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

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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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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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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P-Element Repression in Drosophila melanogaster by a Naturally Occurring Defective Telomeric P Copy

Genetics ◽

10.1093/genetics/155.4.1841 ◽

2000 ◽

Vol 155 (4) ◽

pp. 1841-1854 ◽

Cited By ~ 12

Author(s):

Laurent Marin ◽

Monique Lehmann ◽

Danielle Nouaud ◽

Hassan Izaabel ◽

Dominique Anxolabéhère ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Hybrid Dysgenesis ◽

P Element ◽

Tunisian Population ◽

P Elements ◽

Naturally Occurring ◽

Dependent Component ◽

Associated Sequences ◽

Element Sequence

Abstract In Drosophila melanogaster, hybrid dysgenesis occurs in progeny from crosses between females lacking P elements and males carrying P elements scattered throughout the genome. We have genetically isolated a naturally occurring P insertion at cytological location 1A, from a Tunisian population. The Nasr'Allah-P(1A) element [NA-P(1A)] has a deletion of the first 871 bp including the P promoter. It is flanked at the 3′ end by telomeric associated sequences and at the 5′ end by a HeT-A element sequence. The NA-P(1A) element strongly represses dysgenic sterility and P transposition. However, when testing P-promoter repression, NA-P(1A) was unable to repress a germinally expressed P-lacZ construct bearing no 5′-homology with it. Conversely, a second P-lacZ construct, in which the fusion with lacZ takes place in exon 3 of P, was successfully repressed by NA-P(1A). This suggests that NA-P(1A) repression involves a homology-dependent component.

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A particular P-element insertion is correlated to the P-induced hybrid dysgenesis repression in Drosophila melanogaster

Genetics Research ◽

10.1017/s0016672300030627 ◽

1992 ◽

Vol 60 (1) ◽

pp. 15-24 ◽

Cited By ~ 5

Author(s):

Dominique Higuet ◽

Dominique Anxolabéhére ◽

Danielle Nouaud

Keyword(s):

Drosophila Melanogaster ◽

Promoter Activity ◽

Hybrid Dysgenesis ◽

P Element ◽

P Elements ◽

Element Insertion ◽

Element Number

SummaryTransposable P elements in Drosophila melanogaster cause hybrid dysgenesis if their mobility is not repressed. The ability to regulate the dysgenic activity of the P elements depends on several mechanisms, one of which hypothesized that a particular deleted P element (the KP element) results in a non-susceptibility which is biparentally transmitted. In this study totally nonsusceptible lines, and susceptible lines containing exclusively KP elements (IINS2 line and IIS2 line) were isolated from a M' strain. We show that non-susceptibility is correlated with a particular insertion of one KP element located at the cytological site 47D1. The repression ability of the GD sterility is determined by a recessive chromosomal factor, and cannot be due to the KP-element number. Here the repression of the P mobility is associated with reduction of the P transcripts and the inhibition of P promoter activity.

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Repression of P element-mediated hybrid dysgenesis in Drosophila melanogaster.

Genetics ◽

10.1093/genetics/124.3.663 ◽

1990 ◽

Vol 124 (3) ◽

pp. 663-676 ◽

Cited By ~ 2

Author(s):

M J Simmons ◽

J D Raymond ◽

K E Rasmusson ◽

L M Miller ◽

C F McLarnon ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Maternal Effect ◽

Gonadal Dysgenesis ◽

De Novo ◽

Inbred Lines ◽

Hybrid Dysgenesis ◽

P Element ◽

P Elements ◽

Hybrid Offspring ◽

Element Movement

Abstract Inbred lines derived from a strain called Sexi were analyzed for their abilities to repress P element-mediated gonadal dysgenesis. One line had high repression ability, four had intermediate ability and two had very low ability. The four intermediate lines also exhibited considerable within-line variation for this trait; furthermore, in at least two cases, this variation could not be attributed to recurring P element movement. Repression of gonadal dysgenesis in the hybrid offspring of all seven lines was due primarily to a maternal effect; there was no evidence for repression arising de novo in the hybrids themselves. In one of the lines, repression ability was inherited maternally, indicating the involvement of cytoplasmic factors. In three other lines, repression ability appeared to be determined by partially dominant or additive chromosomal factors; however, there was also evidence for a maternal effect that reduced the expression of these factors in at least two of the lines. In another line, repression ability seemed to be due to recessive chromosomal factors. All seven lines possessed numerous copies of a particular P element, called KP, which has been hypothesized to produce a polypeptide repressor of gonadal dysgenesis. This hypothesis, however, does not explain why the inbred Sexi lines varied so much in their repression abilities. It is suggested that some of this variation may be due to differences in the chromosomal position of the KP elements, or that other nonautonomous P elements are involved in the repression of hybrid dysgenesis in these lines.

