Transposable Element Expression and Regulation Profile in Gonads of Interspecific Hybrids of Drosophila arizonae and Drosophila mojavensis wrigleyi (original) (raw)
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Identification of misexpressed genetic elements in hybrids between Drosophila-related species
Scientific Reports, 2017
Crosses between close species can lead to genomic disorders, often considered to be the cause of hybrid incompatibility, one of the initial steps in the speciation process. How these incompatibilities are established and what are their causes remain unclear. To understand the initiation of hybrid incompatibility, we performed reciprocal crosses between two species of Drosophila (D. mojavensis and D. arizonae) that diverged less than 1 Mya. We performed a genome-wide transcriptomic analysis on ovaries from parental lines and on hybrids from reciprocal crosses. Using an innovative procedure of co-assembling transcriptomes, we show that parental lines differ in the expression of their genes and transposable elements. Reciprocal hybrids presented specific gene categories and few transposable element families misexpressed relative to the parental lines. Because TEs are mainly silenced by piwiinteracting RNAs (piRNAs), we hypothesize that in hybrids the deregulation of specific TE families is due to the absence of such small RNAs. Small RNA sequencing confirmed our hypothesis and we therefore propose that TEs can indeed be major players of genome differentiation and be implicated in the first steps of genomic incompatibilities through small RNA regulation. Interspecific hybridization can be considered as a stress condition with multiple consequences for the hybrid genome. It may cause chromosomal rearrangements, inversions, deletions, changes in gene expression, changes in DNA methylation, among other effects 1,2. Global activation of transposable elements (TEs), which induces profound changes in the hybrid genome, has also been described. Such changes generate new phenotypes and the formation of reproductively isolated populations because the accumulation of structural and functional genomic changes acts as a pressure leading to speciation 3-5. For example, hybrid Helianthus, derived from crosses of the same parental species with other hybrids, have 50% more nuclear DNA than the parental species, mainly due to bursts of transposition 6. Interspecific hybrids of kangaroos from the Macropodidae family also showed variation in amplification of satellite repeats and kerV-1 element, changes in chromatin structure and rearrangements of whole chromosome arms 7 , which demonstrates that during hybridization, increased transposition is observed, inducing significant changes in karyotype 3,8. In Drosophila, studies of intraspecific crosses revealed asymmetric sterility of the offspring. This phenomenon was named hybrid dysgenesis and was first described in the 1960s in D. melanogaster with the I/R system 9 and then the P/M system 10. Hybrid dysgenesis corresponds to aberrant phenotypic traits observed in the F1 of crosses between particular strains or natural populations and was proposed as a possible driver of speciation 1,11. Hybrid dysgenesis was attributed to differences in TE contents between parental lines. We now know that TEs are major components of the genome architecture because they may encompass a large fraction of the genome size and may trigger recombination. However, we also know that most of the TEs in the genomes are inactive. The last decade shed light on TE epigenetic control. In Drosophila, most TEs are post-transcriptionally silenced via a particular class of small RNAs, called piRNAs (piwi-interacting RNAs) 12-14. Subsequently, transcriptional silencing is also caused by chemical histone modifications, which change the chromatin structure 15,16. When the efficiency of the effectors of these pathways is no longer maintained, TEs may transpose into genomes, which leads to significant decreases in fitness, including lethality 17-19. Due to the recent development of our knowledge in epigenetics, we
Proceedings of the National Academy of Sciences, 1997
A hybrid dysgenesis syndrome occurs in Drosophila virilis when males from an established laboratory strain are crossed to females obtained from the wild, causing the simultaneous mobilization of several different transposable elements. The insertion sequence responsible for the mutant phenotype of a dysgenic yellow allele has been characterized and named Penelope. In situ hybridization and Southern analyses reveal the presence of more than 30 copies of this element in the P-like parental strain, whereas Penelope is absent in all M-like strains tested. Penelope contains one 2.5-kb-long ORF that could encode products with homology to integrase and reverse transcriptase. Northern analysis and whole-mount in situ hybridization show strong induction of a 2.6-kb RNA in the ovaries of dysgenic females that is expressed at very low levels in the parental strains or in the progeny from the reciprocal cross. Injection of Penelope-containing plasmids into preblastoderm embryos of an M-like strain results in mutant progeny caused by insertion of Ulysses and perhaps other transposons, suggesting that Penelope expression might be responsible for the observed dysgenesis syndrome and the simultaneous mobilization of other transposable elements.
