P element regulation and X-chromosome subtelomeric heterochromatin in Drosophila melanogaster

Abstract In Drosophila, clusters of P transgenes (P-lac-w) display a variegating phenotype for the w marker. In addition, X-ray-induced rearrangements of chromosomes bearing such clusters may lead to enhancement of the variegated phenotype. Since P-lacZ transgenes in subtelomeric heterochromatin have some P-element repression abilities, we tested whether P-lac-w clusters also have the capacity to repress P-element activity in the germline. One cluster (T-1), located on a rearranged chromosome (T2;3) and derived from a line bearing a variegating tandem array of seven P-lac-w elements, partially represses the dysgenic sterility (GD sterility) induced by P elements. This cluster also strongly represses in trans the expression of P-lacZ elements in the germline. This latter suppression shows a maternal effect. Finally, the combination of variegating P-lac-w clusters and a single P-lacZ reporter inserted in subtelomeric heterochromatic sequences at the X chromosome telomere (cytological site 1A) leads to strong repression of dysgenic sterility. These results show that repression of P-induced dysgenic sterility can be elicited in the absence of P elements encoding a polypeptide repressor and that a transgene cluster can repress the expression of a single homologous transgene at a nonallelic position. Implications for models of transposable element silencing are discussed.

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Genetic and molecular analysis of repression in the P–M system of hybrid dysgenesis in Drosophila melanogaster

Genetics Research ◽

10.1017/s0016672300029360 ◽

1991 ◽

Vol 57 (3) ◽

pp. 213-226 ◽

Cited By ~ 8

Author(s):

Ellen M. Heath ◽

Michael J. Simmons

Keyword(s):

Drosophila Melanogaster ◽

Maternal Effects ◽

X Chromosome ◽

Gonadal Dysgenesis ◽

Inbred Lines ◽

Hybrid Dysgenesis ◽

P Element ◽

P Elements ◽

Two Generations ◽

Highly Correlated

SummaryTwelve inbred lines derived from an M′ strain of Drosophila melanogaster were used to study the repression of P-element-mediated hybrid dysgenesis. Initial assessments indicated that the lines differed in the ability to repress gonadal dysgenesis, and that this ability was highly correlated with the ability to repress snw hypermutability. Later assessments indicated that most of the lines with low or intermediate repression potential evolved to a state of higher repression potential; however, Southern analyses failed to reveal significant changes in the array of genomic P elements that could account for this evolution. In addition, none of the lines possessed the incomplete P element known as KP, which has been proposed to explain repression in some D. melanogaster strains. One of the lines maintained intermediate repression potential throughout the period of study (52 generations), indicating that the intermediate condition was not intrinsically unstable. Genetic analyses demonstrated that in some of the lines, repression potential was influenced by factors that were inherited maternally through at least two generations; however, these factors were not as influential as those in a classic P cytotype strain. Additional tests with a dysgenesis-inducing X chromosome called T-5 indicated that repression itself was mediated by a combination of maternal effects and paternally inherited factors that were expressed after fertilization. These tests also suggested that in some circumstances, the P transposase, or its message, might be transmitted through the maternal cytoplasm.

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Construction of an Unstable Ring-X Chromosome Bearing the Autosomal Dopa Decarboxylase Gene in Drosophila melanogaster and Analysis of Ddc Mosaics

Genetics ◽

10.1093/genetics/115.2.305 ◽

1987 ◽

Vol 115 (2) ◽

pp. 305-311

Author(s):

Donald A Gailey ◽

Deborah L Bordne ◽

Ana Maria Vallés ◽

Jeffrey C Hall ◽

Kalpana White

Keyword(s):

Nervous System ◽

Drosophila Melanogaster ◽

X Chromosome ◽

Recombination Event ◽

P Element ◽

Dopa Decarboxylase ◽

Somatic Instability ◽

Absolute Requirement ◽

Double Recombination ◽

Double Recombination Event

ABSTRACT An unstable Ring-X chromosome, Ddc +- Ring-X carrying a cloned Dopa decarboxylase (Ddc) encoding segment was constructed. The construction involved a double recombination event between the unstable Ring-X, R(1)wvC and a Rod-X chromosome which contained a P-element mediated Ddc + insert. The resulting Ddc +-Ring-X chromosome behaves similarly to the parent chromosome with respect to somatic instability. The Ddc +-Ring-X chromosome was used to generate Ddc mosaics. Analyses of Ddc mosaics revealed that while there was no absolute requirement for the Ddc + expression in either the epidermis or the nervous system, very large mutant clones did affect the viability of the mosaic.

