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

Authors

  • Luming Yang,

    1. Horticulture Department, University of Wisconsin, Madison, WI, USA
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    • These authors contributed equally to this work.
  • Dal-Hoe Koo,

    1. Horticulture Department, University of Wisconsin, Madison, WI, USA
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    • These authors contributed equally to this work.
  • Dawei Li,

    1. Horticulture Department, University of Wisconsin, Madison, WI, USA
    2. Horticulture College, Northwest A & F University, Yangling, China
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  • Tao Zhang,

    1. Horticulture Department, University of Wisconsin, Madison, WI, USA
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  • Jiming Jiang,

    1. Horticulture Department, University of Wisconsin, Madison, WI, USA
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  • Feishi Luan,

    1. Horticulture College, Northeast Agricultural University, Harbin, China
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  • Susanne S. Renner,

    1. Department of Biology, University of Munich, Munich, Germany
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  • Elizabeth Hénaff,

    1. Centre for Research in Agricultural Genomics Consejo Superior de Investigaciones Científicas-Institut de Recerca i Tecnologia Agroalimentàries-Universitat Autònoma de Barcelona-Universitat de Barcelona, Barcelona, Spain
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  • Walter Sanseverino,

    1. Institut de Recerca i Tecnologia Agroalimentàries, Centre for Research in Agricultural Genomics Consejo Superior de Investigaciones Científicas-Institut de Recerca i Tecnologia Agroalimentàries-Universitat Autònoma de Barcelona-Universitat de Barcelona, Barcelona, Spain
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  • Jordi Garcia-Mas,

    1. Institut de Recerca i Tecnologia Agroalimentàries, Centre for Research in Agricultural Genomics Consejo Superior de Investigaciones Científicas-Institut de Recerca i Tecnologia Agroalimentàries-Universitat Autònoma de Barcelona-Universitat de Barcelona, Barcelona, Spain
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  • Josep Casacuberta,

    1. Centre for Research in Agricultural Genomics Consejo Superior de Investigaciones Científicas-Institut de Recerca i Tecnologia Agroalimentàries-Universitat Autònoma de Barcelona-Universitat de Barcelona, Barcelona, Spain
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  • Douglas A. Senalik,

    1. Horticulture Department, University of Wisconsin, Madison, WI, USA
    2. US Department of Agriculture/Agricultural Research Service, Vegetable Crops Research Unit, Madison, WI, USA
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  • Philipp W. Simon,

    1. Horticulture Department, University of Wisconsin, Madison, WI, USA
    2. US Department of Agriculture/Agricultural Research Service, Vegetable Crops Research Unit, Madison, WI, USA
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  • Jinfeng Chen,

    1. College of Horticulture, Nanjing Agricultural University, Nanjing, China
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  • Yiqun Weng

    Corresponding author
    1. Horticulture Department, University of Wisconsin, Madison, WI, USA
    2. US Department of Agriculture/Agricultural Research Service, Vegetable Crops Research Unit, Madison, WI, USA
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Summary

In the large Cucurbitaceae genus Cucumis, cucumber (C. sativus) is the only species with 2= 2= 14 chromosomes. The majority of the remaining species, including melon (C. melo) and the sister species of cucumber, C. hystrix, have 2= 2= 24 chromosomes, implying a reduction from = 12 to = 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., Zhang, Z. et al., 2009, 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.

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