scholarly journals Paternally Inherited P-Element Copy Number Affects the Magnitude of Hybrid Dysgenesis in Drosophila simulans and D. melanogaster

2020 ◽  
Vol 12 (6) ◽  
pp. 808-826 ◽  
Author(s):  
Antonio Serrato-Capuchina ◽  
Jeremy Wang ◽  
Eric Earley ◽  
David Peede ◽  
Kristin Isbell ◽  
...  

Abstract Transposable elements (TEs) are repetitive regions of DNA that are able to self-replicate and reinsert themselves throughout host genomes. Since the discovery of TEs, a prevalent question has been whether increasing TE copy number has an effect on the fitness of their hosts. P-elements (PEs) in Drosophila are a well-studied TE that has strong phenotypic effects. When a female without PEs (M) is crossed to a male with them (P), the resulting females are often sterile, a phenomenon called hybrid dysgenesis (HD). Here, we used short- and long-read sequencing to infer the number of PEs in the genomes of dozens of isofemale lines from two Drosophila species and measured whether the magnitude of HD was correlated with the number of PEs in the paternal genome. Consistent with previous reports, we find evidence for a positive correlation between the paternal PE copy number and the magnitude of HD in progeny from ♀M × ♂ P crosses for both species. Other crosses are not affected by the number of PE copies. We also find that the correlation between the strength of HD and PE copy number differs between species, which suggests that there are genetic differences that might make some genomes more resilient to the potentially deleterious effects of TEs. Our results suggest that PE copy number interacts with other factors in the genome and the environment to cause HD and that the importance of these interactions is species specific.

Genome ◽  
1987 ◽  
Vol 29 (1) ◽  
pp. 195-200 ◽  
Author(s):  
Allen G. Good ◽  
Donal A. Hickey

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.


Genetics ◽  
1988 ◽  
Vol 120 (4) ◽  
pp. 1003-1013
Author(s):  
M S Jackson ◽  
D M Black ◽  
G A Dover

Abstract Mobile P elements in Drosophila melanogaster cause hybrid dysgenesis if their mobility is not repressed. One type of repression, termed P cytotype, is a complex interaction between chromosomes carrying P elements and cytoplasm and is transmitted through the cytoplasm only of females. Another type of repression is found in worldwide M' strains that contain approximately 30 copies per individual of one particular P element deletion-derivative termed the KP element. This repression is transmitted equally through both sexes. In the present study we show that biparentally transmitted repression increases in magnitude together with a rapid increase in KP copy-number in genotypes starting with one or a few KP elements and no other deletion-derivatives. Such correlated increases in repression and KP number per genome occur only in the presence of complete P elements, supporting the interpretation that they are probably a consequence of the selective advantage enjoyed by flies carrying the highest numbers of KP elements. Analysis of Q strains also reveals the presence of qualitative differences in the way the repression of dysgenesis is transmitted. In general, Q strains not containing KP elements have the P cytotype mode of repression, whereas Q strains with KP elements transmit repression through both sexes. This difference among Q strains further supports the existence of at least two types of repression of P-induced hybrid dysgenesis in natural populations of D. melanogaster.


2009 ◽  
Vol 81 (4) ◽  
pp. 679-689 ◽  
Author(s):  
Monica L. Blauth ◽  
Rafaela V. Bruno ◽  
Eliana Abdelhay ◽  
Elgion L.S. Loreto ◽  
Vera L.S. Valente

The P element is one of the most thoroughly studied transposable elements (TE). Its mobilization causes the hybrid dysgenesis that was first described in Drosophila melanogaster. While studies of the P element have mainly been done in D. melanogaster, it is believed that Drosophila willistoni was the original host species of this TE and that P was transposed to the D. melanogaster genome by horizontal transfer. Our study sought to compare the transcriptional behavior of the P element in embryos of D. melanogaster, which is a recent host, with embryos of two strains of D. willistoni, a species that has contained the P element for a longer time. In both species, potential transcripts of transposase, the enzyme responsible for the TE mobilization, were detected, as were transcripts of the 66-kDa repressor, truncated and antisense sequences, which can have the ability to prevent TEs mobilization. The truncated transcripts reveal the truncated P elements present in the genome strains and whose number seems to be related to the invasion time of the genome by the TE. No qualitative differences in antisense transcripts were observed among the strains, even in the D. willistoni strain with the highest frequency of heterochromatic P elements.