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Repression of Hybrid Dysgenesis in Drosophila melanogaster by Combinations of Telomeric P-Element Reporters and Naturally Occurring P Elements

Genetics ◽

10.1093/genetics/149.4.1857 ◽

1998 ◽

Vol 149 (4) ◽

pp. 1857-1866 ◽

Cited By ~ 11

Author(s):

Stéphane Ronsseray ◽

Laurent Marin ◽

Monique Lehmann ◽

Dominique Anxolabéhère

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

Chromatin Structure ◽

Hybrid Dysgenesis ◽

P Element ◽

Pericentromeric Heterochromatin ◽

Combination Effect ◽

P Elements ◽

Naturally Occurring ◽

Nuclear Location

Abstract In Drosophila melanogaster, hybrid dysgenesis occurs in the germline of flies produced by crosses between females lacking P elements and males carrying 25–55 P elements. We have previously shown that a complete maternally inherited repression of P transposition in the germline (P cytotype) can be elicited by only two autonomous P elements located at the X chromosome telomere (cytological site 1A). We have tested whether P transgenes at 1A, unable to code for a P-repressor, may contribute to the repression of P elements. Females carrying a P-lacZ transgene at 1A [“P-lacZ(1A)”], crossed with P males, do not repress dysgenic sterility in their progeny. However, these P-lacZ(1A) insertions, maternally or paternally inherited, contribute to P-element repression when they are combined with other regulatory P elements. This combination effect is not seen when the P-lacZ transgene is located in pericentromeric heterochromatin or in euchromatin; however a P-w,ry transgene located at the 3R chromosome telomere exhibits the combination effect. The combination effect with the P-lacZ(1A) transgene is impaired by a mutant Su(var)205 allele known to impair the repression ability of the autonomous P elements at 1A. We hypothesized that the combination effect is due to modification of the chromatin structure or nuclear location of genomic P elements.

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The maternally inherited regulation of P elements in Drosophila melanogaster can be elicited by two P copies at cytological site 1A on the X chromosome.

Genetics ◽

10.1093/genetics/129.2.501 ◽

1991 ◽

Vol 129 (2) ◽

pp. 501-512 ◽

Cited By ~ 5

Author(s):

S Ronsseray ◽

M Lehmann ◽

D Anxolabéhère

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

P Element ◽

P Elements ◽

Element Activity ◽

High Level ◽

Regulatory Properties ◽

Cellular Condition

Abstract Two P elements, inserted at the cytological site 1A on an X chromosome from an Drosophila melanogaster natural population (Lerik, USSR), were isolated by genetic methods to determine if they are sufficient to cause the P cytotype, the cellular condition that regulates the P family of transposable element. The resulting "Lerik P(1A)" line (abbreviated "Lk-P(1A)") carries only one P element in situ hybridization site but genomic Southern analysis indicates that this site contains two, probably full length, P copies separated by at least one EcoRI cleavage site. Because the Lk-P(1A) line shows some transposase activity, at least one of these two P elements is autonomous. The Lk-P(1A) line fully represses germline P element activity as judged by the GD sterility and snw hypermutability assays; this result shows that the P cytotype can be elicited by only two P element copies. However, the Lk-P(1A) line does not fully repress delta 2-3(99B) transposase activity in the soma, although it fully represses delta 2-3(99B) transposase activity in the germline (delta 2-3(99B) is an in vitro modified P element that produces a high level of transposase activity in both the germline and the soma). The germline regulatory properties of the Lk-P(1A) line are maternally transmitted, even when the delta 2-3(99B) element is used as the source of transposase. By contrast, the partial regulation of delta 2-3(99B) somatic activity is chromosomally inherited. These results suggest that the regulatory P elements of the Lk-P(1A) line are inserted near a germline-specific enhancer.

