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Sequence analysis, chromosomal distribution and long-range organization show that rapid turnover of new and old pBuM satellite DNA repeats leads to different patterns of variation in seven species of the Drosophila buzzatii cluster

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Abstract

We aimed to study patterns of variation and factors influencing the evolutionary dynamics of a satellite DNA, pBuM, in all seven Drosophila species from the buzzatii cluster (repleta group). We analyzed 117 alpha pBuM-1 (monomer length 190 bp) and 119 composite alpha/beta (370 bp) pBuM-2 repeats and determined the chromosome location and long-range organization on DNA fibers of major sequence variants. Such combined methodologies in the study of satDNAs have been used in very few organisms. In most species, concerted evolution is linked to high copy number of pBuM repeats. Species presenting low-abundance and scattered distributed pBuM repeats did not undergo concerted evolution and maintained part of the ancestral inter-repeat variability. The alpha and alpha/beta repeats colocalized in heterochromatic regions and were distributed on multiple chromosomes, with notable differences between species. High-resolution FISH revealed array sizes of a few kilobases to over 0.7 Mb and mutual arrangements of alpha and alpha/beta repeats along the same DNA fibers, but with considerable changes in the amount of each variant across species. From sequence, chromosomal and phylogenetic data, we could infer that homogenization and amplification events involved both new and ancestral pBuM variants. Altogether, the data on the structure and organization of the pBuM satDNA give insights into genome evolution including mechanisms that contribute to concerted evolution and diversification.

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Authors and Affiliations

  1. Departamento de Genética e Evolução, Universidade Federal de São Carlos, Via Washington Luís, Km 235, 13565-905, São Carlos, SP, Brazil

    Gustavo C. S. Kuhn & Orlando Moreira-Filho

  2. Departamento de Genética, Universidade de São Paulo, Faculdade de Medicina de Ribeirão Preto, Ribeirão Preto, SP, Brazil

    Fabio M. Sene

  3. Department of Biology, University of Leicester, Leicester, UK

    Trude Schwarzacher & John S. Heslop-Harrison

Authors
  1. Gustavo C. S. Kuhn
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  2. Fabio M. Sene
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  3. Orlando Moreira-Filho
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  4. Trude Schwarzacher
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  5. John S. Heslop-Harrison
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Corresponding author

Correspondence to Gustavo C. S. Kuhn.

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Supplementary Figure S1

Map of part of South America showing the geographical distribution of the buzzatii cluster with the approximate geographical localities of the Drosophila strains studied in the present work. (1) Morro do Chapéu, Cachoeira do Ferro Doido, Cafarnaum (BA), (2) Ibotirama (BA), (3) Milagres (BA), (4) Grão Mogol (MG), (5) Sertãozinho (SP), (6) Serrana (SP), (7) Arraial do Cabo (RJ), (8) Arroio Teixeira (RS), (9) Tramandai (RS), (10) San Juan, (11) Famatina, (12) Catamarca, (13) Ticucho and (14) Tapia. (PPT 920KB)

Supplementary Figure S2

Nucleotide alignment containing alpha pBuM-1 sequences from D. serido (DsdoA2), D. antonietae (DantA2), D. koepferae (DkoeA2), D. borborema (DborA2) and D. buzzatii (DbuzA1 and DbuzA2). The nucleotide sequences of direct neighbor repeats (dimers) are named as a and b after the repeat notations. The method used for the isolation of the sequences is shown within parentheses (PA2 = primers A2F/R). The region corresponding to the annealing of primers A1F, A2F (green) and A1F, A2R (red) is indicated (yellow represents overlap of primers). The location of restriction sites responsible for the isolation of high-copy number alpha repeats is indicated. Asterisks represent deletions. See Table 1 for accession numbers. (DOC 73.5KB)

Supplementary Figure S3

Nucleotide alignment containing alpha/beta pBuM-2 sequences from D. gouveai (DgouAB), D. seriema (DsmaAB), D. antonietae (DantAB), D. serido (DsdoAB), D. koepferae (DkoeAB), D. borborema (DborAB) and D. buzzatii (DbuzAB). The beta sequence is underlined. The method used for the isolation of the sequences is shown (PA2 = primers A2F/R and PB1 = primers PB1F/R). The region corresponding to the annealing of primers A2F, B1F (green) and A2R, B1R (red) is indicated (yellow represents overlap of primers). The location of restriction sites responsible for the isolation of high-copy-number alpha/beta repeats is also indicated. Some of the alpha/beta repeats showing large rearrangements were not included. Asterisks represent deletions. See Table 1 for accession numbers. (DOC 128KB)

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Kuhn, G.C.S., Sene, F.M., Moreira-Filho, O. et al. Sequence analysis, chromosomal distribution and long-range organization show that rapid turnover of new and old pBuM satellite DNA repeats leads to different patterns of variation in seven species of the Drosophila buzzatii cluster. Chromosome Res 16, 307–324 (2008). https://doi.org/10.1007/s10577-007-1195-1

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