1993 ◽  
Vol 61 (2) ◽  
pp. 81-90 ◽  
Author(s):  
Chantal Vaury ◽  
Alain Pélisson ◽  
Pierre Abad ◽  
Alain Bucheton

SummaryI factors are transposable elements of Drosophila melanogaster similar to mammalian LINEs, that transpose by reverse transcription of an RNA intermediate and are responsible for the I–R system of hybrid dysgenesis. There are two categories of strains in this species: inducer, that contain about 15 I elements at the various sites on chromosomal arms, and reactive, that lack active I factors. I elements occur in various Drosophila species. Potentially functional I factors from Drosophila teissieri can transpose when introduced by P-element-mediated transformation in a reactive strain of Drosophila melanogaster. We have studied the properties of Drosophila melanogaster strains into which such an I factor from Drosophila teissieri, named Itei, was introduced. Typical hybrid dysgenesis is produced when males carrying Itei are crossed with reactive females. However, more than one copy of the element seems necessary to produce dysgenic traits, whereas only one I factor of Drosophila melanogaster seems to be sufficient. The copy number of Itei in transformed lines maintained by endogamous crosses increases rapidly and stabilizes at values similar to those observed in inducer strains. As Drosophila teissieri contains much fewer copies than the Drosophila melanogaster strains, this suggests that the copy number of I elements is not simply regulated by sequences present in the element itself.


1992 ◽  
Vol 60 (1) ◽  
pp. 15-24 ◽  
Author(s):  
Dominique Higuet ◽  
Dominique Anxolabéhére ◽  
Danielle Nouaud

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.


1989 ◽  
Vol 54 (1) ◽  
pp. 13-22 ◽  
Author(s):  
Stéphane Ronsseray ◽  
Monique Lehmann ◽  
Georges Periquet

SummaryM and M′ strains of Drosophila melanogaster in the P-M system of hybrid dysgenesis were compared in two series of tests, with the following results. (1) The singed-weak hypermutability regulation test showed that M′ strains had lower P excision rates than M strains, suggesting that P-elements repression must occur in M′ strains although it is not detectable by gonadal dysgenesis assays. (2) The evolution of mixed P + M and mixed P + M′ populations was compared, using a strong P strain. The P + M cultures invariably evolved in a few generations into strong P cultures, while the P + M′ cultures evolved into P-type cultures with reduced P-factor potentials. However, after 30 generations of culture, both these types of mixed cultures had similar P copy numbers, suggesting that regulation of copy number had occurred in them.


1992 ◽  
Vol 59 (1) ◽  
pp. 1-9 ◽  
Author(s):  
Walter F. Eanes ◽  
Cedric Wesley ◽  
Brian Charlesworth

SummaryThe accumulation of a transposable element inside chromosomal inversions is examined theoretically by a mathematical model, and empirically by counts of P elements associated with inversion polymorphisms in natural populations of Drosophila melanogaster. The model demonstrates that, if heterozygosity for an inversion effectively reduces element associated production of detrimental chromosome rearrangements, a differential accumulation of elements is expected, with increased copy number inside the minority inversion. Several-fold differential accumulations are possible with certain parameter values. We present data on P element counts for inversion polymorphisms on all five chromosome arms of 157 haploid genomes from two African populations. Our observations show significantly increased numbers of elements within the regions associated with the least common, or minority arrangements, in natural inversion polymorphisms.


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 ◽  
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 ◽  
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.


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