scholarly journals HYBRID DYSGENESIS IN DROSOPHILA MELANOGASTER: NATURE AND INHERITANCE OF P ELEMENT REGULATION

Genetics ◽  
1985 ◽  
Vol 111 (2) ◽  
pp. 337-350
Author(s):  
Margaret G Kidwell

ABSTRACT The genetic determination of the control of resistance or susceptibility to germ line changes mediated by P elements was studied in two strains and in derivatives of crosses between them. One strain, characterized as true M, completely lacked P elements. The second strain, pseudo-M (M'), carried a number of P elements, but these did not have the potential to induce the gonadal sterility that is associated with P-M hybrid dysgenesis. Individuals from the true M strain were invariably unable to suppress P factor activity (i.e., all daughters of outcrosses of M females and P males were sterile). In contrast, individuals from the M' strain showed variable degrees of suppression that were manifested in a wide range of gonadal sterility frequencies in standard tests. This continuous distribution pattern was reproducible for more than 25 generations.—The results of the genetic analysis indicate that a strain with a variable degree of suppression of gonadal dysgenesis is not necessarily in a transient state between the extreme conditions of P and M cytotype. A large variance in the ability to suppress gonadal dysgenesis with a mean value intermediate between the extremes of P and M cytotype may be a relatively stable strain characteristic. No reciprocal cross effect was observed in the suppression of sterility of F1 females from M × M' matings. Thus, the existence of M' strains indicates a Mendelian component in P element regulation and suggests that cytotype, which has an extrachromosomal aspect, may be only one of perhaps several mechanisms involved in regulation. Analysis of the effects of individual chromosomes from the M' strain showed that each chromosome contributed to the reduction of gonadal dysgenesis in the progeny of test matings. The results are consistent with a one-component titration model for P element regulation.

Genetics ◽  
1990 ◽  
Vol 124 (3) ◽  
pp. 663-676 ◽  
Author(s):  
M J Simmons ◽  
J D Raymond ◽  
K E Rasmusson ◽  
L M Miller ◽  
C F McLarnon ◽  
...  

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.


Genetics ◽  
1988 ◽  
Vol 119 (4) ◽  
pp. 815-828
Author(s):  
M G Kidwell ◽  
K Kimura ◽  
D M Black

Abstract P elements were introduced into M strain genomes by chromosomal contamination (transposition) from P strain chromosomes under conditions of P-M hybrid dysgenesis. A number of independently maintained contaminated lines were subsequently monitored for their ability to induce gonadal (GD) sterility in the progeny of reference crosses, over a period of 60 generations, in two experiments. The efficiency of chromosomal contamination was high; all tested lines acquired P elements following the association of M and P chromosomes in the same genome for a single generation. All the contaminated lines also sustained an initial unstable phase, marked by high frequencies of transposition and sterility within lines, in the absence of P element regulation. Subsequently, each of the lines rapidly evolved to one of three relatively stable strain types whose phenotypic and molecular properties correspond rather closely to those of the P, Q and M' strains that have previously been characterized. The numbers and structures of P elements and the presence or absence of P element regulation during the early generations appeared to be critical factors determining the subsequent course of evolution. On the basis of GD sterility frequencies, both the mean level of P activity, and the average capacity for P element regulation, were reduced in lines raised at 25 degrees, relative to those raised at 20 degrees, during the early generations. This latter result is consistent with the expectation that natural selection will tend to modify the manifestation of dysgenic traits, such as high temperature sterility, which cause a reduction of fitness. However, overall, stochastic factors appeared to predominate in determining the course of evolution of individual lines.


1991 ◽  
Vol 57 (3) ◽  
pp. 213-226 ◽  
Author(s):  
Ellen M. Heath ◽  
Michael J. Simmons

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.


1991 ◽  
Vol 57 (3) ◽  
pp. 227-234 ◽  
Author(s):  
John D. Raymond ◽  
Todd A. Ojala ◽  
Jennifer White ◽  
Michael J. Simmons

SummaryThe ability to repress P-element-induced gonadal dysgenesis was studied in 14 wild-type strains of D. melanogaster derived from populations in the central and eastern United States. Females from each of these strains had a high ability to repress gonadal dysgenesis in their daughters. Reciprocal hybrids produced by crossing each of the wild-type strains with an M strain demonstrated that repression ability was determined by a complex mixture of chromosomal and cytoplasmic factors. Cytoplasmic transmission of repression ability was observed in all 14 strains and chromosomal transmission was observed in 12 of them. Genomic Southern blots indicated that four of the strains possessed a particular type of P element, called KP, which has been proposed to account for the chromosomal transmission of repression ability. However, in this study several of the strains that lacked KP elements exhibited as much chromosomal transmission of repression ability as the strains that had KP elements, suggesting that other kinds of P elements may be involved.


