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Effect of location, organization, and repeat-copy number in satellite-DNA evolution

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Abstract

Here, we analyze the evolutionary dynamics of a satellite-DNA family in an attempt to understand the effect of factors such as location, organization, and repeat-copy number in the molecular drive process leading to the concerted-evolution pattern found in this type of repetitive sequences. The presence of RAE180 satellite-DNA in the dioecious species of the plant genus Rumex is a noteworthy feature at this respect, as RAE180 satellite repeats have accumulated differentially, showing a distinct distribution pattern in different species. The evolution of dioecious Rumex gave rise to two phylogenetic clades: one clade composed of species with an ancestral XX/XY sex chromosome system and a second, derived clade of species with a multiple sex–chromosome system XX/XY1Y2. While in the XX/XY dioecious species, the RAE180 satellite-DNA is located only in a small autosomal locus, the RAE180 repeats are present also in a small autosomal locus and additionally have been massively amplified in the Y chromosomes of XX/XY1Y2 species. Here, we have found that the RAE180 repeats of the autosomal locus of XX/XY species are characterized by intra-specific sequence homogeneity and inter-specific divergence and that the comparison of individual nucleotide positions between related species shows a general pattern of concerted evolution. On the contrary, both in the autosomal and the Y-linked loci of XX/XY1Y2 species, ancestral variability has remained with reduced rates of sequence homogenization and of evolution. Thus, this study demonstrates that molecular mechanisms of non-reciprocal exchange are key factors in the molecular drive process; the satellite DNAs in the non-recombining Y chromosomes show low rates of concerted evolution and intra-specific variability increase with no inter-specific divergence. By contrast, freely recombining loci undergo concerted evolution with genetic differentiation between species as occurred in the autosomal locus of XX/XY species. However, evolutionary periods of rapid sequence change might alternate with evolutionary periods of stasis with variability remaining by the reduced action of molecular mechanisms of non-reciprocal exchange as occurred in XX/XY1Y2 species, which could depend on repeat-copy number and the processes involved in their amplification.

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Acknowledgments

Our thanks to Dr. Ginés López González (Real Jardín Botánico de Madrid, Spain), and to the Parque Nacional de Sierra Nevada and to the Parque Natural de la Sierra de Baza, for kindly providing the material analyzed in this article. We also are deeply indebted to Dr. Miguel Burgos of the University of Granada for advice and help with the satellite-DNA quantification procedure. This research was supported by grant CGL2006-00444/BOS of the Ministerio of Ciencia e Innovación (Spain) and Fondo Europeo de Desarrollo Regional (FEDER, EU).

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Authors and Affiliations

  1. Departamento de Genética, Facultad de Ciencias, Universidad de Granada, 18071, Granada, Spain

    R. Navajas-Pérez, M. E. Quesada del Bosque & M. A. Garrido-Ramos

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  1. R. Navajas-Pérez
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  2. M. E. Quesada del Bosque
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  3. M. A. Garrido-Ramos
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Corresponding author

Correspondence to M. A. Garrido-Ramos.

Additional information

Communicated by S. Hohmann.

R. Navajas-Pérez and M. E. Quesada del Bosque contributed equally to this work.

Electronic supplementary material

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Supplementary material Sm1

Graphic representation of patterns of distributions of mutations at individual nucleotide positions across repeats a–f in two species, A and B (modified from Strachan et al. 1985 and from Pons et al. 2002). SP A-B . Shared polymorphic site between species A and B. The same mutation (black circles) is shared by some repeats of both species. I–VI. Transition stages during the spread of new mutations in the molecular drive process: Classes I–VI. Class I represents complete homogeneity across all repeats randomly sampled from a pair of species (white circles). Classes II, III, and IV would represent intermediate stages where a new mutation (black circle) is gradually spread throughout the satellite-DNA family in one species, whereas the other species remains homogeneous for the progenitor base in the corresponding position. All subsequent mutations (grey circle) beyond this point are represented by the pattern shown in class VI. (PDF 15.3 kb)

Supplementary material Sm2

Multiple sequence alignment for RAE180 sequences from R. suffruticosus and R. acetosella (PDF 9.18 kb)

Supplementary material Sm3

Multiple sequence alignment for RAE180 sequences from R. acetosa and R. papillaris (PDF 8.04 kb)

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Navajas-Pérez, R., Quesada del Bosque, M.E. & Garrido-Ramos, M.A. Effect of location, organization, and repeat-copy number in satellite-DNA evolution. Mol Genet Genomics 282, 395–406 (2009). https://doi.org/10.1007/s00438-009-0472-4

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  • DOI: https://doi.org/10.1007/s00438-009-0472-4

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