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Evolutionary flux of P element regulation in a Drosophila melanogaster hybrid dysgenesis cline

Genetics Research ◽

10.1017/s0016672399003742 ◽

1999 ◽

Vol 73 (3) ◽

pp. 205-216 ◽

Cited By ~ 7

Author(s):

D. J. FRENCH ◽

P. CORISH ◽

M. SHI ◽

G. A. DOVER

Keyword(s):

Drosophila Melanogaster ◽

Evolutionarily Stable Strategy ◽

Hybrid Dysgenesis ◽

P Element ◽

Eastern Coast ◽

Type I ◽

The South ◽

The North ◽

Evolutionarily Stable ◽

P Element Regulation

Clines of P-induced hybrid dysgenesis provide a means for monitoring the evolution of transposition repression over space and time. We have studied the molecular and phenotypic profiles of flies taken from a 2900 km cline along the eastern coast of Australia, which had previously been characterized over 10 years ago as having P populations in the north, Q populations at central sites and M′ populations in the south. We have found that Q and M′ populations of flies have increased their range within the cline at the expense of P lines. Q populations were found to be in the north of the cline and M′ populations in the south. Some of the northern Q lines transmit repression through both sexes and type I deletion elements have been isolated from them. We suggest that these elements are responsible for Q type repression. The results support our model that populations made up of Q individuals with strong biparentally transmitted repression form an evolutionarily stable strategy for the repression of hybrid dysgenesis in Drosophila melanogaster.

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The accumulation of P-elements on the tip of the X chromosome in populations of Drosophila melanogaster

Genetics Research ◽

10.1017/s0016672300027798 ◽

1989 ◽

Vol 53 (1) ◽

pp. 1-6 ◽

Cited By ~ 27

Author(s):

James W. Ajioka ◽

Walter F. Eanes

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

De Novo ◽

Natural Populations ◽

Mobile Elements ◽

P Element ◽

P Elements ◽

High Occurrence ◽

Elevated Rate

SummaryLittle information exists about the mechanisms that determine the fate of mobile elements in natural populations. In this study we catalogue the distribution of 638 P-elements across 114 X chromosomes in samples drawn from three natural populations of Drosophila melanogaster. There is an extremely high occurrence of elements at the tip relative to the rest of the euchromatic chromosome. We demonstrate that the distribution of de novo insertions of the P-element on a specific laboratory chromosome is markedly different; no P-elements were recovered at the tip in the 243 insertion events recorded. In contrast, insertion data for the π2 chromosome suggests an elevated rate associated with the tip site although it does not appear sufficient to explain the large differential accumulation on wild chromosomes. This raises the issue of inter chromosome (or tip) variation in relative rates, as well as the possibility that rates of elimination are lower at the tip.

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A COMPARISON OF MUTATION RATES FOR SPECIFIC LOCI AND CHROMOSOME REGIONS IN DYSGENIC HYBRID MALES OF DROSOPHILA MELANOGASTER

Genetics ◽

10.1093/genetics/106.1.85 ◽

1984 ◽

Vol 106 (1) ◽

pp. 85-94

Author(s):