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Natural Repressors of P-induced hybrid dysgenesis in Drosophila melanogaster: a model for repressor evolution

Genetics Research ◽

10.1017/s0016672300033577 ◽

1996 ◽

Vol 67 (2) ◽

pp. 109-121 ◽

Cited By ~ 11

Author(s):

P. Corish ◽

D. M. Black ◽

D. W. Featherston ◽

J. Merriam ◽

G. A. Dover

Keyword(s):

Drosophila Melanogaster ◽

Selective Advantage ◽

Hybrid Dysgenesis ◽

P Element ◽

Type I ◽

Sensitive Assay ◽

Stable Strategy ◽

Naturally Occurring ◽

Constitutive Production ◽

Repressor Element

SummaryType I repressors control P element transposition and comprise full length elements and elements with small 3′ deletions in the final exon. Using a sensitive assay for measuring the strength of repression of P element transposition in somatic and germline tissues, we have isolated and characterized a naturally occurring type I repressor element from a Q population of Drosophila melanogaster. We demonstrate that the almost complete repression of transposition in this population is a mixture of KP elements with intermediate levels of repression, and the strong contribution of a single 2·6 kb P element deletion derivative, which we call SR (Strong Repressor). A deletion in the final intron of SR allows for the constitutive production of a putative 75 kDa repressor protein in germline tissues in addition to the production of the 66 kDa repressor in the soma, which would result in a biparental mode of inheritance of repression. Basedon the four observed classes of natural Q populations, we propose a model in which populations containing SR-like elements, capable of producing strong type I repressor constitutively, have a selective advantage over populations which rely either on maternally transmitted P cytotype or on KPinduced weak levels of repression. Such populations may subsequently spread and constitute an evolutionary stable strategy for the repression of hybrid dysgenesis in Drosophila melanogaster.

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Hybrid dysgenesis in Drosophila simulans associated with a rapid global invasion of the P-element

10.1101/031781 ◽

2015 ◽

Cited By ~ 1

Author(s):

Tom Hill ◽

Christian Schlotterer ◽

Andrea J Betancourt

Keyword(s):

Drosophila Melanogaster ◽

Related Species ◽

Hybrid Dysgenesis ◽

P Element ◽

Genetic Element ◽

P Elements ◽

Transcriptomic Data ◽

Selfish Genetic Element ◽

Element Free ◽

Global Invasion

In a classic example of the invasion of a species by a selfish genetic element, the P-element was horizontally transferred from a distantly related species into Drosophila melanogaster. Despite causing 'hybrid dysgenesis', a syndrome of abnormal phenotypes that include sterility, the P-element spread globally in the course of a few decades in D. melanogaster. Until recently, its sister species, including D. simulans, remained P-element free. Here, we find a hybrid dysgenesis-like phenotype in the offspring of crosses between D. simulans strains collected in different years; a survey of 181 strains shows that around 20% of strains induce hybrid dysgenesis. Using genomic and transcriptomic data, we show that this dysgenesis-inducing phenotype is associated with the invasion of the P-element. To characterize this invasion temporally and geographically, we survey 631 D. simulans strains collected on three continents and over 27 years for the presence of the P-element. We find that the D. simulans P-element invasion occurred rapidly and nearly simultaneously in the regions surveyed, with strains containing P-elements being rare in 2006 and common by 2014. Importantly, as evidenced by their resistance to the hybrid dysgenesis phenotype, strains collected from the latter phase of this invasion have adapted to suppress the worst effects of the P-element.

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P element insertions and rearrangements at the singed locus of Drosophila melanogaster.

