Intervening sequences in the ribosomal RNA genes of Ascaris lumbricoides: DNA sequences at junctions and genomic organization.

Back, Eduard; Meir, Efrat; Müller, Fritz; Schaller, Dominique; Neuhaus, Heinz; Aeby, Pierre; Tobler, Heinz

doi:10.1002/j.1460-2075.1984.tb02167.x

Cited by 23 publications

(16 citation statements)

References 32 publications

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“…Since the genomic DNAs were isolated from pools of animals, we cannot distinguish between these two alternatives. The A. lumbricoides cDNA probe crosshybridizes under high-stringency conditions to the P. equo- The probe hybridizes to the major organizational form of the Ascaris rDNA as well as to a fainter band, representing the minor rDNA form (26). (B) Total P. equorum DNA digested with EcoRI.…”

Section: Methodsmentioning

confidence: 99%

“…No signal is detected in the somatic DNA of both species, demonstrating the elimination of the ALEP-1 gene from all somatic cells in both nematodes. As a control, the blot was retested with cloned Ascaris rDNA (26).…”

Section: Methodsmentioning

confidence: 99%

“…Arrow indicates the deduced length of the mRNA that codes for ALEP-1. (B) The same filter was rehybridized with a nick-translated, cloned Ascaris 18S rDNA fragment (26), showing that the same amount of RNA (5 ,ug) was loaded in the first three lanes (oocyte, day 1, and day 4). The day-li lane, however, contained less RNA, but even after very long exposure time, no hybridization signal with the ALEP-1 probe could be detected.…”

Section: Methodsmentioning

confidence: 99%

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Eliminated chromatin of Ascaris contains a gene that encodes a putative ribosomal protein.

Etter

Aboutanos

Tobler

et al. 1991

Proc. Natl. Acad. Sci. U.S.A.

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Chromatin diminution in the nematodes Parascaris equorum and-Ascaris lumbrcoides leads to the formation of somatic cells that contain less DNA than the germ-line cells. We present molecular evidence for the coding potential of germ-line-specific DNA. We report on a cDNA clone that codes for a putative ribosomal protein (ALEP-1, for A. lumbricoides eliminated protein 1). That the corresponding gene is located in the eliminated portion of the genome indicates a difference in germ-line and somatic ribosomes of A. lumbricoides and P. equorum. Elimination of the ALEP-1 gene from all somatic cells in its fully active state may represent an alternative way to gene regulation.It is generally believed that development and differentiation of a multicellular organism are based on regulation of a constant genome in the different cell types rather than on qualitative or quantitative changes in the genetic content. Chromatin diminution in Parascaris equorum and Ascaris lumbricoides represents the classic exception to this socalled DNA constancy rule. In both nematodes, this phenomenon is correlated with the separation of the germ line from the somatic cell lines. Chromatin diminution was discovered by T. Boveri in P. equorum more than 100 years ago and provided the first direct proof for the early segregation and independent development of the germ line and the somatic cell lines (1). This segregation was predicted by A. Weismann in his famous germ-line theory established in 1885 (2). During the process of chromatin diminution, about 25% (A. lumbricoides) or 80-90% (P. equorum) of the germ-line DNA-mostly satellite DNA, but also some middlerepetitive and single-copy DNA sequences-is expelled from the presomatic cells (3)(4)(5)(6)(7). Earlier studies did not reveal any evidence for the elimination of genetically active material (3,8). In this paper we show that the germ-line-specific material of A. lumbricoides contains coding potential. We present a cDNA clone that codes for a putative ribosomal protein and demonstrate that the corresponding gene is lost from the somatic cell lines.* This finding opens new aspects concerning the possible biological function of the chromatin elimination process. MATERIALS AND METHODSGrowth of Ascaris and Nucleic Acid Preparation. Adult females were dissected and intestines, oocytes, and eggs were isolated. Eggs were incubated at 30°C in water containing 0.1% formaldehyde and the RNA was harvested at days 1, 4, and 11 of incubation. Genomic DNA and both total and poly(A)+ RNA were isolated by standard methods (5,9,10

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Eliminated chromatin of Ascaris contains a gene that encodes a putative ribosomal protein.

Etter

Aboutanos

Tobler

et al. 1991

Proc. Natl. Acad. Sci. U.S.A.

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“…The specificity of this intron's transposition has been shown to be a result of an endonuclease encoded by its 240-amino-acid ORF (10). It is interesting that a 4.5-kb element was found to interrupt a fraction of the 26S ribosomal genes of Ascaris lumbricoides (2). These elements are located 34 bp upstream of the insect Ri elements and are flanked by 13-bp duplications of target sequence.…”

Section: Methodsmentioning

confidence: 99%

The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons.

