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Holokinetic centromeres and efficient telomere healing enable rapid karyotype evolution

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Abstract

Species with holocentric chromosomes are often characterized by a rapid karyotype evolution. In contrast to species with monocentric chromosomes where acentric fragments are lost during cell division, breakage of holocentric chromosomes creates fragments with normal centromere activity. To decipher the mechanism that allows holocentric species an accelerated karyotype evolution via chromosome breakage, we analyzed the chromosome complements of irradiated Luzula elegans plants. The resulting chromosomal fragments and rearranged chromosomes revealed holocentromere-typical CENH3 and histone H2AThr120ph signals as well as the same mitotic mobility like unfragmented chromosomes. Newly synthesized telomeres at break points become detectable 3 weeks after irradiation. The presence of active telomerase suggests a telomerase-based mechanism of chromosome healing. A successful transmission of holocentric chromosome fragments across different generations was found for most offspring of irradiated plants. Hence, a combination of holokinetic centromere activity and the fast formation of new telomeres at break points enables holocentric species a rapid karyotype evolution involving chromosome fissions and rearrangements.

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Acknowledgments

We are grateful to Ingo Schubert and all members of the Chromosome Structure & Function group for their fruitful discussions and to Katrin Kumke for excellent technical assistance. This work was supported by the Deutsche Forschungsgemeinschaft (SPP 1384, HO 1779/17-1) and the IPK (Gatersleben). The work performed at the Masaryk University was supported by the Czech Science Foundation (13-06943S), project CEITEC (CZ.1.05/1.1.00/02.0068) of the European Regional Development Fund and project CZ.1.07/2.3.00./20.0189 co-financed from European Social Fund and the State Budget of the Czech Republic.

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No research involving human participants or animals was performed.

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Authors and Affiliations

  1. Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), OT Gatersleben, Correnstrasse 3, D-06466, Stadt Seeland, Germany

    Maja Jankowska, Jörg Fuchs, Veit Schubert & Andreas Houben

  2. Julius Kühn-Institute, Institute for Breeding Research on Horticultural Crops, Erwin-Baur-Straße 27, D-06484, Quedlinburg, Germany

    Evelyn Klocke

  3. Mendel Centre for Plant Genomics and Proteomics, CEITEC, Masaryk University, Kamenice 5, CZ-625 00, Brno, Czech Republic

    Miloslava Fojtová, Pavla Polanská & Jiří Fajkus

  4. Laboratory of Functional Genomics and Proteomics, NCBR, Faculty of Science, Masaryk University, Kamenice 5, CZ-625 00, Brno, Czech Republic

    Miloslava Fojtová, Pavla Polanská & Jiří Fajkus

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  1. Maja Jankowska
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  2. Jörg Fuchs
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Correspondence to Andreas Houben.

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Supporting Information Movie S1

Rotation animation of L. elegans non-irradiated mitotic metaphase chromosomes after immunostaining with anti-H2AThr120ph and FISH using the Arabidopsis-type telomere probe (See also Fig. 2a). Note, the centromere spans over the entire chromosome, from telomere to telomere (MPG 6493 kb)

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Jankowska, M., Fuchs, J., Klocke, E. et al. Holokinetic centromeres and efficient telomere healing enable rapid karyotype evolution. Chromosoma 124, 519–528 (2015). https://doi.org/10.1007/s00412-015-0524-y

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