* Institut Jacques Monod, Universités Paris 6 et 7, CNRS, Laboratoire Dynamique du Génome et Evolution, Paris, France
CNRS. Laboratoire Population, Génétique et Evolution, Gif sur Yvette, France
Correspondence: E-mail: higuet{at}ccr.jussieu.fr.
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Abstract |
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Key Words: hybrid dysgenesis hobo element permissivity microsatellite
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Introduction |
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The behavior of hobo elements with regard to the TPE repeats remains to be elucidated. Indeed, the 3TPE hobo element (HFL1) has been shown experimentally to be active, which is consistent with its worldwide distribution. Ladevèze et al. (1994, 1998, 2001) have shown in transgenic lines that this element is able to spread within the genome of D. melanogaster. In other respects, in European populations the 5TPE element is distributed along a centrifugal frequency gradient. In Western European populations this element is even more frequent than the 3TPE element (Bonnivard, Bazin, and Higuet 2002), and the authors suggest that the 5TPE element could be replacing the 3TPE element in European populations. We have shown that the 5TPE element is active and has been transposed in transgenic lines of D. melanogaster (Souames et al. 2003). Then, the situation observed in natural populations could be the consequence of the intrinsic ability of the 5TPE hobo element to transpose.
In this article we report an investigation of the capacity of 5TPE hobo elements to invade transgenic lines of D. melanogaster. To detect any interactions, we carried out our investigation in two different genetic contexts, a noncompetitive genetic context, in which 5TPE or 3TPE elements evolved in isolation, and a competitive genetic context, in which they evolved together in the same line. To survey the evolution of hobo elements in the lines over time, molecular and functional parameters have been used. At the molecular level we surveyed the evolution over time of the mean copy number per fly of full-sized hobo elements. At the functional level, we used the ability of hobo elements to induce a hybrid dysgenesis syndrome. This occurs in the F1 progeny of dysgenic crosses involving females devoid of hobo elements (E females) and males bearing hobo elements (H males). Increasing mutation rate, chromosomal rearrangements and breakage, male recombination, and thermosensitive sterility at 23°25°C can be observed (Blackman et al. 1987; Yannopoulos et al. 1987; Stamatis et al. 1989). Complete agonadism is responsible for the thermosensitive sterility symptom (GD sterility). From these symptoms, we used the GD sterility to estimate the activity and the permissivity in each line. The hobo activity is defined as the ability of hobo elements to induce GD sterility in the dysgenic cross. The permissivity is the ability of the females to allow hobo activity in their progeny when they are crossed with males harboring active hobo elements. A low level of GD sterility reflects a low level of permissivity that indicates a regulatory potential of the tested line. A high level of GD sterility reflects a high level of permissivity that signals the absence of a regulatory potential. We show that the ability of the 5TPE element to invade the genome of D. melanogaster could be related not only to its intrinsic transposition capacity but also to a putative regulatory effect on the 3TPE element.
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Materials and Methods |
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The CyHBL1 strain was used as the reference strain for estimating the mean copy number of full-sized hobo elements in the lines, because it contains one copy of the HFL1 element per diploid genome (Calvi and Gelbart 1994). The 23.5/Cy MRF reference strain was used as a source of hobo transposase in the permissivity analysis (Yannopoulos et al. 1983; 1987; Bazin and Higuet 1996). The 23.5/Cy MRF reference strain harbors 3TPE hobo elements.
Transgenic Lines: Constructs and Microinjections
The pHfl1 plasmid is a complete 3TPE hobo element cloned in the pBlueScript (Calvi, Hong, and Gelbart 1991). The pHfl5 is a 5TPE element obtained by substituting an S region with 5TPE repeats for the S region of pHfl1 (Béatrice Denis, personal communication). The pHfl plasmids (1 and 5) were digested by two enzymes, KpnI and NaeI, to obtain a restriction fragment that contains the complete hobo element plus 0.5-kb of genomic DNA and a small fragment of pBlueScript. These 3.4-kb fragments, containing either the 3TPE hobo element or the 5TPE hobo element, were inserted into the KpnI/StuI pUAST plasmid fragment. This plasmid, described in Brand and Perrimon (1993), contains the 5' and the 3' ends of the P element with the miniwhite reporter gene. The resulting constructs are pP{3TPE hobo, white+} and pP{5TPE hobo, white+}.
