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

Abstract

SUMMARYIn the large Cucurbitaceae genus Cucumis, cucumber (C. sativus) is the only species with 2n = 2x = 14 chromosomes. The majority of the remaining species, including melon (C. melo) and the sister species of cucumber, C. hystrix, have 2n = 2x = 24 chromosomes, implying a reduction from n = 12 to n = 7. To understand the underlying mechanisms, we investigated chromosome synteny among cucumber, C. hystrix and melon using integrated and complementary approaches. We identified 14 inversions and a C. hystrix lineage-specific reciprocal inversion between C. hystrix and melon. 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 inferred chromosomes (AK1-AK12) of an ancestor similar to melon and C. hystrix had strikingly different evolutionary fates, with cucumber chromosome C1 apparently resulting from insertion of chromosome AK12 into the centromeric region of translocated AK2/AK8, cucumber chromosome C3 originating from a Robertsonian-like translocation between AK4 and AK6, and cucumber chromosome C5 originating from fusion of AK9 and AK10. Chromosomes C2, C4 and C6 were the result of complex reshuffling of syntenic blocks from three (AK3, AK5 and AK11), three (AK5, AK7 and AK8) and five (AK2, AK3, AK5, AK8 and AK11) ancestral chromosomes, respectively, through 33 fusion, translocation and inversion events. Previous results (Huang, S., Li, R., , Nat. Genet. 41, 1275-1281; Li, D., Cuevas, H.E., Yang, L., Li, Y., Garcia-Mas, J., Zalapa, J., Staub, J.E., Luan, F., Reddy, U., He, X., Gong, Z., Weng, Y. 2011a, BMC Genomics, 12, 396) showing that cucumber C7 stayed largely intact during the entire evolution of Cucumis are supported. Results from this study allow a fine-scale understanding of the mechanisms of dysploid chromosome reduction that has not been achieved previously.

Chromosome-Specific Painting in Cucumis Species Using Bulked Oligonucleotides

“…Cucumber chromosome 7 (C7) has maintained a complete synteny with a single chromosome in the Cucumis species without interchromosomal rearrangements (Huang et al 2009;Yang et al 2014). Comparative genetic and genomic studies revealed a high degree of synteny and collinearity in the long arm of C7 (8 Mb) across the Cucumis species and beyond (Yang et al 2014). Thus, C7 provides an ideal target to test crossspecies chromosome painting using bulked oligo probes.…”

“…Seeds of all PI lines were obtained from the U.S. National Plant Germplasm System (Ames, IA). An interspecific F 1 hybrid between C. hystrix (accession TH1) and cucumber inbred line Gy14 was developed with embryo rescue (Yang et al 2014) and used for homeologous chromosome pairing study.…”

Molecular Phylogeny, Biogeography and an e-Monograph of the Papaya Family (Caricaceae) as an Example of Taxonomy in the Electronic Age

“…In Cucumis sativus, a similar mix of mechanisms led to dysploid chromosome reduction from an n = 12 ancestor to the n = 7 karyotype of cucumber (Yang et al 2013). Different from the other genera so far studied, large and small chromosome pairs are identifiable in the karyotype the two Jarilla species ( Fig.…”

“…1), possibly involving reduction a fusion of two chromosomes, which would explain the change from n = 9 to n = 8. Dysploid reductions in chromosome number have been analyzed in detail in Arabidopsis (Yogeeswaran et al 2005;Mandakova and Lysak 2008), Triticeae (Luo et al 2009), and recently Cucumis in fully sequenced genomes of cucumber and its sister species were compared (Yang et al 2013). In…”

Two reported cytotypes of the emergent orchid model species Erycina pusilla are two different species

“…This variability plays a critical role in species evolution and has been considered to be a consequence of chromosome rearrangement (Faria and Navarro 2010;Heslop-Harrison and Schwarzacher 2011). Such rearrangement may increase or decrease the chromosome number in the karyotype and is termed ascending or descending dysploidy (Schubert and Lysak 2011;Leitch et al 2013;De Storme and Mason 2014;Yang et al 2014).…”