Complete sequences of the rRNA genes of Drosophila melanogaster (original) (raw)
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Complete Sequences of the rRNA Genes of Drosophila melanogaster 1
Molecular Biology and Evolution, 1988
In this, the first of three papers, we present the sequence of the ribosomal RNA (rRNA) genes of Drosophila melanogaster. The gene regions of D. melanogaster rDNA encode four individual rRNAs: 18s (1,995 nt), 5.8s (123 nt), 2s (30 nt), and 28s (3,945 nt). The ribosomal DNA (rDNA) repeat of D. melanogaster is AT rich (65.9% overall), with the spacers being particularly AT rich. Analysis of DNA simplicity reveals that, in contrast to the intergenic spacer (IGS) and the external transcribed spacer (ETS), most of the rRNA gene regions have been refractory to the action of slippage-like events, with the exception of the 28s rRNA gene expansion segments. It would seem that the 28s rRNA can accommodate the products of slippage-like events without loss of activity. In the following two papers we analyze the effects of sequence divergence on the evolution of (1) the 28s gene "expansion segments" and (2) the 28s and 18s rRNA secondary structures among eukaryotic species, respectively. Our detailed analyses reveal, in addition to unequal crossingover, (1) the involvement of slippage and biased mutation in the evolution of the rDNA multigene family and (2) the molecular coevolution of both expansion segments and the nucleotides involved with compensatory changes required to maintain secondary structures of RNA.
Molecular biology and evolution, 1988
This paper examines the effects of DNA sequence evolution on RNA secondary structures and compensatory mutations. Models of the secondary structures of Drosophila melanogaster 18S ribosomal RNA (rRNA) and of the complex between 2S, 5.8S, and 28S rRNAs have been drawn on the basis of comparative and energetic criteria. The overall AU richness of the D. melanogaster rRNAs allows the resolution of some ambiguities in the structures of both large rRNAs. Comparison of the sequence of expansion segment V2 in D. melanogaster 18S rRNA with the same region in three other Drosophila species and the tsetse fly (Glossina morsitans morsitans) allows us to distinguish between two models for the secondary structure of this region. The secondary structures of the expansion segments of D. melanogaster 28S rRNA conform to a general pattern for all eukaryotes, despite having highly divergent sequences between D. melanogaster and vertebrates. The 70 novel compensatory mutations identified in the 28S rR...
Nontranscribed spacers in Drosophila ribosomal DNA
Chromosoma, 1981
Ribosomal DNA nontranscribed spacers in Drosophila virilis DNA have been examined in some detail by restriction site analysis of cloned segments of rDNA, nucleic acid hybridizations involving unfractionated rDNA, and base composition estimates, The overall G+C content of the spacer is 27-28%; this compares with 39% for rDNA as a whole, 40% for main band DNA, and 26% for the D. virilis satellites. Much of the spacer is comprised of 0.25 kb repeats revealed by digestion with Msp I, Fnu DII or Rsd I, which terminate very near the beginning of the template for the ribosomal RNA precursor. The spacers are heterogeneous in length among rDNA repeats, and this is largely accounted for by variation among rDNA units in the number of 0.25 kb elements per spacer. Despite its high A+T content and the repetitive nature of much of the spacer, and the proximity of rDNA and heterochromatin in Drosophila, pyrimidine tract analysis gave no indication of relatedness between the spacer and satellite DNA sequences. Species of Drosophila closely related to D. virilis have rDNA spacers that are homologous with those in D. virilis to the extent that hybridization of a cloned spacer segment of D. virilis rDNA to various DNA is comparable with hybridization to homologous DNA, and distributions of restriction enzyme cleavage sites are very similar (but not identical) among spacers of the various species. There is spacer length heterogeneity in the rDNA of all species, and each species has a unique major rDNA spacer length. Judging from Southern blot hybridization, D. hydei rDNA spacers have 20-30% sequence homology with D. virilis rDNA spacers, and a repetitive component is similarly sensitive to Msp I and Fnu DII digestion. D. melanogaster rDNA spacers have little or no homology with counterparts in D. virilis rDNA, despite a similar content of 0.25 kb repetitive elements. In contrast, sequences in rDNA that encode 18S and 28S ribosomal RNA have been highly conserved during the divergence of Drosophila species; this is inferred from interspecific hybridizations involving ribosomal RNA and a comparison of distributions of restriction enzyme cleavage sites in rDNA.