Dechorionated early embryos from the ME yw strain (devoid of P and hobo elements) were microinjected with pP{3TPE hobo, white+} and pP{5TPE hobo, white+} constructs using the 2.3 helper plasmid as a P transposase source (Laski, Rio, and Rubin 1986). The F0 survival adults were crossed with individuals from the yw strain on standard medium at 25°C. The individual F1 progeny were screened for eye color that ranged from pale yellow to orange. Thus, brothers and sisters with a given eye color were crossed to establish a transgenic line. Four independent transgenic lines with the 3TPE element (lines
, ß,
, and
) and one line with the 5TPE element (line
) were obtained. It was possible to distinguish heterozygous and homozygous individuals using an eye color screening.
hobo T-lines
One hundred hobo T-lines were established in the laboratory from the four independent transgenic lines bearing the 3TPE element and the transgenic line bearing the 5TPE element. These lines were maintained in vials at 25°C and at each generation parents (50 to 100 individuals) were discarded after 24 hours of egg-laying. Thirty hobo 3T-lines were obtained from a single pair of heterozygous flies of the initial transgenic lines bearing the 3TPE hobo element, among which four were chosen to be analyzed. The 3-A and 3-B lines were obtained from the same progenitor transgenic line, whereas 3-C and 3-D lines were independently obtained from two other transgenic lines (table 1). Thirty hobo 5T-lines were obtained from a single pair of heterozygous flies of the initial transgenic line bearing the 5TPE hobo element. We chose four lines (5-A to 5-D) to be analyzed (table 1). These hobo 3T-lines and hobo 5T-lines provide a noncompetitive genetic context in which to study hobo behavior.
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Functional Analysis of the Behavior of hobo Elements
One of the parameters of the hybrid dysgenesis syndrome induced by hobo elements that we used to estimate the activity of hobo elements and the permissivity of the lines was GD sterility, measured by atrophied gonads (i.e., complete agonadism as defined in the P-M system by Kidwell and Novy 1979). In other respects, GD sterility has also been used to estimate the intra-strain GD sterility that reflects the result of both hobo activity and permissivity.
Intra-strain GD Sterility Assay
The intra-strain GD sterility (intraGD) was measured at the 11th, 17th, and 20th generations after the establishment of the lines. A mean number of 50 females (at least 35 females) per line and per generation were sampled and fed for 2 days on standard medium at 25°C before being dissected. The intraGD was estimated as the percentage of dystrophic ovaries: (number dystrophic ovaries/number dissected) x 100.
Activity of the hobo T-lines
In each hobo T-line, the hobo activity (induced GD sterility) was measured in the F1 progeny of crosses between five zola strain females (E females) and five hobo T-line males (males under test). Crosses were performed at 25°C for six generations (5th, 7th, 11th, 14th, 17th, and 20th). At each generation, each line was studied through two replicates, and a mean of 50 females per replicate were dissected.
Permissivity of the hobo T-lines
The permissivity of each hobo T-line was measured in the F1 female progeny of the crosses between females from the T-lines (females under test) and males from the 23.5/Cy MRF reference strain (H males) and based on the GD sterility induced by the paternal 23.5 MRF chromosome. The analyses were performed twice after the 11th generation. Eight of the 16 mass-cultured T-lines (5-B, 5-C, 3-C, 3-D, 53-B, 53-D, 35-A, and 35-D) and four other hobo T-lines maintained in vials (510, 328, 5310, and 354; table 1) were analyzed. The GD sterility was measured by determining the number of dystrophic ovaries. The control cross of permissivity involved females from the yw strain used for the transformation experiment.
Molecular Analysis of the Behavior of hobo Elements
Southern Blot Analysis
DNA extractions were performed on 30 females from each hobo T-line according to the Junakovic, Caneva, and Ballario (1984) protocol. Two micrograms of DNA were digested with the XhoI enzyme that generates a 2.6-kb internal fragment corresponding to the complete hobo element. Six generations (5th, 7th, 11th, 14th, 17th, and 20th) were tested. The standard Southern blot technique (Sambrook, Fritsch, and Maniatis 1989) was used to estimate the mean copy number of full-sized hobo elements in the lines. To assess the amount of DNA present, the membranes were hybridized with a white gene probe that reveals the endogenous white gene. The relative amount of DNA in the lanes was estimated by scanning densitometry, using the signal intensities of the endogenous white gene referring to the yw strain. To estimate the number of full-sized hobo elements, the membranes were then hybridized with a hobo probe, an eluted XhoI internal fragment from the hobo108 plasmid (Streck, MacGaffey, and Beckendorf 1986). The mean copy number of full-sized elements per fly in a line corresponds to the ratio of the hobo108 signal intensities of the hobo T-line and the CyHBL1 strain, corrected by the ratio of DNA amount.
