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

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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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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Cytotype regulation in Drosophila melanogaster: synergism between telomeric and non-telomeric P elements

Genetics Research ◽

10.1017/s0016672309990322 ◽

2009 ◽

Vol 91 (6) ◽

pp. 383-394 ◽

Cited By ~ 7

Author(s):

CARINA BELINCO ◽

STEPHANIE N. DIPRIMA ◽

RYAN E. WOLFF ◽

MICHAEL W. THORP ◽

JARED T. BUSCHETTE ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Maternal Effects ◽

Germ Line ◽

Molecular Level ◽

Hybrid Dysgenesis ◽

P Elements ◽

Two Generations

SummaryThe X-linked telomeric P elements TP5 and TP6 interact synergistically with non-telomeric P elements to repress hybrid dysgenesis. In this repression, the telomeric P elements exert maternal effects, which, however, are not sufficient to establish synergism with the non-telomeric P elements. Once synergism is established, the capacity to repress dysgenesis in the offspring of a cross persists for at least two generations after removing the telomeric P element from the genotype. At the molecular level, synergism between telomeric and non-telomeric P elements is correlated with effective elimination of P-element mRNA in the germ line. Maternally transmitted mutations in the genes aubergine, piwi and Suppressor of variegation 205 [Su(var)205] block the establishment of synergism between telomeric and non-telomeric P elements, and paternally transmitted mutations in piwi and Su(var)205 disrupt synergism that has already been established. These findings are discussed in terms of a model of cytotype regulation of P elements based on Piwi-interacting RNAs (piRNAs) that are amplified by cycling between sense and antisense species.

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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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STERILITY AND HYPERMUTABILITY IN THE P-M SYSTEM OF HYBRID DYSGENESIS IN DROSOPHILA MELANOGASTER

Genetics ◽

10.1093/genetics/114.4.1147 ◽

1986 ◽

Vol 114 (4) ◽

pp. 1147-1163

Author(s):

Gordon J Kocur ◽

Eric A Drier ◽

Michael J Simmons

Keyword(s):

Drosophila Melanogaster ◽

Gonadal Dysgenesis ◽

Hybrid Dysgenesis ◽

P Element ◽

Insertion Mutation ◽

Eastern United States ◽

X Chromosomes ◽

P Elements ◽

Y Chromosomes ◽

Wild Strains

ABSTRACT Inbred wild strains of Drosophila melanogaster derived from the central and eastern United States were used to make dysgenic hybrids in the P-M system. These strains possessed P elements and the P cytotype, the condition that represses P element transposition. Their hybrids were studied for the mutability of the P element insertion mutation, snw, and for the incidence of gonadal dysgenesis (GD) sterility. All the strains tested were able to induce hybrid dysgenesis by one or both of these assays; however, high levels of dysgenesis were rare. Sets of X chromosomes and autosomes from the inbred wild strains were more effective at inducing GD sterility than were sets of Y chromosomes and autosomes. In two separate analyses, GD sterility was positively correlated with snw mutability, suggesting a linear relationship. However, one strain appeared to induce too much GD sterility for its level of snw destabilization, indicating an uncoupling of these two manifestations of hybrid dysgenesis.

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Quantitative effects of P elements on hybrid dysgenesis in Drosophila melanogaster.

Genetics ◽

10.1093/genetics/124.3.647 ◽

1990 ◽

Vol 124 (3) ◽

pp. 647-662 ◽

Cited By ~ 1

Author(s):

K E Rasmusson ◽

M J Simmons ◽

J D Raymond ◽

C F McLarnon

Keyword(s):