Genetics ◽

10.1093/genetics/119.1.75 ◽

1988 ◽

Vol 119 (1) ◽

pp. 75-83

Author(s):

H Roiha ◽

G M Rubin ◽

K O'Hare

Keyword(s):

Drosophila Melanogaster ◽

High Frequency ◽

The Other ◽

Hybrid Dysgenesis ◽

P Element ◽

Wild Type ◽

Tandem Arrangement ◽

P Elements

Abstract DNA from the singed gene of Drosophila melanogaster was isolated using an inversion between a previously cloned P element at cytological location 17C and the hypermutable allele singed-weak. Five out of nine singed mutants examined have alterations in their DNA maps in this region. The singed locus is a hotspot for mutation during P-M hybrid dysgenesis, and we have analyzed 22 mutations induced by P-M hybrid dysgenesis. All 22 have a P element inserted within a 700-bp region. The precise positions of 10 P element insertions were determined and they define 4 sites within a 100-bp interval. During P-M hybrid dysgenesis, the singed-weak allele is destabilized, producing two classes of phenotypically altered derivatives at high frequency. In singed-weak, two defective P elements are present in a "head-to-head" or inverse tandem arrangement. Excision of one element results in a more extreme singed bristle phenotype while excision of the other leads to a wild-type bristle phenotype.

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Regulation of P-Element Transposase Activity in Drosophila melanogaster by hobo Transgenes That Contain KP Elements

Genetics ◽

10.1093/genetics/161.1.205 ◽

2002 ◽

Vol 161 (1) ◽

pp. 205-215 ◽

Cited By ~ 1

Author(s):

Michael J Simmons ◽

Kevin J Haley ◽

Craig D Grimes ◽

John D Raymond ◽

Joseph C L Fong

Keyword(s):

Drosophila Melanogaster ◽

P Element ◽

Drosophila Genome ◽

Maternal Transmission ◽

Alternate Splicing ◽

Hsp70 Promoter ◽

P Elements ◽

Naturally Occurring ◽

Element Activity ◽

Transformation Vectors

Abstract Fusions between the Drosophila hsp70 promoter and three different incomplete P elements, KP, SP, and BP1, were inserted into the Drosophila genome by means of hobo transformation vectors and the resulting transgenic stocks were tested for repression of P-element transposase activity. Only the H(hsp/KP) transgenes repressed transposase activity, and the degree of repression was comparable to that of a naturally occurring KP element. The KP transgenes repressed transposase activity both with and without heat-shock treatments. Both the KP element and H(hsp/KP) transgenes repressed the transposase activity encoded by the modified P element in the P(ry+, Δ2-3)99B transgene more effectively than that encoded by the complete P element in the H(hsp/CP)2 transgene even though the P(ry+, Δ2-3)99B transgene was the stronger transposase source. Repression of both transposase sources appeared to be due to a zygotic effect of the KP element or transgene. There was no evidence for repression by a strictly maternal effect; nor was there any evidence for enhancement of KP repression by the joint maternal transmission of H(hsp/KP) and H(hsp/CP) transgenes. These results are consistent with the idea that KP-mediated repression of P-element activity involves a KP-repressor polypeptide that is not maternally transmitted and that KP-mediated repression is not strengthened by the 66-kD repressor produced by complete P elements through alternate splicing of their RNA.

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Hybrid dysgenesis in Drosophila melanogaster: the elimination of P elements through repeated backcrossing to an M-type strain

Genome ◽

10.1139/g87-033 ◽

1987 ◽

Vol 29 (1) ◽

pp. 195-200 ◽

Cited By ~ 2

Author(s):

Allen G. Good ◽

Donal A. Hickey

Keyword(s):

Drosophila Melanogaster ◽

Dna Hybridization ◽

Copy Number ◽

Natural Populations ◽

Hybrid Dysgenesis ◽

P Element ◽

P Elements ◽

Element Activity ◽

Equivalent Reduction ◽

Replicative Transposition

The rapid increase in the frequency of P elements in natural populations of Drosophila melanogaster has led to the suggestion that these elements can spread in nature through replicative transposition. In an attempt to model the introduction of a small number of P flies into an M population we backcrossed P flies and their offspring to M flies. Two components of dysgenesis, P element activity and P element copy number (measured by DNA hybridization), were monitored each generation. In these experiments P elements were not capable of spreading rapidly enough to maintain 30–50 copies per fly and were rapidly lost from the population. We also found that the reduction in a fly's ability to induce gonadal dysgenesis was matched by an equivalent reduction in P element copy number as measured by DNA hybridization. These results are discussed in terms of the conventional mechanisms of selection or segregation; the conclusion is that there are conditions under which P elements can be lost from a population. Key words: hybrid dysgenesis, P element, transposable elements, Drosophila.

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