Abstract
Allo-octoploid cultivated strawberry (Fragaria × ananassa) originated through a combination of polyploid and homoploid hybridization, domestication of an interspecific hybrid lineage, and continued admixture of wild species over the last 300 years. While genes appear to flow freely between the octoploid progenitors, the genome structures and diversity of the octoploid species remain poorly understood. The complexity and absence of an octoploid genome frustrated early efforts to study chromosome evolution, resolve subgenomic structure, and develop a single coherent linkage group nomenclature. Here, we show that octoploid Fragaria species harbor millions of subgenome-specific DNA variants. Their diversity was sufficient to distinguish duplicated (homoeologous and paralogous) DNA sequences and develop 50K and 850K SNP genotyping arrays populated with co-dominant, disomic SNP markers distributed throughout the octoploid genome. Whole-genome shotgun genotyping of an interspecific segregating population yielded 1.9M genetically mapped subgenome variants in 5,521 haploblocks spanning 3,394 cM in F. chiloensis subsp. lucida, and 1.6M genetically mapped subgenome variants in 3,179 haploblocks spanning 2,017 cM in F. × ananassa. These studies provide a dense genomic framework of subgenome-specific DNA markers for seamlessly cross-referencing genetic and physical mapping information and unifying existing chromosome nomenclatures. Using comparative genomics, we show that geographically diverse wild octoploids are effectively diploidized, nearly completely collinear, and retain strong macro-synteny with diploid progenitor species. The preservation of genome structure among allo-octoploid taxa is a critical factor in the unique history of garden strawberry, where unimpeded gene flow supported its origin and domestication through repeated cycles of interspecific hybridization.
Highlights
Despite a small effective population size, our analyses show that massive genetic diversity has been preserved in F. × ananassa, with negligible difference between wild species and domesticated germplasm
Correlations of F. × ananassa, F. chiloensis, and F. virginiana diversity across the 28 octoploid chromosomes ranged from 0.93–0.97, showing that the magnitude and distribution of genomic diversity are broadly conserved among octoploid taxa
This suggested that F. × ananassa was not strongly bottlenecked by domestication, or that its domestication bottleneck was mitigated by continued introgression of allelic diversity from wild subspecies (Darrow, 1966)
Summary
Interspecific homoploid hybridization and polyploidy-inducing hybrid events have been creative forces in plant genome evolution and speciation, acting as catalysts for de novo reorganization of chromosome structure (Jiao et al, 2011; Yakimowski and Rieseberg, 2014; Soltis et al, 2014b; Soltis et al, 2014a; Vallejo-Marín et al, 2015; McKain et al, 2016; Soltis et al, 2016; Wendel et al, 2016; Alix et al, 2017; Mandáková et al, 2019). The chromosomes of octoploid garden strawberry (2n = 8x = 56) evolved through a combination of ancient polyploidy, and repeated homoploid hybridization in the last three centuries (Duchesne, 1766; Darrow, 1966). Meiotic mispairing in interspecific homoploid hybrids can lead to rearranged offspring chromosomes that differ from the chromosomes of one or both parents, resulting in reproductive barriers and hybrid speciation, as has been widely documented in sunflower (Helianthus) and other plants (Rieseberg, 1997; Burke et al, 2004; Abbott et al, 2010; Barb et al, 2014; Yakimowski and Rieseberg, 2014). Reproductive barriers among octoploid Fragaria taxa remain essentially nonexistent, fueling the recurrence of interspecific homoploid hybridization in the origin, domestication, and modern-day breeding of F. Reproductive barriers among octoploid Fragaria taxa remain essentially nonexistent, fueling the recurrence of interspecific homoploid hybridization in the origin, domestication, and modern-day breeding of F. × ananassa
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