A new subgenome of the Camelina genus reveals genome dominance is controlled by chromosomal proximity

Abstract

Camelina sativa is an oilseed of the Brassicaceae, whose close relatives vary in ploidy number, providing a novel platform for studying plant genome evolution. The availability of diploid, tetraploid and hexaploid species of Camelina allow the evolutionary trajectory and fate of duplicated genes in the neopolyploid Camelina species to be elucidated. Here we report an improved assembly of the widely used C. sativa reference DH55 and three new genome assemblies of Camelina microcarpa; one tetraploid CN119243 (2n = 26), and two hexaploids with divergent chromosome numbers, Type 1 - CN119205 (2n=40) and Type 2 - CN120025 (2n=38). The tetraploid represents the first step in the evolutionary path to form C. sativa, while the hexaploids suggest three divergent lineages in the formation of higher ploidy Camelina species. The previously uncharacterized fourth subgenome found in C. microcarpa Type 2, although showing some homology to the C. sativa diploid progenitor genome, C. neglecta, showed numerous unique chromosomal rearrangements differentiating it from other subgenomes present in known Camelina species. Although this species was recently formed, the second subgenome showed gene expression dominance, which was in contrast to both 2n=40 Camelina species where the third subgenome was dominant. The expression dominance in Type 2 C. microcarpa contradicted the accepted two-step evolutionary process which led to the generation of related Brassicaceae species. However, the observed genome dominance in all Camelina species was negatively correlated with inter-subgenome chromatin interaction frequencies, suggesting that chromosome confirmation and proximity in the nucleus contributes to this mechanism of genome evolution. Despite the differences in genome structure, successful inter-specific hybridization provided evidence of chromosomal exchange between the divergent third sub-genomes of C. sativa and C. microcarpa Type 2, opening up a novel avenue to new diversity in the established oilseed. Key pointsO_LIAn improved genomic understanding of Camelina species and identification of distinct subgenome structures and relationships, which will facilitate strategies to increase the genetic diversity in C. sativa. C_LIO_LISubgenome evolution and subgenome dominance in polyploids is associated with chromosomal architecture and proximity in the nucleus. C_LIO_LIGenome assemblies representing all ploidy levels in the Camelina genus provide a unique and valuable platform for polyploid research. C_LI