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Cerevls Ae RNA14 Suggests That Melanogaster by Suppressor Of Downloaded from genesdev.cshlp.org on September 25, 2021 - Published by Cold Spring Harbor Laboratory Press Homology with Saccharomyces cerevls ae RNA14 suggests that phenotypic suppression in Drosophila melanogaster by suppressor of f. o.rked occurs at the level of RNA stabd ty Andrew Mitchelson, Martine Simonelig, 1 Carol Williams, and Kevin O'Hare 2 Department of Biochemistry, Imperial College of Science Technology and Medicine, London SW7 2AZ, UK The suppressor of forked [su(f)] locus of Drosophila melanogaster encodes at least one cell-autonomous vital function. Mutations at su(f) can affect the expression of unlinked genes where retroviral-like transposable elements are inserted. Changes in phenotype are correlated with changes in mRNA profiles, indicating that su(f) affects the production and/or stability of mRNAs. We have cloned the su(f) gene by P-element transposon tagging. Alterations in the DNA map of eight lethal alleles were detected in a 4.3-kb region. P-element- mediated transformation using a fragment including this interval rescued all aspects of the su(f) mutant phenotype. The gene is transcribed to produce a major 2.6-kb RNA and minor RNAs of 1.3 and 2.9 kb, which are present throughout development, being most abundant in embryos, pupae, and adult females. The major predicted gene product is an 84- kD protein that is homologous to RNA14 of Saccharomyces cerevisiae, a vital gene where mutation affects mRNA stability. This suggests that phenotypic modification by su(f) occurs at the level of RNA stability. [Key Words: Drosophila; modifier gene; transposable element; suppression] Received October 12, 1992; accepted November 23, 1992. Mutations at the suppressor of forked locus [su(f)] lead to can be detected, and the flies have defective bristles. alterations of the phenotypes associated with mutations Lack of either su(Hw) or su(f) products results in sup- at unlinked genes. Phenotypes may be made more mu- pression of the mutant bristle phenotype and accumula- tant {enhanced) or less mutant {suppressed). The su(f) tion of apparently wild-type f RNAs. gene is one of several Drosophila modifier genes, includ- Genetic studies have shown that the different suppres- ing the suppressor of Hairy wing [su(Hw)], suppressor of sor genes act independently, suggesting that they inter- sable [su(s)], suppressor of white-apricot [su(w~)], and vene at different stages in the production of an mRNA suppressor of purple [su(pr)] loci. Mutations of these (Rutledge et al. 1988}. Steps where suppressor genes modifier genes affect the phenotypes of at least 35 mu- might act include transcription, splicing, polyadenyla- tant alleles of 17 different loci (Rutledge et al. 1988; tion, and RNA stability. Several suppressor genes have Lindsley and Zimm 1992). been cloned, and their putative gene products are consis- Alleles that respond to these trans-acting modifiers tent with this hypothesis. The su(Hw) gene was sug- have retroviral-like transposable elements inserted in gested to encode an activator of gypsy transcription noncoding regions of the genes. The insertions either (Parkhurst and Corces 19861, and the gene product has eliminate or alter the pattern of transcription, resulting multiple zinc finger motifs like those found in other in a mutant phenotype. Mutation of the modifier gene DNA-binding proteins {Parkhurst et al. 1988). Analysis appears to modulate further the pattern of RNA pro- of su(w ~) showed that it affected its own RNA splicing duced and so suppress or enhance the mutant phenotype. pattern {Zachar et al. 1987), and the gene product has For example, in forked 1 (fl) a gypsy element is inserted arginine/serine-rich motifs similar to those found in within an intron of the forked (f) gene (Parkhurst and other RNA splicing proteins (Li and Bingham 1991). The Corces 1985; McLachlan 1986). No stable f transcripts su(s) gene also appears to affect splicing (Fridell et al. 1990), perhaps at the level of precursor RNA stability (Geyer et al. 1991). It encodes a nuclear protein similar to 1Present address: Dynamique du genome et evolution, Institut Jaques Monod, Universite Paris 7, 75005 Paris, France. RNA-binding proteins with ribonucleoprotein (RNP) 2Correspondingauthor. motifs (Voelker et al. 1991). GENES & DEVELOPMENT 7:241-249 91993 by Cold Sprin- HarborLaboratory Press ISSN 0890-9369/93 $3.00 241 Downloaded from genesdev.cshlp.org on September 25, 2021 - Published by Cold Spring Harbor Laboratory Press Mitchelson et al. Most su(f) alleles are lethal, consistent with there be- in the original mutant stocks was then substantially re- ing an important role for the gene product. Of the viable duced by