Genetics ◽  
1986 ◽  
Vol 114 (4) ◽  
pp. 1147-1163
Author(s):  
Gordon J Kocur ◽  
Eric A Drier ◽  
Michael J Simmons

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.


Genetics ◽  
1990 ◽  
Vol 124 (3) ◽  
pp. 647-662 ◽  
Author(s):  
K E Rasmusson ◽  
M J Simmons ◽  
J D Raymond ◽  
C F McLarnon

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.


Genetics ◽  
1989 ◽  
Vol 121 (2) ◽  
pp. 281-291
Author(s):  
S B Daniels ◽  
A Chovnick ◽  
M G Kidwell

Abstract The molecular and phenotypic analysis of several previously described P element-transformed lines of Drosophila simulans was extended in order to determine whether they had the potential to produce a syndrome of P-M hybrid dysgenesis analogous to the one in Drosophila melanogaster. The transformed line with the highest number of P elements at the beginning of the analysis, DsP pi-5C, developed strong P activity potential and P element regulation, properties characteristic of D. melanogaster P strains. The subsequent analysis of sublines derived from 34 single pair matings of DsP pi-5C revealed that they were heterogeneous with respect to both their P element complements and P activity potentials, but similar with respect to their regulatory capabilities. The subline with the highest P activity, DsP pi-5C-27, was subsequently used as a reference P strain in the genetic analysis of the D. simulans transformants. In these experiments, the reciprocal cross effect was observed with respect to both gonadal sterility and male recombination. As in D. melanogaster, the induction of gonadal sterility in D. simulans was shown to be temperature-dependent. Molecular analysis of DsP pi-5C-27 revealed that it has approximately 30 P elements per genome, at least some of which are defective. The number of potentially complete P elements in its genome is similar to the number in the D. melanogaster P strain, Harwich-77. Overall our analysis indicates that P-transformed lines of D. simulans are capable of expressing the major features of P-M hybrid dysgenesis previously demonstrated in D. melanogaster and that P elements appear to behave in a similar way in the two sibling species.


Genetics ◽  
1993 ◽  
Vol 133 (3) ◽  
pp. 605-622 ◽  
Author(s):  
K E Rasmusson ◽  
J D Raymond ◽  
M J Simmons

Abstract Individual P elements that were genetically isolated from wild-type strains were tested for their abilities to repress two aspects of hybrid dysgenesis: gonadal dysgenesis and mutability of a double-P element-insertion allele of the singed locus (snw). These elements were also characterized by Southern blotting, polymerase chain reaction amplification and DNA sequencing. Three of the elements were 1.1-kb KP elements, one was a 1.2-kb element called D50, and one was a 0.5-kb element called SP. These three types of elements could encode polypeptides of 207, 204, and 14 amino acids, respectively. Gonadal dysgenesis was repressed by two of the KP elements (denoted KP(1) and KP(6)) and by SP, but not by the third KP element (KP(D)), nor by D50. Repression of gonadal dysgenesis was mediated by a maternal effect, or by a combination of zygotic and maternal effects generated by the P elements themselves. The mutability of snw was repressed by the KP(1) and KP(6) elements, by D50 and by SP, but not by KP(D); however, the SP element repressed snw mutability only when the transposase came from complete P elements and the D50 element repressed it only when the transposase came from the modified P element known as delta 2-3. In all cases, repression of snw mutability appeared to be mediated by a zygotic effect of the isolated P element. Each of the isolated elements was also tested for its ability to suppress the phenotype of a P-insertion mutation of the vestigial locus (vg21-3). D50 was a moderate suppressor whereas SP and the three KP elements had little or no effect. These results indicate that each isolated P element had its own profile of repression and suppression abilities. It is suggested that these abilities may be mediated by P-encoded polypeptides or by antisense P RNAs initiated from external genomic promoters.


Genetics ◽  
2002 ◽  
Vol 161 (1) ◽  
pp. 195-204 ◽  
Author(s):  
Michael J Simmons ◽  
Kevin J Haley ◽  
Craig D Grimes ◽  
John D Raymond ◽  
Jarad B Niemi

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.


1998 ◽  
Vol 71 (1) ◽  
pp. 21-30 ◽  
Author(s):  
RICHARD M. BADGE ◽  
JOHN F. Y. BROOKFIELD

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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