Polymerase Chain Reaction Analysis
The lines were established from heterozygous individuals, and two main classes were expected: [H] class individuals containing hobo elements and [E] class individuals devoid of these elements. Actually, the [H] class consists of one class in the hobo 3T-lines and one in the hobo 5T-lines, the [3] and [5] classes, respectively, whereas it consisted of [3], [5], and [3,5] classes in hobo 35T-lines and hobo 53T-lines. To estimate the proportions of the different classes in the lines, samples of 10 flies were individually analyzed at the 7th and the 20th generations by h11-h6 polymerase chain reaction (PCR) amplification (Bazin and Higuet 1996). The h11 (17561774) and h6 (21482168) primers are specific primers of the S region that contains the TPE repeats. DNA extractions were performed following the DiFranco et al. protocol (1995), and PCR products were screened on a 2% agarose gel allowed to migrate on ice for 3 hours at 100 V.
Statistical Analysis
Hierarchical analyses of variance (ANOVA), followed by Duncan multiple pairwise comparisons, were performed on the activity data (after arcsin transformation), and on the mean copy number of full-sized hobo elements. We performed the r coefficient of correlation test on arcsin
transformed data of the activity and the mean copy number of full-sized elements. To compare the proportions of classes of individuals in the lines, we performed exact Fisher tests with the level of significance corrected using the sequential Bonferroni technique (Rice 1989). To compare the levels of permissivity, we performed a Chi-square test. All statistical analyses were performed using the S.A.S. statistics software package (S.A.S. Institute, Cary, NC, 1989).
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Results |
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Noncompetitive versus Competitive Genetic Backgrounds
The ANOVA on activity data did not reveal significant differences in the mean activity levels estimated on all replicates and at all generations between hobo 35T-lines / hobo 53T-lines and hobo 5T-lines / hobo 3T-lines (P > 0.05). The ANOVA and Duncan multiple pairwise comparisons revealed that, even though the activity level did not increase through time, it has fluctuated (P < 0.05; table 2). Hence, the activity level at the 5th generation is lower than that of the later generations tested (table 2). With regard to the mean copy number of full-sized elements, the ANOVA revealed a weak replicate effect (P < 0.05; table 3). It also revealed an effect of the type of line (P < 0.01). The Duncan multiple pairwise comparisons revealed that hobo 3T-lines are statistically different from the hobo 53T, hobo 35T, and hobo 5T-lines (P < 0.05). Finally, the ANOVA revealed a generation effect (P < 0.001) that is due to the difference in the mean copy number of full-sized elements between the 5th generation and the 20th generation (Duncan multiple pairwise comparison, P < 0.05).
Permissivity of the Females of the hobo T-lines
The mean level of permissivity of the yw strain is estimated to be 27.81% GD (table 4). The mean level of permissivity of the hobo 3T-lines is estimated to be 45.27% GD, whereas that of the hobo 5T-lines is estimated to be lower, 6.69% GD (table 4). The hobo 3T-lines are significantly more permissive than the yw strain (2 = 90.82; df = 1; P < 0.001), whereas the hobo 5T-lines are less permissive than this same reference strain (
2 = 204.97; df = 1; P < 0.001). Five of the six lines tested showed lower levels (4.9% to 13.4% GD) than yw, whereas the 5310 line showed a higher level of permissivity (43.7% GD). Lastly, we observed low levels of permissivity in the F1 progeny of crosses in both directions between a hobo 3T-line and hobo 5T-line (9.5% and 15.2% GD). The variability between the lines bearing both elements could be due to differing proportions of 5TPE and 3TPE elements in these lines.
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hobo 3T-lines versus hobo 5T-lines
In hobo 3T-lines and hobo 5T-lines, two classes were expected: individuals harboring hobo elements ([3] or [5] class) and individuals devoid of hobo elements ([E] class) (table 5). All the Fisher exact tests that we performed in hobo 3T-lines and hobo 5T-lines were nonsignificant (P > 0.05), suggesting that the replicates in hobo 3T-lines and hobo 5T-lines were homogeneous in any given generation and that no change in the proportions occurred over time. The hobo 3T-lines and hobo 5T-lines were not significantly different at the 7th generation tested with regard to the proportions of [H] individuals (i.e., [3] or [5]) and [E] individuals (P > 0.05). In contrast, hobo 3T-lines and hobo 5T-lines were significantly different at the 20th generation (P < 0.05). This difference is due mainly to the under-representation of the [3] class in the 3-B line.