Diverse transposable elements are mobilized in hybrid dysgenesis in Drosophila virilis
Proceedings of the …, 1995
We describe a system of hybrid dysgenesis in Drosophila virilis in which at least four unrelated transposable elements are all mobilized following a dysgenic cross. The data are largely consistent with the superposition of at least three different systems of hybrid dysgenesis, each repressing a different transposable element, which break down following the hybrid cross, possibly because they share a common pathway in the host. The data are also consistent with a mechanism in which mobilization of a single element triggers that of others, perhaps through chromosome breakage. The mobilization of multiple, unrelated elements in hybrid dysgenesis is reminiscent of McClintock's evidence [McClintock, B. (1955) Brookhaven Symp. Biol. 8, 58-74] for simultaneous mobilization of different transposable elements in maize.
Scientific Reports
Interspecific hybridization is a stressful condition that can lead to sterility and/or inviability through improper gene regulation in Drosophila species with a high divergence time. However, the extent of these abnormalities in hybrids of recently diverging species is not well known. Some studies have shown that in Drosophila, the mechanisms of postzygotic isolation may evolve more rapidly in males than in females and that the degree of viability and sterility is associated with the genetic distance between species. Here, we used transcriptomic comparisons between two Drosophila mojavensis subspecies and D. arizonae (repleta group, Drosophila) and identified greater differential gene expression in testes than in ovaries. We tested the hypothesis that the severity of the interspecies hybrid phenotype is associated with the degree of gene misregulation. We showed limited gene misregulation in fertile females and an increase in the amount of misregulation in males with more severe ste...
G3 Genes|Genomes|Genetics, 2017
Transposable elements (TEs) are virtually ubiquitous components of genomes, yet they often impose significant fitness consequences on their hosts. In addition to producing specific deleterious mutations by insertional inactivation, TEs also impose general fitness costs by inducing DNA damage and participating in ectopic recombination. These latter fitness costs are often assumed to be dosage-dependent, with stronger effects occurring in the presence of higher TE copy numbers. We test this assumption in Drosophila melanogaster by considering the relationship between the copy number of two active DNA transposons, P-element and hobo element, and the incidence of hybrid dysgenesis, a sterility syndrome associated with transposon activity in the germline. By harnessing a subset of the Drosophila Genetic Reference Panel (DGRP), a group of fully-sequenced D. melanogaster strains, we describe quantitative and structural variation in P-elements and hobo elements among wild-derived genomes an...
A Genome-Wide Survey of Genetic Instability by Transposition in Drosophila Hybrids
Hybridization between species is a genomic instability factor involved in increasing mutation rate and new chromosomal rearrangements. Evidence of a relationship between interspecific hybridization and transposable element mobilization has been reported in different organisms, but most studies are usually performed with particular TEs and do not discuss the real effect of hybridization on the whole genome. We have therefore studied whole genome instability of Drosophila interspecific hybrids, looking for the presence of new AFLP markers in hybrids. A high percentage (27-90%) of the instability markers detected corresponds to TEs belonging to classes I and II. Moreover, three transposable elements (Osvaldo, Helena and Galileo) representative of different families, showed an overall increase of transposition rate in hybrids compared to parental species. This research confirms the hypothesis that hybridization induces genomic instability by transposition bursts and suggests that genomic stress by transposition could contribute to a relaxation of mechanisms controlling TEs in the Drosophila genome.