substituting the autosomes and recombining alleles, four are temperature-sensitive lethals (Dudick et away the distal portion of the X chromosome. Several al. 1974; Russell 1974; J/irgens and Gateff 1979; Wilson independent recombinant sublines were then analyzed 1980). They have similar periods of temperature-sensi- by DNA blotting, and the one with the fewest remaining tive lethality from late first-instar larvae to just after P elements, a subline of su(f) 28, was used as a source of puparium formation. Analysis of somatic clones has DNA to construct genomic libraries in k vectors. Phage shown that the lethal phenotype is cell autonomous. with homology to the P element were purified and sorted The su(f) gene therefore encodes a vital cell-autonomous into groups corresponding to sites where a P element is function, and we presume that this function is related to inserted in this particular su(f) 28 subline. Flanking the phenotypic suppression of some mutations caused by probes were then used in DNA blotting experiments to insertion of transposable elements. We undertook the identify the element associated with the lethal pheno- cloning of the su(f) gene as a vital cell-autonomous gene type of su(f) 28. Figure 1A shows that the B1 group P el- the role of which is likely to be in mRNA production or ement is absent in six independent revertants of su(f) 28. stability. In contrast, hybridization of the same filter to a probe flanking the $7 P element (Fig. 1B) showed that it was present in both mutants and revertants. Analysis of Results DNA from su(f) 27 flies showed that this allele also has an insertion in the region where the B 1 group P element is Cloning of DNA sequences from su(f) inserted (see Fig. 4, below) and that this insertion was The su(f) gene is the most proximal single-copy gene in absent in revertants of su(f) 2z. Subsequent cloning exper- the map of the X chromosome (Schalet and Lefevre iments confirmed that the insertion detected in su(f) 2z is 1973). It is within the euchromatin-heterochromatin a P element (see below). transition region at the base of the X. It has proved dif- Sequences flanking the B 1 group P element were used ficult, or impossible, to clone genes from this region by to screen a Sau3AI partial digest library of wild-type chromosomal walking because there are large blocks of (Canton-S) DNA (Mariani et al. 1985). Figure 2 shows a repeated sequences (Miklos et al. 1984, 1988). We there- restriction map of the 33 kb isolated and the site of in- fore cloned DNA sequences from su(f) by P-element sertion of the P element in su(f) 28. The SalI site 150 bp to transposon tagging. A collection of 110 lethal mutations the left of the insertion site was designated coordinate induced on the X chromosome by PM hybrid dysgenesis 0.0. On the basis of the mapping of breakpoints associ- (M. Simmons, University of Minnesota, St. Paul) was ated with chromosomal rearrangements (L. Kelly, pets. screened for su(f) mutants. Two stocks, 1(1)M897 and comm.; A. Mitchelson, M. Simonelig, C. Williams, and 1(1)MS252, were found to complement a temperature- K. O'Hare, unpubl.), we have drawn the DNA maps so sensitive lethal su(f) mutant at the permissive tempera- that left to right is distal to proximal (- to +) with ture but not at the restrictive temperature. respect to the centromere. DNA blotting experiments To ensure that these stocks had bona fide P-element have revealed the presence of appreciable amounts of insertion mutations of su(f), they were tested for rever- repetitive DNA in the cloned interval (data not shown); sion during hybrid dysgenesis. Both I(1)MS97 and the approximate extent of repetitive sequences is shown 1(1)MS252 gave viable revertants at rates between 3 x in Figure 2. An analysis of the repetitive DNA sequences 10 -3 and 7 x 10 -3 and have been designated su(f) 27 and in the su(f) region will be presented elsewhere (M. Tudor, su(f) 28, respectively. The number of P elements present A. Mitchelson, and K. O'Hare, in prep.). Figure 1. Identification of the P element responsible for su(f) 28. {A) DNA samples were digested with BamHI and SalI and probed with pB1 .L, a fragment flanking the B1 group P element. In flies heterozygous for su(f) 28, a second band larger than wild type is present; in each revertant line, only the wild-type band is seen. DNA samples: (Lane 1) Canton-S; {lane 2) FM6; (lane 31 su(f)28/FM6; (lane 4} subline 1 of su(f)28/ FM6; (lanes 5-7) three independent viable revertants of subline 1; (lane 8) subline 2 of su(f)28/FM6; (lanes 9-11) three indepen- dent viable revertants of subline 2. (B) The same filter probed with pS7.SR; a fragment flanking the $7 group P element. In each revertant line, the $7 P element is re- tained.
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