Lens species genome assemblies reveal evolutionarily fragile chromosomes associated with pericentric inversions

Abstract

The genus Lens is comprised of seven diploid species, including the cultivated crop Lentil, and six wild relatives often used in breeding programs for beneficial allele introgression. Lens species are proposed to exhibit considerable levels of genome structural variation both within and between species, which has implications for plant breeding and evolutionary genomics. Plant centromeres are key regions involved in chromosomal stability, where structural changes can be linked to meiotic abnormalities, resulting in inversions, translocations, and deletions of chromosomal segments. Fabeae centromeres are known to be diverse and do not fit the centromere drive model. The origins of this centromere diversity and the evolutionary trends remain unclear, but recent studies suggest that centromere structural variation plays a role in creating new sequence combinations that contribute to the unique centromere evolution patterns observed in legumes. We sequenced, assembled, and performed gene synteny analysis in the genomes of all seven Lens species using long-read sequencing technologies. We also located and characterized the centromeres in these genomes through ChIP-seq experiments to better understand their role in Lens chromosomal stability. Synteny analysis reveals that Lens genomes have undergone extensive rearrangements during evolution, with multiple translocations and inversions identified between species. Specific Lens chromosomes appear more susceptible to rearrangements over time. These same chromosomes also exhibit higher rates of rearrangement throughout Lens speciation. Fragile chromosomes are associated with the occurrence of pericentric inversions, likely disrupting stability. The diversity in satellite sequences in Lens centromeres likely results from structural changes accumulated throughout Lens evolution. These findings suggest that genome and centromere structure play significant roles in generating centromere diversity within this legume genus.