Michael J Simmons ◽

John D Raymond ◽

Nancy A Johnson ◽

Thomas M Fahey

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

The Other ◽

Hybrid Dysgenesis ◽

P Element ◽

Mutation Rates ◽

P Elements ◽

White Locus ◽

Insertion Mutations ◽

Chromosome Regions

ABSTRACT The mutation rates of specific loci and chromosome regions were estimated for two types of dysgenic hybrid males. These came from crosses between P or Q males and M females in the P-M system of hybrid dysgenesis. The M × P hybrids were the more mutable for each of the loci and chromosome regions tested. The Beadex locus was highly mutable in these hybrids but did not mutate at all in the sample of gametes from the M × Q hybrids. The singed locus had 75% of the mutability of Beadex in the M × P hybrids; it was also mutable in the M × Q hybrids. The white locus was only slightly mutable in the M × P hybrids and not at all mutable in the M × Q hybrids. The mutations in singed and white probably arose from the insertion of P elements into these loci; the mutations at Beadex probably involved the action of a P element located near this locus on the X chromosome of the P strain that was used in the experiments. Mutations in two chromosome regions, one including the zeste-white loci and the other near the miniature locus, were much more frequent in the M × P hybrids than in the M × Q hybrids. These mutations also probably arose from P element insertions. The implication is that insertion mutations occur infrequently in the M × Q hybrids, possibly because most of the P elements they carry are defective. In M × P hybrids, there is variation among loci with respect to P elements mutagenesis, indicating that P elements possess a degree of insertional specificity.

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Characterization of MR (P) strains of Drosophila melanogaster: the number of intact P elements and their genetic effect

Genetics Research ◽

10.1017/s0016672300029967 ◽

1991 ◽

Vol 58 (3) ◽

pp. 211-223 ◽

Cited By ~ 3

Author(s):

Jan C. J. Eeken ◽

Ron J. Romeyn ◽

Anja W. M. De Jong ◽

George Yannopoulos ◽

Albert Pastink

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

Genetic Effect ◽

P Element ◽

Insertion Mutagenesis ◽

P Elements ◽

Genetic Activity ◽

Carcinogenic Agents

SummaryTo study the effect of mutagenic/carcinogenic agents on P-element transposition, the P strains used should be denned, especially with respect to the number of intact and functional P elements present. In this investigation, the relation between the number of complete P elements present in dysgenic males and P-insertion mutagenesis was studied in several MR (P) strains. The main conclusions from this investigation are: (1) Complete P elements can be present in the genome without genetic activity (even in a ‘dysgenic’ cross). As a consequence, the number of complete P elements present in particular dysgenic flies, is not necessarily an indication of their dysgenic genetic activity. (2) The MR-h12/Cy strain carries two complete P elements, one on the X chromosome without and one on the MR chromosome with genetic activity (making this strain most suitable for studies on P-transposition mechanisms).

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A hobo Transgene That Encodes the P-Element Transposase in Drosophila melanogaster: Autoregulation and Cytotype Control of Transposase Activity

Genetics ◽

10.1093/genetics/161.1.195 ◽

2002 ◽

Vol 161 (1) ◽

pp. 195-204 ◽

Cited By ~ 1

Author(s):

Michael J Simmons ◽

Kevin J Haley ◽

Craig D Grimes ◽

John D Raymond ◽

Jarad B Niemi

Keyword(s):

Drosophila Melanogaster ◽

Gonadal Dysgenesis ◽

P Element ◽

Hsp70 Gene ◽

Alternate Splicing ◽

Male And Female ◽

P Elements ◽

Male Germline ◽

Female Germline ◽

Transposase Expression

Abstract Drosophila were genetically transformed with a hobo transgene that contains a terminally truncated but otherwise complete P element fused to the promoter from the Drosophila hsp70 gene. Insertions of this H(hsp/CP) transgene on either of the major autosomes produced the P transposase in both the male and female germlines, but not in the soma. Heat-shock treatments significantly increased transposase activity in the female germline; in the male germline, these treatments had little effect. The transposase activity of two insertions of the H(hsp/CP) transgene was not significantly greater than their separate activities, and one insertion of this transgene reduced the transposase activity of P(ry+, Δ2-3)99B, a stable P transgene, in the germline as well as in the soma. These observations suggest that, through alternate splicing, the H(hsp/CP) transgene produces a repressor that feeds back negatively to regulate transposase expression or function in both the somatic and germline tissues. The H(hsp/CP) transgenes are able to induce gonadal dysgenesis when the transposase they encode has P-element targets to attack. However, this ability and the ability to induce P-element excisions are repressed by the P cytotype, a chromosomal/cytoplasmic state that regulates P elements in the germline.

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