Hybridization‐facilitated genome merger and repeated chromosome fusion after 8 million years

Summary The small genus Ricotia (nine species, Brassicaceae) is confined to the eastern Mediterranean. By comparative chromosome painting and a dated multi‐gene chloroplast phylogeny, we reconstructed the origin and subsequent evolution of Ricotia. The ancestral Ricotia genome originated through hybridization between two older genomes with n = 7 and n = 8 chromosomes, respectively, on the Turkish mainland during the Early Miocene (c. 17.8 million years ago, Ma). Since then, the allotetraploid (n = 15) genome has been altered by two independent descending dysploidies (DD) to n = 14 in Ricotia aucheri and the Tenuifolia clade (2 spp.). By the Late Miocene (c. 10 Ma), the latter clade started to evolve in the most diverse Ricotia core clade (6 spp.), the process preceded by a DD event to n = 13. It is noteworthy that this dysploidy was mediated by a unique chromosomal rearrangement, merging together the same two chromosomes as were merged during the origin of a fusion chromosome within the paternal n = 7 genome c. 20 Ma. This shows that within a time period of c. 8 Myr genome evolution can repeat itself and that structurally very similar chromosomes may originate repeatedly from the same ancestral chromosomes by different pathways (end‐to‐end translocation versus nested chromosome insertion). Significance statement The ancestral Ricotia genome was formed by a rare inter‐clade hybridization event, followed by cladogenesis accompanied by three decreases in chromosome number (descending dysploidies). The last dysploidy was mediated by a unique chromosomal rearrangement, proving that structurally identical or similar fusion chromosomes may be formed in land plants from the same precursor chromosomes by different translocation mechanisms repeatedly after several million years.