X and Y chromosomal ribosomal DNA of drosophila: comparison of spacers and insertions
Cell, 1978
In Drosophila melanogaster, the genes coding for 18s and 28s ribosomal RNA (rDNA) are clustered at one locus each on the X and the Y chromosomes. We have compared the structure of rDNA at the two loci. The 18s and 28s rRNAs coded by the X and Y chromosomes are very similar and probably identical (Maden and Tartof, 1974). In D. melanogaster, many rDNA repeating units are interrupted in the 28s RNA sequence by a DNA region called the insertion. There are at least two sequence types of insertions. Type 1 insertions include the most abundant 5 kilobase (kb) class and homologous small (0.5 and 1 kb) insertions. Most insertions between 1.5 and 4 kb have no homology to the 5 kb class and are identified as type 2 insertions. In X rDNA, about 49% of all rDNA repeats have type 1 insertions, and another 16% have type 2 insertions. On the Y chromosome, only 16% of all rDNA repeats are interrupted, and most if not all insertions are of type 2. rDNA fragments derived from the X and Y chromosomes have been cloned in E. coli. The homology between the nontranscribed spacers in X and Y rDNA was studied with cloned fragments. Stable heteroduplexes were found which showed that these regions on the two chromosomes are very similar. The evolution of rDNA in D. melanogaster might involve genetic exchange between the X and Y chromosomal clusters with restrictions on the movement of type 1 insertions to the Y chromosome.
Heredity, 2005
The evolution of the chromosomal location of ribosomal RNA gene clusters and the organization of heterochromatin in the Drosophila melanogaster group were investigated using fluorescence in situ hybridization and DAPI staining to mitotic chromosomes. The investigation of 18 species (11 of which were being examined for the first time) belonging to the melanogaster and ananassae subgroups suggests that the ancestral configuration consists of one nucleolus organizer (NOR) on each sex chromosome. This pattern, which is conserved throughout the melanogaster subgroup, except in D. simulans and D. sechellia, was observed only in the ercepeae complex within the ananassae subgroup. Both sexlinked NORs must have been lost in the lineage leading to D. varians and in the ananassae and bipectinata complexes, whereas new sites, characterized by intra-species variation in hybridization signal size, appeared on the fourth chromosome related to heterochromatic rearrangements. Nucleolar material is thought to be required for sex chromosome pairing and disjunction in a variety of organisms including Drosophila. Thus, either remnant sequences, possibly intergenic spacer repeats, are still present in the sex chromosomes which have lost their NORs (as observed in D. simulans and D. sechellia), or an alternative mechanism has evolved. Heredity (2005) 94, 388-395.
‘Compensatory slippage’ in the evolution of ribosomal RNA genes
Nucleic Acids Research, 1990
The distribution patterns of shared short repetitive motifs in the expansion segments of the large subunit rRNA genes of different species show that these segments are coevolvlng as a set and that in two examined vertebrate species the RNA secondary structures are conserved as a consequence of runs of motifs In one region being compensated by complementary motifs in another. These unusual processes, Involving replication-slippage, have implications for the evolution of ribosomal RNA and for the use of the rDNA multigene family as a 'molecular clock' for assessing relationships between species.
