Repeatome turnover meets stable chromosomes: Repetitive DNA sequences mark speciation and gene pool boundaries in sugar beet and wild beets

Sugar beet (Beta vulgaris subsp. vulgaris) and its wild beet relatives share a base chromosome number of nine and similar chromosome morphologies. Yet, interspecific breeding is impeded by chromosome and sequence divergence that is still not fully understood. Since repetitive DNA sequences represent the fastest evolving parts of the genome, they likely impact genomic variability and contribute to the separation of beet gene pools. Hence, we investigated if innovations and losses in the repeatome can be linked to chromosomal differentiation and speciation. We traced genome- and chromosome-wide evolution across sugar beet and twelve wild beets comprising all sections of the beet genera Beta and Patellifolia. For this, we combined data from short and long read sequencing, flow cytometry, bioinformatics and cytogenetics to build a comprehensive data framework for our beet panel that spans the complete scale from DNA sequence to chromosome up to the genome. Both, genome sizes (694 Mbp in the diploid B. vulgaris subsp. maritima to 2,471 Mbp in the pentaploid B. intermedia) and repeat profiles (53 to 68% repeats), reflect the separation of the beet species into gene pools: We identified section- and species-specific repeat emergences and losses, e.g. of the retrotransposons causal for genome expansions in the section Corollinae/Nanae. Since most genomic variability was found in the satellite DNAs, we focused on tracing the 19 beetSat families across the three beet sections/genera. These taxa harbor evidence for contrasting strategies in repeat evolution, leading to contrasting satellite DNA profiles and fundamentally different centromere architectures, ranging from chromosomal uniformity in Beta and Patellifolia species to the formation of patchwork chromosomes in Corollinae/Nanae species. We show that repetitive DNA sequences are causal for genome size expansion and contraction across the beet genera, providing insights into the genomic underpinnings of beet speciation. Satellite DNAs in particular vary considerably among beet taxa, leading to the evolution of distinct chromosomal setups in the three gene pools. These differences likely contribute to the barriers in beet breeding between the gene pools. Thus, with their isokaryotypic chromosome sets, beet genomes present an ideal system for studying the link between repeats, genome variability, and chromosomal differentiation and provide a theoretical basis for understanding barriers in crop breeding.