 2019, Edger et al. published a reference genome for Fragaria×ananassa on Nature Genomics, along with some evolutionary inference of their own data.
Edger et al. sequenced Fragaria×ananassa’s genome with a combination of short- and long-read approaches, totaling a 615× coverage that ensures the high resolution of their genetic data. They utilized computational analysis techniques, which had been employed in previous allopolyploid genome studies, to combine various sequences, and corrected misassembles through related genetic map. Core genes as well as repetitively components were carefully annotated (Edger et al. 2019).
Since Fragaria×ananassa is an allopolyploid, it has been long hypothesized that Fragaria×ananassa’s octoploid genome is formed from the hybridization of four ancestral Fragaria diploid subgenomes, but previously no solid evidence was available to indicate the exact progenitor strains (Njuguna et al. 2013). With the updated genome data, Edger et al. sought to compare Fragaria×ananassa’s genetic composition with several diploid candidates’ genome. Experimenters sequenced and de novo assembled 31 transcriptomes of every Fragaria diploid. Phylogenomic analysis was then conducted with genome-wide data to reflect the evolutionary and chronological relationship between diploid candidates and Fragaria×ananassa. Results indicate that F. vesca, F. iinumae, F. viridis, and F. nipponica are the four strains contributing subgenomes to the rise of such allopolyploid genome. The conclusion is solidified when geographical distribution of the ancestral Fragaria is taken into consideration: interbreeding between F. iinumae and F. nipponica probably formed tetraploids in East Asia, which encountered Fragaria viridis on the Eurasia continent; when hexaploidy offspring entered the American continent, they bred with the branch of F. vesca subsp. Bracheata to form the original octoploid progenitors (Edger et al. 2019).
Interestingly, in the Fragaria×ananassa genome, transposable element (TE) occupies around 36% of the entire genome assembly. This phenomenon coordinates to the subgenome dominance hypothesis (Alger and Edger 2020), which suggests that one of the four parental Fragaria subgenomes has higher levels of gene expression, ultimately leading to greater gene retention in polyploidy evolution. TEs are known to suppress gene expression, and the abundance of TEs in Fragaria×ananassa suggests some extents of selective reduction in subgenome expression. Mapping diploid subgenomes and investigating TE existence in proximity, Edger et al. eventually discovered that F. vesca is the dominant subgenome, while the other three count for relatively less gene expression in Fragaria×ananassa.
In conclusion, such unprecedented, high-quality data about the octoploid strawberry genome contributes to the discovery of Fragaria×ananassa’s evolutionary history, including its four diploid progenitors, the geographical spread of Fragaria relatives, as well as the subgenome dominance effects taken place during the polyploid formation. Most obviously, the published reference genome facilitates further studies of the entire Fragaria species, and have general agricultural and commercial implications as well. For instance, as Edger et al. mentions in their publication, in order to prevent strawberries from invasive diseases, breeders may want to look into the expression of plant resistance (R) genes. Though R genes are established to have a high expression in the dominant diploid ancestor F. vesca, they haven’t been functionally identified in Fragaria×ananass in any previous study (Edger et al. 2019). The annotated genome provides foundation for targeting R gene expression in various strawberry strains, and are helpful in the development of gene markers and studies of R gene preservation in multiple polyploid cultivars. On the other hand, with the phylogenetic relationship established in the study, researchers are also able to reveal further details in strawberry evolution. Methodologies in the study also become a model for future research on polyploidy genome construction.
References：
Alger E. I., and P. P. Edger, 2020 One subgenome to rule them all: underlying mechanisms of subgenome dominance. Current Opinion in Plant Biology 54: 108–113. https://doi.org/10.1016/j.pbi.2020.03.004
Edger P. P., T. J. Poorten, R. VanBuren, M. A. Hardigan, M. Colle, et al., 2019 Origin and evolution of the octoploid strawberry genome. Nature Genetics 51: 541–547. https://doi.org/10.1038/s41588-019-0356-4
Folta K. M., and C. R. Barbey, 2019 The strawberry genome: a complicated past and promising future. Horticulture Research 6: 1–3. https://doi.org/10.1038/s41438-019-0181-z
Mollerus S., 2007 Strawberries. https://www.flickr.com/photos/clairity/1328402515/. Accessed February 19th, 2021. (Cover Photo)
Njuguna W., A. Liston, R. Cronn, T.-L. Ashman, and N. Bassil, 2013 Insights into phylogeny, sex function and age of Fragaria based on whole chloroplast genome sequencing. Mol Phylogenet Evol 66: 17–29. https://doi.org/10.1016/j.ympev.2012.08.026
