Origin and Evolution of Diploid and Allopolyploid Camelina Genomes was Accompanied by Chromosome Shattering

Abstract

Complexes of diploid and polyploid species have formed frequently during the evolution of land plants. In false flax (Camelina sativa), an important hexaploid oilseed crop closely related to Arabidopsis (Arabidopsis thaliana), the putative parental species as well as the origin of other Camelina species remained unknown. By using bacterial artificial chromosome-based chromosome painting, genomic in situ hybridization, and multi-gene phylogenetics, we aimed to elucidate the origin and evolution of the polyploid complex. Genomes of diploid camelinas (Camelina hispida, n 5 7; Camelina laxa, n 5 6; and Camelina neglecta, n 5 6) originated from an ancestral n 5 7 genome. The allotetraploid genome of Camelina rumelica (n 5 13, N 6 H) arose from hybridization between diploids related to C. neglecta (n 5 6, N 6 ) and C. hispida (n 5 7, H), and the N subgenome has undergone a substantial post-polyploid fractionation. The allohexaploid genomes of C. sativa and Camelina microcarpa (n 5 20, N 6 N 7 H) originated through hybridization between an auto-allotetraploid C. neglecta-like genome (n 5 13, N 6 N 7 ) and C. hispida (n 5 7, H), and the three subgenomes have remained stable overall since the genome merger. Remarkably, the ancestral and diploid Camelina genomes were shaped by complex chromosomal rearrangements, resembling those associated with human disorders and resulting in the origin of genome-specific shattered chromosomes.

Exceptional subgenome stability and functional divergence in the allotetraploid Ethiopian cereal teff

“…This same pattern of rearrangement is observed in the banana (Musa balbisiana) A and B subgenomes, which diverged~5.4 mya and have several megabase pair sized translocations and inversions between them 38 . The allohexaploid false flax (Camelina stativa) has evidence of shattered chromosomes with numerous rearrangements and fractionation of the subgenomes compared to the diploid progenitors 39 .…”

Genome Synteny Has Been Conserved Among the Octoploid Progenitors of Cultivated Strawberry Over Millions of Years of Evolution

“…This is unique compared to extensive karyotype evolution documented in polyploid species involving numerous chromosomal fusion and rearrangement events, e.g. Camelina sativa (Mandáková et al, 2019).…”

“…Interspecific homoploid hybridization and polyploidy-inducing hybrid events have been creative forces in plant genome evolution and speciation, acting as catalysts for de novo reorganization of chromosome structure (Jiao et al, 2011;Yakimowski and Rieseberg, 2014;Soltis et al, 2014b;Soltis et al, 2014a;Vallejo-Marín et al, 2015;McKain et al, 2016;Soltis et al, 2016;Wendel et al, 2016;Alix et al, 2017;Mandáková et al, 2019). The cultivated strawberry (Fragaria × ananassa Duchesne ex Rozier) is unique among domesticated crop species because it arose through both processes.…”

“…The chromosomes of octoploid garden strawberry (2n = 8x = 56) evolved through a combination of ancient polyploidy, and repeated homoploid hybridization in the last three centuries (Duchesne, 1766;Darrow, 1966). The presence of duplicated (homoeologous) chromosomes in plants frequently leads to meiotic anomalies and associated chromosomal rearrangements, e.g., translocations and inversions, that reduce or eliminate gene flow between the donors and their polyploid offspring (Soltis et al, 2014a;Soltis et al, 2014b;Alix et al, 2017;Latta et al, 2019;Mandáková et al, 2019). Similarly, meiotic mispairing in interspecific homoploid hybrids can lead to rearranged offspring chromosomes that differ from the chromosomes of one or both parents, resulting in reproductive barriers and hybrid speciation, as has been widely documented in sunflower (Helianthus) and other plants (Rieseberg, 1997;Burke et al, 2004;Abbott et al, 2010;Barb et al, 2014;Yakimowski and Rieseberg, 2014).…”

Assessing Diversity in theCamelinaGenus Provides Insights into the Genome Structure ofCamelina sativa

“…The genome sequence of C. sativa suggested a neopolyploid that had evolved from three lower chromosome number species, specifically one n = 6 and two n = 7 species (Kagale et al 2014). Camelina species such as C. neglecta, C. laxa and C. hispida possess the same haploid chromosome numbers as subgenomes of the hexaploid and recent work has proposed that C. neglecta and C. hispida could indeed be extant progenitors of C. sativa (Mandáková et al 2019). The study of these lower ploidy species could be instrumental in defining the relationship among the species as well as uncovering the polyploidization history of Camelina (Brock et al 2019).…”