Chromosome-scale assembly with a phased sex-determining region resolves features of early Z and W chromosome differentiation in a wild octoploid strawberry

Abstract

When sex chromosomes stop recombining, they start to accumulate differences. The sex-limited chromosome (Y or W) especially is expected to degenerate via the loss of nucleotide sequence and the accumulation of repetitive sequences. However, how early signs of degeneration can be detected in a new sex chromosome is still unclear. The sex determining region (SDR) of the octoploid strawberries is young, small, and dynamic. Using PacBio HiFi reads, we obtained a chromosome scale assembly of a female (ZW) Fragaria chiloensis plant carrying the youngest and largest of the known SDR on the W in strawberries. We fully characterized the previously incomplete SDR, confirming its gene content, genomic location and evolutionary history. Resolution of gaps in the previous characterization of the SDR added 10 kbp of sequence including a non-canonical LTR-retrotransposon; whereas the Z sequence revealed a Harbinger transposable element adjoining the SDR insertion site. Limited genetic differentiation of the sex chromosomes coupled with structural variation may indicate an early stage of W degeneration. The sex chromosomes have a similar percentage of repeats but differ in their repeat distribution. Differences in the pattern of repeats (transposable element polymorphism) apparently precede sex chromosome differentiation, thus potentially contributing to recombination cessation as opposed to being a consequence of it.

Telomere-to-Telomere and Haplotype-Phased Genome Assemblies of the Heterozygous Octoploid ‘Florida Brilliance’ Strawberry (Fragaria × ananassa)

“…In particular, 'Florida Brilliance' sub-genome A showed higher sequence similarity with F. vesca than other sub-genomes, which agrees with Hardigan et al (5). Translocations on 3C, 4A, 4B and 4C were apparent when comparing with the genome of F. chiloensis (Figure 3D) (10). The genetic positions from a 'Florida Brilliance' linkage map and physical coordinates of SNPs showed good collinearity (Figure 4).…”

“…Translocations on 3C, 4A, 4B and 4C were apparent when comparing with the genome of F . chiloensis (Figure 3D) (10). The genetic positions from a ‘Florida Brilliance’ linkage map and physical coordinates of SNPs showed good collinearity (Figure 4).…”

“…Several chromosomal rearrangements in the F. chiloensis reference relative to F. vesca and 'Royal Royce' (F. × ananassa) have been reported (10) and are also visible when compared to 'Florida Brilliance' (Figure 3). For example, the alignment against F. chiloensis shows disagreement in continuity in 3 chromosomes (Fchil3-B2, Fchil4-Av, and Fchil4-Bi) (Figure 3D).…”

“…When examined by sub-genome, we observed sub-genome dominance: A > B > C > D based on the proportion of complete vs fragmented or missing genes in the ‘Florida Brilliance’ genome assembly, as with ‘Royal Royce’(5), and F . chiloensis (10). Genome structure ‘AAAAAABB’ along with sub-genome dominance might support the model hypothesizing one subgenome arising from cytoplasm donor F .…”

Does polyploidy inhibit sex chromosome evolution in angiosperms?

“…Gates (1926) and Wright et al (2015) suggested that the multiplied sex chromosomes (Z or X) in polyploids can gradually transform into autosomes, and this appears to have occurred in polyploid Rumex acetosella, which each retained have only one pair of sex chromosomes (XY for males) (Singh, 1968;Cunado et al, 2007). The dioecious octoploid Fragaria (e.g., Fragaria chiloensis) species that arose from hermaphroditic diploid progenitors also each have only one SLR on one of the homologues in each species studied (Tennessen et al, 2016;Cauret et al, 2022), while the others may have become autosomes. The "new" autosomes could still be just like the ancestral X or Z chromosome, or their genes might be lost due to diploidization.…”