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These comparisons revealed just one significant difference at the 7th generation between the [5,*] and [E/5] classes of the hobo 35T-lines plus hobo 53T-lines and the [5] and [E] classes of hobo 5T-lines (P < 0.05). Such a difference was not found when we compared [3,*] and [E/3] classes to [3] and [E] classes in hobo 3T-lines. The initiation of each hobo 3T-line and hobo 5T-line involved one pair of flies that were heterozygous for the insert containing the hobo element. The initiation of each hobo 35T-line and hobo 53T-line involved one pair of flies heterozygous for one insert (containing the 3TPE element or 5TPE element) and homozygous for the site without the other insert. Thus, in early generations the [E/3] and [E/5] classes in the hobo 35T-lines and hobo 53T-lines were expected to be higher than the [E] classes in the hobo 3T-lines and hobo 5T-lines. Unexpectedly, the hobo 35T-lines and hobo 53T-lines did not differ from hobo 3T-lines ([3,*], [E/3] vs. [3], [E]), whereas such a difference was detected with regard to the 5TPE hobo element. Then, in a competitive genetic background, the 3TPE hobo element could be more invasive than the 5TPE element in early generations.
Deleted Elements
Deleted elements of very similar sizes (1.8 kb XhoI fragment) were detected in some lines from each type at different times during the evolution of the lines. Curiously, deleted elements were detected in the 3-A and 3-B lines from the 5th generation, revealing that at least one excision and DNA repair event had occurred before this generation (fig. 5). Deleted elements (1.8 kb XhoI fragment) were also detected in the 5-A line later than in the hobo 3T-lines, at the 17th and the 20th generations (data not shown). The very same elements were also detected in the 35-A T-line from the 5th generation (fig. 5), and later in the 35-D T-line at the 11th generation (data not shown). Finally, they were detected in the 53-A line at the 11th and 20th generations (data not shown).
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Discussion |
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The GD sterility is the symptom of the hybrid dysgenesis syndrome that we used to assess the hobo activity level, the permissivity level, and the result of both parameters i.e., the intra-strain GD sterility. This raises the question of whether the GD sterility is due to hobo elements or to an inbreeding effect in the host strain. We can clearly attribute the GD sterility to the presence of hobo elements insofar as neither the yw host strain nor the zola test strain ever shows any GD sterility at 25°C (complete agonadism). Moreover, both reciprocal crosses between individuals from the yw strain and the zola strain never show any GD sterility in the same conditions.
In our experiment the mean copy number of hobo elements per fly remained low (from 4 to 7), as in previous studies of the 3TPE element (from 2 to 10) carried out by Ladevèze et al. (1994, 1998, 2001) and Galindo et al. (1995). In some of our lines, XhoI fragments of the same size (
1.8 kb), putatively corresponding to 2.1 kb internally deleted elements (deletion of 800 bp), appeared independently in the lines at different generations. These deleted elements are bigger than the Th and Oh elements consisting of 1.5 and 1.1 kb XhoI fragments, respectively (Périquet et al. 1989), and the 1.7 kb Kh element (Kim and Kim 1999). It would be interesting to clone these deleted elements to see whether they have all been deleted from the same sites. There is no evidence that these deleted elements are involved in regulating the activity of the hobo elements.
The lines that bore only the 3TPE element (hobo 3T-lines) are clearly different from the other lines we established. Indeed, hobo 3T-lines are particularly distinct insofar as two situations were observed. In two lines (3-A and 3-B), the introduction of a hobo element did not trigger an invasion of the genome, whereas in the other two (3-C and 3-D) the element did start to invade. In contrast, the introduction of the 5TPE element triggered an invasion in all the hobo 5T-lines. The heterogeneity of hobo 3T-lines could be explained by a position effect of the initial insert. However, the progenitor transgenic line of 3-A and 3-B lines harbored two inserts, and when established, the 3-A line inherited both inserts whereas the 3-B line inherited only one (fig. 5). Even if one of the initial inserts was locked in a specific position on the genome, it is unlikely that both inserts would be. However, because we started our analyses at the 5th generation, it is not impossible that the 3TPE element was active in these lines. This would be consistent with the fact that deleted elements appeared from these lines insofar as the appearance of such elements is related to the excision of the complete element and the DNA repair step that follows. Lastly, these two lines raised an interesting issue in that despite the noninvasive state, the element is maintained in the lines. Moreover, none of the 26 hobo 3T-lines initially established have lost their elements as revealed by an h11-h6 PCR analysis on samples of 10 mixed flies at the 16th generation.
