Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intrachromosomal exchanges drive concerted evolution

BACKGROUND The individual copies of tandemly repeated genes, such as ribosomal DNA (rDNA), evolve coordinately within a species. This phenomenon has been called concerted evolution, and is thought to be caused by sequence-homogenizing mechanisms, such as gene conversion or unequal crossing-over between individual copies of the gene family. As these processes would act between the arrays on homologous and non-homologous chromosomes, the whole family of repeats would be expected to undergo homogenization in a given interbreeding population. RESULTS In order to study the homogenization process, we have examined polymorphisms within the internal transcribed spacer (ITS) of the rDNA in populations of Drosophila melanogaster at the sequence level, by DNA sequencing and temperature-gradient gel electrophoresis. Among 84 ITS clones sequenced from five different wild-type strains, we found three polymorphic sites that are apparently in the process of homogenization. However, these three sites, as well as combinations of them, occurred at different frequencies in the different strains. Moreover, temperature-gradient gel electrophoresis analysis of an ITS fragment including these three sites shows that single chromosomes from locally interbreeding populations can harbor rDNA arrays that are largely homogenized for different sequence variants. CONCLUSIONS The presence of chromosomal arrays that are homogeneous for different variants in interbreeding populations of Drosophila melanogaster indicates that there is little recombination between the chromosomes while new mutations are being homogenized along the individual arrays. The most likely explanation for this finding is that intrachromosomal recombination events occur at much higher rates than recombination between homologous chromosomes. Thus, the first step of the homogenization process would occur mainly within chromosomal lines. Such behavior of tandem repeat arrays suggests a simple explanation of how selection can act on a multigene family, namely by acting on whole chromosomally confined repeat arrays rather than on individual repeat units.

[1]  C. Strobeck,et al.  Evolution of the ribosomal DNA spacers of Drosophila melanogaster: different patterns of variation on X and Y chromosomes. , 1987, Genetics.

[2]  R. Jorgensen,et al.  Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[3]  E. Coen,et al.  Unequal exchanges and the coevolution of X and Y rDNA arrays in drosophila melanogaster , 1983, Cell.

[4]  O. Ryder,et al.  Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[5]  I. Dawid,et al.  X and Y chromosomal ribosomal DNA of drosophila: comparison of spacers and insertions , 1978, Cell.

[6]  K. Mullis,et al.  Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. , 1988, Science.

[7]  R. Hawley,et al.  Recombinational Controls of rDNA Redundancy in Drosophila , 1989 .

[8]  A. Clark,et al.  Evolution of ribosomal RNA gene copy number on the sex chromosomes of Drosophila melanogaster. , 1991, Molecular biology and evolution.

[9]  P. D’Eustachio,et al.  Human nucleolus organizers on nonhomologous chromosomes can share the same ribosomal gene variants. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[10]  M. Muramatsu,et al.  Drosophila melanogaster has different ribosomal RNA sequences on S and Y chromosomes. , 1979, Journal of molecular biology.

[11]  R. Wartell,et al.  Detecting base pair substitutions in DNA fragments by temperature-gradient gel electrophoresis. , 1990, Nucleic acids research.

[12]  T. Ohta,et al.  The cohesive population genetics of molecular drive. , 1984, Genetics.

[13]  T. Schedl,et al.  fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. , 1988, Genetics.

[14]  G. Dover,et al.  Linkage disequilibrium and molecular drive in the rDNA gene family. , 1989, Genetics.

[15]  John M. Hancock,et al.  Complete sequences of the rRNA genes of Drosophila melanogaster. , 1988, Molecular biology and evolution.

[16]  A. Clark,et al.  Ribosomal DNA and Stellate gene copy number variation on the Y chromosome of Drosophila melanogaster. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[17]  E. Coen,et al.  Rate of turnover of structural variants in the rDNA gene family of Drosophila melanogaster , 1982, Nature.

[18]  T. Strachan,et al.  Dynamics of concerted evolution of ribosomal DNA and histone gene families in the melanogaster species subgroup of Drosophila. , 1982, Journal of molecular biology.

[19]  T. Ohta.  Simple model for treating evolution of multigene families , 1976, Nature.

[20]  K. Sugimoto,et al.  The structure and evolution of ribosomal and 5S DNAs in Xenopus laevis and Xenopus mulleri. , 1974, Cold Spring Harbor symposia on quantitative biology.

[21]  S. Endow,et al.  Magnification: gene amplification by an inducible system of sister chromatid exchange. , 1988, Trends in genetics : TIG.

[22]  R. Frankham,et al.  X-Y Exchange and the Coevolution of the X and Y Rdna Arrays in Drosophila melanogaster. , 1987, Genetics.

[23]  I. Dawid,et al.  Similarities and differences in the structure of X and Y chromosome rRNA genes of Drosophila , 1976, Nature.

[24]  G. Dover.  Molecular drive in multigene families: How biological novelties arise, spread and are assimilated , 1986 .

[25]  G. P. Smith,et al.  Evolution of repeated DNA sequences by unequal crossover. , 1976, Science.

[26]  S. Paumard-Rigal,et al.  X chromosome variations of Bacillus thuringiensis supernatant resistance and ribosomal DNA content in Drosophila melanogaster wild-type Oregon R lines , 1993, Heredity.

[27]  Masatoshi Nei,et al.  Evolution of genes and proteins. , 1983 .

[28]  G. Dover,et al.  Molecular drive: a cohesive mode of species evolution , 1982, Nature.

[29]  M. Slatkin,et al.  Linkage disequilibrium in human ribosomal genes: implications for multigene family evolution. , 1988, Genetics.

[30]  A. von Haeseler,et al.  Comparative evolutionary analysis of rDNA ITS regions in Drosophila. , 1994, Molecular biology and evolution.

[31]  Y. Kan,et al.  Rapid duplication and loss of genes coding for the alpha chains of hemoglobin. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[32]  M. Slatkin.  Interchromosomal biased gene conversion, mutation and selection in a multigene family. , 1986, Genetics.

[33]  J. Kennison,et al.  Reciprocal recombination and the evolution of the ribosomal gene family of Drosophila melanogaster. , 1989, Genetics.

[34]  T. Nagylaki,et al.  Intrachromosomal gene conversion and the maintenance of sequence homogeneity among repeated genes. , 1982, Genetics.

[35]  L. Lerman,et al.  Length-independent separation of DNA restriction fragments in two-dimensional gel electrophoresis , 1979, Cell.

[36]  S. Williams,et al.  Molecular genetic analysis of Drosophila rDNA arrays. , 1992, Trends in genetics : TIG.

[37]  J. B. Walsh,et al.  Selection and biased gene conversion in a multigene family: consequences of interallelic bias and threshold selection. , 1986, Genetics.

[38]  H. Gelderblom,et al.  A very small porcine virus with circular single-stranded DNA , 1982, Nature.

[39]  T. Nagylaki.  Evolution of multigene families under interchromosomal gene conversion. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[40]  T. Ohta,et al.  Population genetics of multigene families that are dispersed into two or more chromosomes. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[41]  K. Tartof.  Unequal mitotic sister chromatin exchange as the mechanism of ribosomal RNA gene magnification. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[42]  B. Azzarone,et al.  Spontaneous transformation of human skin fibroblasts derived from neoplastic patients , 1976, Nature.