Mechanisms of Decreasing Dysploidy in Cucumis

In Cucumis (family Cucurbitaceae), cucumber (C. sativus) is the only species with 2n = 2x = 14 chromosomes. The majority of the remaining species, including melon (C. melo) and C. hystrix, have 2n = 2x = 24 chromosomes suggesting a reduction from n = 12 to n = 7. To understand the underlying mechanisms we investigated chromosome synteny among cucumber, C. hystrix, and melon. We identified 14 inversions and a C. hystrix lineage-specific reciprocal inversion between C. hystrix and melon. We identified the location and orientation of 53 C. hystrix syntenic blocks on the seven cucumber chromosomes which allowed us to infer at least 59 chromosome rearrangement events leading to the seven cucumber chromosomes, including five fusions, four translocations, and 50 inversions. The 12 inferred chromosomes of an ancestor (AK1-AK12) similar to melon and C. hystrix had strikingly different evolutionary fates, with cucumber chromosome C1 apparently resulting from the insertion of chromosome AK12 into the centromeric region of translocated AK2/AK8, cucumber C3 originating from a Robertsonian-like translocation between AK4 and AK6, and C5 from the fusion of AK9 and AK10. Chromosomes C2, C4 and C6 were the result of complex reshuffling of syntenic blocks from 3 (AK3, AK5, and AK11), 3 (AK5, AK7, and AK8) and 5 (AK2, AK3, AK5, AK8 and AK11) ancestral chromosomes, respectively, through 33 fusion, translocation and inversion events. Cucumber C7 stayed largely intact during the entire evolution of Cucumis.