The contribution of DNA slippage to eukaryotic nuclear 18S rRNA evolution
Journal of Molecular Evolution, 1995
Six of 204 eukaryotic nuclear small-subunit ribosomal RNA sequences analyzed show a highly significant degree of clustering of short sequence motifs that indicates the fixation of products of replication slippage within them in their recent evolutionary history. A further 72 sequences show weaker indications of sequence repetition. Repetitive sequences in SSU rRNAs are preferentially located in variable regions and in particular in V4 and V7. The conserved region immediately 5' to V7 (C7) is also consistently repetitive. Whereas variable regions vary in length and appear to have evolved by the fixation of slippage products, C7 shows no indication of length variation. Repetition within C7 is therefore either not a consequence of slippage or reflects very ancient slippage events. The phylogenetic distribution of sequence simplicity in small-subunit rRNAs is patchy, being largely confined to the Mammalia, Apicomplexa, Tetrahymenidae, and Trypanosomatidae. The regions of the molecule associated with sequence simplicity vary with taxonomic grouping as do the sequence motifs undergoing slippage. Comparison of rates of insertion and substitution in a lineage within the genus Plasmodium confirms that both rates are higher in variable regions than in conserved regions. The insertion rate in variable regions is substantially lower than the substitution rate, suggesting that selection acts more strongly on slippage products than on point mutations in these regions. Patterns of coevolution between variable regions *Present address: MRC Clinical Sciences Centre, Royal Postgraduate Medical School, Hammersrnith Hospital, London W12 0NN, UK may reflect the consequences of selection acting on the incorporation of slippage-derived sequences across the gene. Key words: 18S rRNA evolution --Molecular coevolution --Replication slippage --Variable regions --Compensatory slippage Drosophila melanogaster. Mol Biol Evol 5:393-414 Kimura M, Ohta T (1972) On the stochastic model for estimation of mutational distance between homologous proteins. J Mol Evol 2: 87-90 Kornegay JR, Kocher TD, Williams LA, Wilson AC (1993) Pathways of lysozyme evolution inferred from the sequences of cytochrome b in birds. J Mol Evol 37:367-379 Leipe DD, Gunderson JH, Nerad TA, Sogin ML (1993) Small subunit ribosomal RNA+ of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol Biochem Parasitol 59:41-48 Larsen N, Olsen GJ, Maldak BL, McCanghey MJ, Overbeek R, Macke TJ, Woese CR (1993) The ribosomal database project. Nucleic Acids Res 21:3021-3023
Evolution of 5S rRNA gene families in Drosophila
Chromosome Research
In Drosophila virilis, the three clusters of 5S rRNA genes on chromosome 5 comprise two different gene families (B and C), which differ profoundly in the organization of their spacer sequences. While C-type genes, which are found in two of the clusters, exhibit a true repetitive character, the B-type genes of the third cluster are each embedded in completely different genomic environments. Southern blots of genomic DNA of different D. virilis subspecies, D. hydei and D. melanogaster probed with 5S rRNA gene spacer and coding sequences demonstrate the specificity of C-type sequences for the D. virilis species group. The comparative analysis of flanking sequences of 5S rRNA genes of D. virilis, members of the D. melanogaster species subgroup and of the blowfly Calliphora erythrocephala reveals the existence of conserved sequence motifs both in the 5' upstream and 3' downstream flanking regions. Their possible roles in the control of expression and processing of the 5S rRNA pre...
Characterization of ribosomal DNA (rDNA) in Drosophila arizonae
Genetics and Molecular Biology, 2000
Ribosomal DNA (rDNA) is a multigenic family composed of one or more clusters of repeating units (RU). Each unit consists of highly conserved sequences codifying 18S, 5.8S and 28S rRNA genes intercalated with poorly conserved regulatory sequences between species. In this work, we analyzed the rDNA of Drosophila arizonae, a member of the mulleri complex (Repleta group). Using genomic restriction patterns, cloning and mapping of some representative rDNA fragments, we were able to construct a representative restriction map. RU in this species are 13.5-14 kb long, restriction sites are completely conserved compared with other drosophilids and the rDNA has an R1 retrotransposable element in some RU. We were unable to detect R2 elements in this species.