Specific activation of an I-like element in Drosophila interspecific hybrids
Genome biology and evolution, 2014
The non-long terminal repeat (LTR) retrotransposon I, which belongs to the I superfamily of non-LTR retrotransposons, is well known in Drosophila because it transposes at a high frequency in the female germline cells in I-R hybrid dysgenic crosses of Drosophila melanogaster. Here, we report the occurrence and the upregulation of an I-like element in the hybrids of two sister species belonging to the repleta group of the genus Drosophila, D. mojavensis, and D. arizonae. These two species display variable degrees of pre- and postzygotic isolation, depending on the geographic origin of the strains. We took advantage of these features to explore the transposable element (TE) dynamics in interspecific crosses. We fully characterized the copies of this TE family in the D. mojavensis genome and identified at least one complete copy. We showed that this element is transcriptionally active in the ovaries and testes of both species and in their hybrids. Moreover, we showed that this element i...
Ontogenetic consequences of dysgenic crosses in Drosophila virilis
The International Journal of Developmental Biology, 2013
Hybrid dysgenesis (HD) syndrome in Drosophila virilis presumably results from the mobilization of several unrelated mobile genetic elements in dysgenic hybrids. Morphogenetic events during oogenesis and spermatogenesis were investigated in detail in the progeny of D. virilis dysgenic crosses. Using germ-cell specific anti-Vasa staining, we monitored the fate of germline cells at different ontogenetic stages in strains of D. virilis and their hybrids. Anti-Vasa staining indicated that the major loss of pole cells occurs in dysgenic embryos at stage 11-14 after primordial germ cells (PGC) pass the midgut wall. At later ontogenetic stages, including larvae, pupae and imagoes, we often observed an abnormal development of gonads in dysgenic individuals with a frequent occurrence of unilateral and bilateral gonadal atrophy. Dysgenic females were characterized by the presence of various sterile ovarian phenotypes that predominantly include agametic ovarioles, while other atypical forms such as tumor-like ovarioles and dorsalized ovariolar follicles may also be present. Testis abnormalities were also frequently observed in dysgenic males. The sterility manifestations depended on the strain, the growing temperature and the age of the flies used in crosses. The observed gonadal sterility and other HD manifestations correlated with the absence of maternal piRNAs homologous to Penelope and other transposons in the early dysgenic embryos. We speculate that gonadal abnormalities mimicking several known sterility mutations probably result from the disturbance of developmental gene expression machinery due to the activation of unrelated families of transposons in early dysgenic embryos.
Proceedings of The National Academy of Sciences, 2005
Hybrid dysgenesis in Drosophila is a syndrome of gonadal atrophy, sterility, and male recombination, and it occurs in the progeny of crosses between males that harbor certain transposable elements (TEs) and females that lack them. Known examples of hybrid dysgenesis in Drosophila melanogaster result from mobilization of individual families of TEs, such as the P element, the I element, or hobo. An example of hybrid dysgenesis in Drosophila virilis is unique in that multiple, unrelated families of TEs become mobilized, but a TE designated Penelope appears to play a major role. In all known examples of hybrid dysgenesis, the paternal germ line transmits the TEs in an active state, whereas the female germ line maintains repression of the TEs. The mechanism of maternal maintenance of repression is not known. Recent evidence suggests that the molecular machinery of RNA interference may function as an important host defense against TEs. This protection is mediated by the action of endogenous small interfering RNAs (siRNAs) composed of dsRNA molecules of 21-25 nt that can target complementary transcripts for destruction. In this paper, we demonstrate that endogenous siRNA derived from the Penelope element is maternally loaded in embryos through the female germ line in D. virilis. We also present evidence that the maternal inheritance of these endogenous siRNAs may contribute to maternal repression of Penelope. hybrid dysgenesis | maternal effect | RNA interference | transposable element