Xiong¹,

Eickbush²

1988

Mol. Cell. Biol.

133

125

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Two types of insertion elements, Ri and R2 (previously called type I and type II), are known to interrupt the 28S ribosomal genes of several insect species. In the silkmoth, Bombyx mori, each element occupies approximately 10% of the estimated 240 ribosomal DNA units, while at most only a few copies are located outside the ribosomal DNA units. We present here the complete nucleotide sequence of an RI insertion from B. mori (RlBm) Recently we determined the complete nucleotide sequence of the 4.2-kilobase (kb) R2 element of Bombyx mori (R2Bm). This analysis revealed the presence of a 1,151-amino-acid ORF. Because the central region of this ORF contains homology to reverse transcriptase-like enzymes, we suggested that the origin of R2 was that of a retrotransposon (7). We further suggested that if this element retains its ability to transpose, this could explain why insects are unable to rid their rDNA loci of these elements despite the ability of rDNA units to undergo sequence turnover by unequal crossovers.In this paper we report the nucleotide sequence of a complete 5.1-kb Rl insertion element from B. mori (RlBm) (Fig. 1B). From a detailed restriction map 114 on May 12, 2018 by guest

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“…In Ascaris lumbricoides, a 4.5-kb element interrupts a small fraction of the 26S rRNA genes at a position which corresponds to 34 bp upstream of the insect Ri element (2). Like the Ri element of insects, the Ascaris element is flanked by a 14-bp duplication of rDNA sequences.…”

mentioning

confidence: 99%

The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme.

Burke¹,

Calalang²,

Eickbush³

1987

Mol. Cell. Biol.

129

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Two classes of DNA elements interrupt a fraction of the rRNA repeats of Bombyx mon. We have analyzed by genomic blotting and sequence analysis one class of these elements which we have named R2. These elements occupy approximately 9% of the rDNA units of B. mon and appear to be homologous to the type II rDNA insertions detected in Drosophila melanogaster. Approximately 25 copies of R2 exist within the B. mori genome, of which at least 20 are located at a precise location within otherwise typical rDNA units. Nucleotide sequence analysis has revealed that the 4.2-kilobase-pair R2 element has a single large open reading frame, occupying over 82% of the total length of the element. The central region of this 1,151-amino-acid open reading frame shows homology to the reverse transcriptase enzymes found in retroviruses and certain transposable elements. Amino acid homology of this region is highest to the mobile line 1 elements of mammals, followed by the mitochondrial type II introns of fungi, and the pol gene of retroviruses. Less homology exists with transposable elements of D. melanogaster and Saccharomyces cerevisiae. Two additional regions of sequence homology between LI and R2 elements were also found outside the reverse transcriptase region. We suggest that the R2 elements are retrotransposons that are site specific in their insertion into the genome. Such mobility would enable these elements to occupy a small fraction of the rDNA units of B. mori despite their continual elimination from the rDNA locus by sequence turnover.A fraction of the 28S ribosomal genes in several insect species is interrupted by segments of non-rDNA approximately 5 kilobases (kb) in length (see the review by Beckingham [3]). Based on the nucleotide sequences of their junction regions, these insertions have been divided into two classes. Type I elements have been reported in Drosophila virilis (34), D. melanogaster (7, 37), Calliphora erythrocephala (43), and Bombyx mori (12,16). They interrupt the 28S rRNA gene at a location approximately two-thirds of the distance from the 5' end of the gene and are flanked by a 14-base-pair (bp) duplication of rDNA sequences. Type II elements have only been reported in D. melanogaster (7,37) and B. mori (12,16). They interrupt the 28S gene 75 bp upstream of the type I elements and do not contain flanking duplications of rDNA sequences. In D. melanogaster, rDNA units containing either of these elements are transcribed at a significantly lower level than are the remaining rDNA units (20,23,28). To be consistent with the singleletter nomenclature frequently used to describe repetitive or transposable DNA elements and to avoid possible confusion with the type I and II intron sequences of fungal mitochondrial DNAs, we suggest that these elements be referred to as the Ri (type I) and R2 (type II) elements (R referring to rDNA units).Disruption of the large rRNA genes has also been detected in noninsect species. In Ascaris lumbricoides, a 4.5-kb element interrupts a small fraction of the 26S rRNA genes at ...

show abstract

Intervening sequences in the ribosomal RNA genes of Ascaris lumbricoides: DNA sequences at junctions and genomic organization.

Cited by 23 publications

References 32 publications

Eliminated chromatin of Ascaris contains a gene that encodes a putative ribosomal protein.

Eliminated chromatin of Ascaris contains a gene that encodes a putative ribosomal protein.

The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons.

The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme.

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