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Next-generation sequencing, FISH mapping and synteny-based modeling reveal mechanisms of decreasing dysploidy in Cucumis

Luming Yang, Dal-Hoe Koo, Dawei Li, Tao Zhang, Jiming Jiang, Feishi Luan, Susanne S. Renner, Elizabeth Henaff, Walter Saneverino, Jordi Garcia-Mas, Josep Casacuberta, Douglas A. Senalik, Philipp W. Simon, Jinfeng Chen, Yiqun Weng
Plant Journal 2014 v.77 no.1 pp. 16-30
Cucumis melo, Cucumis sativus, chromosome inversions, chromosome mapping, chromosome translocation, chromosomes, cucumbers, cytogenetic analysis, evolution, fluorescence in situ hybridization, gene fusion, genome, genomics, melons, models, sequence homology
In the family of Cucurbitaceae, cucumber (Cucumis sativus) is the only species with 14 chromosomes. The majority of the remaining species, including melon and the sister species of cucumber, C. hystrix, have 24 chromosomes. To understand the underlying mechanisms of chromosome reduction from n=12 to n=7, we investigated chromosome synteny among cucumber, C. hystrix, and melon using integrated and complementary genomics, cytogenetic and molecular approaches. The results reveal the location and orientation of 53 C. hystrix syntenic blocks on the seven cucumber chromosomes and allow us to infer at least 59 chromosome rearrangement events that led to the seven cucumber chromosomes, including five fusions, four translocations, and 50 inversions. The 12 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 a head-to-head fusion between AK9 and AK10. Chromosomes C2, C4 and C6 were the result of complex reshuffling of syntenic blocks from 3, 4 and 5 ancestral chromosomes, respectively, through 33 fusion, translocation and inversion events. Previous results that cucumber C7 stayed largely intact during the entire evolution of Cucumis are supported. Having the new genome of the closest relative of cucumber, together with that of melon, allows a fine-scale understanding of the mechanisms of dysploid chromosome reduction not achieved previously.