Gonadal Dysgenesis ◽

Quantitative Relationship ◽

Inbred Lines ◽

Hybrid Dysgenesis ◽

P Element ◽

Insertion Mutation ◽

Simple Relationship ◽

P Elements ◽

A Cell ◽

Element Number

Abstract Genetic analyses involving chromosomes from seven inbred lines derived from a single M' strain were used to study the quantitative relationships between the incidence and severity of P-M hybrid dysgenesis and the number of genomic P elements. In four separate analyses, the mutability of snw, a P element-insertion mutation of the X-linked singed locus, was found to be inversely related to the number of autosomal P elements. Since snw mutability is caused by the action of the P transposase, this finding supports the hypothesis that genomic P elements titrate the transposase present within a cell. Other analyses demonstrated that autosomal transmission ratios were distorted by P element action. In these analyses, the amount of distortion against an autosome increased more or less linearly with the number of P elements carried by the autosome. Additional analyses showed that the magnitude of this distortion was reduced when a second P element-containing autosome was present in the genome. This reduction could adequately be explained by transposase titration; there was no evidence that it was due to repressor molecules binding to P elements and inhibiting their movement. The influence of genomic P elements on the incidence of gonadal dysgenesis was also investigated. Although no simple relationship between the number of P elements and the incidence of the trait could be discerned, it was clear that even a small number of elements could increase the incidence markedly. The failure to find a quantitative relationship between P element number and the incidence of gonadal dysgenesis probably reflects the complex etiology of this trait.

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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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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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A novel repressor of P element transposition in Drosophila melanogaster

Genetics Research ◽

10.1017/s0016672397003066 ◽

1998 ◽

Vol 71 (1) ◽

pp. 21-30 ◽

Cited By ~ 4

Author(s):

RICHARD M. BADGE ◽

JOHN F. Y. BROOKFIELD

Keyword(s):

Drosophila Melanogaster ◽

Inbred Line ◽

Gonadal Dysgenesis ◽

Full Length ◽

P Element ◽

Temperature Dependent ◽

P Elements

We have discovered, in an inbred line (Loua) of Drosophila melanogaster from Zaïre, a third chromosome showing unusual P element repression. Repression of P element transposition by this chromosome, named Loua3, is dominant zygotic and has three unusual properties. Firstly, its repression of the gonadal dysgenesis caused by a strong P haplotype is strongly temperature-dependent, being most evident at higher rearing temperatures. Secondly, subdivision of Loua3 by recombination abolishes repression: the effect is apparently a function of the intact chromosome. Finally, Loua3 also diminishes somatic lethality when chromosomes carrying many ‘ammunition’ elements (Birmingham2) are exposed to the constitutive transposase source Δ2-3(99B). The chromosome has 17 P elements, none full-length, located in at least 12 dispersed positions.

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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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Molecular analysis of the P-M gonadal dysgenesis cline in eastern Australian Drosophila melanogaster.

Genetics ◽

10.1093/genetics/119.4.889 ◽

1988 ◽

Vol 119 (4) ◽

pp. 889-902

Author(s):

I A Boussy ◽

M J Healy ◽

J G Oakeshott ◽

M G Kidwell

Keyword(s):

Drosophila Melanogaster ◽

Transposable Element ◽

Gonadal Dysgenesis ◽

Molecular Techniques ◽

P Element ◽

Latitudinal Cline ◽

Deletion Derivative ◽

P Elements ◽

Regulatory Ability ◽

Eastern Australia

Abstract The latitudinal cline in P-M gonadal dysgenesis potential in eastern Australia has been shown to comprise three regions which are, from north to south respectively, P, Q, and M, with the P-to-Q and Q-to-M transitions occurring over relatively short distances. The P element complements of 30 lines from different regions of the cline were determined by molecular techniques. The total amount of P element-hybridizing DNA was high in all lines, and it did not correlate in any obvious way with the P-M phenotypes of individual lines. The number of potentially full-sized P elements per genome was high in lines from the P regions, but variable or low among lines from the Q and M regions, and thus declined overall from north to south. A particular P element deletion-derivative, the KP element, occurred in all the tested lines. The number of KP elements was low in lines from the P region, much higher in lines from the Q region, and highest among lines from the M region, thus forming a cline reciprocal to that of the full-sized P elements. Another transposable element, hobo, which has been described as causing dysgenic traits similar to those of P-M hybrid dysgenesis, was shown to be present in all lines and to vary among them in number, but not in any latitudinal pattern. The P-M cline in gonadal dysgenesis potential can be inferred to be based on underlying clinal patterns of genomic P element complements. P activity of a line was positively correlated with the number of full-sized P elements in the line, and negatively correlated with the number of KP elements. Among Q and M lines, regulatory ability was not correlated with numbers of KP elements.

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