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Accumulation of Y-specific satellite DNAs during the evolution of Rumex acetosa sex chromosomes

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Abstract

The study of the molecular structure of young heteromorphic sex chromosomes of plants has shed light on the evolutionary forces that control the differentiation of the X and Y during the earlier stages of their evolution. We have used the model plant Rumex acetosa, a dioecious species with multiple sex chromosomes, 2n = 12 + XX female and 2n = 12 + XY1Y2 male, to analyse the significance of repetitive DNA accumulation during the differentiation of the Y. A bulk segregant analysis (BSA) approach allowed us to identify and isolate random amplified polymorphic DNA (RAPD) markers linked to the sex chromosomes. From a total of 86 RAPD markers in the parents, 6 markers were found to be linked to the Ys and 1 to the X. Two of the Y-linked markers represent two AT-rich satellite DNAs (satDNAs), named RAYSII and RAYSIII, that share about 80% homology, as well as with RAYSI, another satDNA of R. acetosa. Fluorescent in situ hybridisation demonstrated that RAYSII is specific for Y1, whilst RAYSIII is located in different clusters along Y1 and Y2. The two satDNAs were only detected in the genome of the dioecious species with XX/XY1Y2 multiple sex chromosome systems in the subgenus Acetosa, but were absent from other dioecious species with an XX/XY system of the subgenera Acetosa or Acetosella, as well as in gynodioecious or hermaphrodite species of the subgenera Acetosa, Rumex and Platypodium. Phylogenetic analysis with different cloned monomers of RAYSII and RAYSIII from both R. acetosa and R. papillaris indicate that these two satDNAs are completely separated from each other, and from RAYSI, in both species. The three Y-specific satDNAs, however, evolved from an ancestral satDNA with repeating units of 120 bp, through intermediate satDNAs of 360 bp. The data therefore support the idea that Y-chromosome differentiation and heterochromatinisation in the Rumex species having a multiple sex chromosome system have occurred by different amplification events from a common ancestral satDNA. Since dioecious species with multiple XX/XY1Y2 sex chromosome systems of the section Acetosa appear to have evolved from dioecious species with an XX/XY system, the amplification of tandemly repetitive elements in the Ys of the section Acetosa is a recent evolutionary process that has contributed to an increase in the size and differentiation of the already non-recombining Y chromosomes.

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Acknowledgments

This work was supported by grants BXX2000-1144-C02 and BOS2003-08737-C02 awarded by the Dirección General de Investigación (DGI) of the Ministerio de Ciencia of Spain. The work of BV and EK was supported by the LC06004 grant from Ministry of Education, grant 521/06/0056 from the Grant Agency of the Czech Republic, and grants no. AV0Z50040507 and AV0Z50040702 from the Academy of Sciences of the Czech Republic.

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Authors and Affiliations

  1. Departamento de Biología Aplicada, Escuela Politécnica Superior, Universidad de Almería, 04120, Almería, Spain

    Beatrice Mariotti, Susana Manzano & Manuel Jamilena

  2. Institute of Biophysics, Academy of Sciences of the Czech Republic, Brno, Czech Republic

    Eduard Kejnovský & Boris Vyskot

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  1. Beatrice Mariotti
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  2. Susana Manzano
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  3. Eduard Kejnovský
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  4. Boris Vyskot
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  5. Manuel Jamilena
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Correspondence to Manuel Jamilena.

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Communicated by Y. Van de Peer.

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Mariotti, B., Manzano, S., Kejnovský, E. et al. Accumulation of Y-specific satellite DNAs during the evolution of Rumex acetosa sex chromosomes. Mol Genet Genomics 281, 249–259 (2009). https://doi.org/10.1007/s00438-008-0405-7

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  • DOI: https://doi.org/10.1007/s00438-008-0405-7

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