Evolutionary Origins and Dynamics of Octoploid Strawberry Subgenomes Revealed by Dense Targeted Capture Linkage Maps

Abstract

Whole-genome duplications are radical evolutionary events that have driven speciation and adaptation in many taxa. Higher-order polyploids have complex histories often including interspecific hybridization and dynamic genomic changes. This chromosomal reshuffling is poorly understood for most polyploid species, despite their evolutionary and agricultural importance, due to the challenge of distinguishing homologous sequences from each other. Here, we use dense linkage maps generated with targeted sequence capture to improve the diploid strawberry (Fragaria vesca) reference genome and to disentangle the subgenomes of the wild octoploid progenitors of cultivated strawberry, Fragaria virginiana and Fragaria chiloensis. Our novel approach, POLiMAPS (Phylogenetics Of Linkage-Map-Anchored Polyploid Subgenomes), leverages sequence reads to associate informative interhomeolog phylogenetic markers with linkage groups and reference genome positions. In contrast to a widely accepted model, we find that one of the four subgenomes originates with the diploid cytoplasm donor F. vesca, one with the diploid Fragaria iinumae, and two with an unknown ancestor close to F. iinumae. Extensive unidirectional introgression has converted F. iinumae-like subgenomes to be more F. vesca-like, but never the reverse, due either to homoploid hybridization in the F. iinumae-like diploid ancestors or else strong selection spreading F. vesca-like sequence among subgenomes through homeologous exchange. In addition, divergence between homeologous chromosomes has been substantially augmented by interchromosomal rearrangements. Our phylogenetic approach reveals novel aspects of the complicated web of genetic exchanges that occur during polyploid evolution and suggests a path forward for unraveling other agriculturally and ecologically important polyploid genomes.

HaploSNP affinities and linkage map positions illuminate subgenome composition in the octoploid, cultivated strawberry ( Fragaria×ananassa )

“…Thus, the seven YN-rich homologues are clearly distinguishable as a coherent subgenomic set with affinity to F. vesca, warranting their A-subgenome designation as being consistent with most prior authors [21,26]. Thus, the A subgenome consists of homoeologues LG1A through LG7A, and given the disomic inheritance patterns of A subgenome markers must exist in two copies in the octoploid genome.…”

“…A subsequent re-evaluation of the scaffolds and anchoring of that assembly using a SNP-based linkage map of F. vesca subsp. bracteata developed through sequencing of genomic DNA fragments captured on RNA baits [26] has produced a far more accurate representation of the F. vesca genome (denoted Fvb). Thus, the markers mapped in this investigation were used as queries to BLAST the Fvb pseudomolecules.…”

“…In such populations, traits of interest may be linked to alleles not represented on the genotyping array, reducing the resolving power of markers on the array. In these instances, other genotyping systems, such as target capture using RNA baits as was used for linkage map development in F. ×ananassa and its wild progenitor species by [26], or the genotyping by sequencing protocol of Elshire et al [30] used for linkage map development in other Rosaceous species such as Rubus [31] may be considered as complementary tools for marker and linkage map development. Importantly, the results of array-based studies such as the present one will provide valuable guidance in the design of the next generation strawberry SNP arrays and/or other high throughput genotyping platforms.…”

“…[23][24][25]. More recently, Tennessen et al [26] employed a combination of targeted DNA capture and next generation sequencing to obtain evidence for a new genome model AvAvBiBiB1B1B2B2 (2Av,2Bi,2B1,2B2), positing a single subgenome (Av) deriving from an F. vesca-like ancestor, a single subgenome (Bi) derived from an F. iinumae-like diploid ancestor, and two subgenomes (B1 and B2) derived from a F. iinumae-like autotetraploid.…”

“…They also postulated that a unidirectional flow of genomic information had occurred within the octolopoid genome from the F. vesca-like subgenome to the other three subgenomes [26]. Other recent authors have differentiated the four homoeologues of each chromosome as A, B, C, and D for purposes of convenience [10,17], without advancing explicit hypothesis about subgenomic composition.…”