The hobo 5T-lines are more homogeneous than hobo 3T-lines. Moreover, the mean copy number of full-sized elements is higher in hobo 5T-lines than in hobo 3T-lines, but the activity levels were equivalent. This suggests that the 5TPE element is less active than the 3TPE element in a noncompetitive genetic context. This could explain why, in hobo 5T-lines, unlike the hobo 3T-lines, we found a correlation between the activity and the mean copy number of full-sized elements. Indeed, if the activity of the element is low; the copy number would have an impact on the level of activity, whereas this would not be the case if the element was very activei.e., one copy inducing a high level of activity. Moreover, with regard to permissivity, females bearing 3TPE elements showed a higher level of permissivity than females from the yw strain. In contrast, females bearing 5TPE elements showed a lower level of permissivity than females from the yw strain or from hobo 3T-lines. This suggests that the 3TPE element could induce GD sterility in the nondysgenic cross. However, the 328 line shows no GD sterility when crossed either way with the yw strain or when crossed with 23.5/Cy MRF females (data not shown). This suggests that the 3TPE element could enhance the activity of the 3TPE elements of the 23.5 MRF chromosome, whereas the 5TPE element could regulate the activity of these elements.
The proportions of the different classes of individuals in the lines with regard to the presence of 3TPE and/or 5TPE elements showed that the hobo 5T-lines seem to maintain their elements at least as efficiently as the hobo 3T-lines. However, in a competitive genetic background, we observed that there were relatively fewer individuals belonging to the [3] class than to the [5] class, despite an equilibrated situation at the 7th generation. This could suggest that in a competitive situation the 5TPE element may be more efficiently maintained alone (the [5] class) than the 3TPE element alone (the [3] class). This situation does not mean that the 3TPE element will necessarily disappear, as it could be maintained, mainly in the [3,5] class. This situation can be extended to the 87 hobo T-lines remaining from the 100 lines initially established. These lines were studied by an h11-h6 PCR on samples of 10 mixed flies per line. At the 16th generation, all the lines that initially had the 3TPE element or the 5TPE element gave a PCR signal. In the 34 lines that initially bore the 3TPE element and the 5TPE element, we observed 18 [3,5] lines, 12 [5] lines, 1 [3] line, and 3 [E] lines. Because of the under-representation of the [3] class relative to the [5] class, we could suggest that in a competitive context, the 3TPE element is maintained better when accompanied by the 5TPE element, whereas the 5TPE element is maintained even if it occurs alone. This could result in a higher frequency of the 5TPE element than of the 3TPE element in a competitive situation, and this would be consistent with the situation seen in some Western European populations that do indeed display higher frequencies of the 5TPE element (Bonnivard, Bazin, and Higuet 2002).
With regard to the hobo activity, the hobo 35T-lines and hobo 53T-lines are not different from the hobo 5T-lines. This suggests that the 5TPE element could decrease the activity of the 3TPE element. This is consistent with the results of the analysis of the permissivity in hobo 3T-lines and hobo 5T-lines that showed that the 5TPE hobo elements regulate the activity of 3TPE elements. Moreover, in hobo 35T-lines and hobo 53T-lines, the levels of permissivity are close to that of hobo 5T-lines. To explain such an effect, we have to speculate about the mechanistic aspects of the hobo element because the structure of the putative transposase of the hobo element is particularly poorly documented. However, Essers, Adolphs, and Kunze (2000) showed that the transposase of the maize Ac transposable element contains a domain involved in dimerization. This domain is highly conserved in the hAT superfamily. In the hobo element, this domain is located at 123 bp downstream from the TPE repeats (41 amino acids at the protein level). We could therefore argue that hobo transposase could at least act as a dimer, and consequently any change in the number of TPE repeats could have an impact either on the dimerization or the presentation of the active site of the transposase. In a noncompetitive situation the hobo transposase can only be a homodimer of 3TPE or 5TPE transposase, but in a competitive situation three classes of transposase could be formed: a 3TPE or 5TPE homodimer or a heterodimer. It is possible that in a competitive situation the 5TPE element could poison the 3TPE element transposase and that this would give it a competitive advantage by decreasing deleterious effects. Such a phenomenon could explain why the 3TPE element is maintained mainly in the [3,5] class in hobo 35T-lines and hobo 53T-lines. We need now to investigate further the hypothesis of the dimeric action of the hobo transposase relative to the TPE repeats, which could be the key to understanding the history of hobo elements in D. melanogaster species.
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Acknowledgements |
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Footnotes |
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