The role of the transposable element hobo in the origin of endemic inversions in wild populations of Drosophila melanogaster

Lyttle, Terrence W.; Haymer, David S.

doi:10.1007/bf00133715

Cited by 59 publications

(21 citation statements)

References 68 publications

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“…Rearrangements in which the breakpoints lack hobo elements may represent cases in which the hobo elements excised after having caused the rearrangements. The new intrachromosomal rearrangements reported here do not appear to have been described in the literature, neither in natural nor in laboratory populations of D. melanogaster (Ashburner & Lemeunier 1976;Lemeunier & Aulard 1992;Lyttle & Haymer 1992;Eggleston et al 1996). All new inversions have one breakpoint similar to that of natural endemic inversions, except In(3L)74A;76B, whose breakpoints were not described before this study.…”

Section: Resultsmentioning

confidence: 46%

Hobo transposons causing chromosomal breakpoints

Ladevèze

Aulard

et al. 1998

Proc. R. Soc. Lond. B

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Several laboratory surveys have shown that transposable elements (TEs) can cause chromosomal breaks and lead to inversions, as in dysgenic crosses involving P-elements. However, it is not presently clear what causes inversions in natural populations of Drosophila. The only direct molecular studies must be taken as evidence against the involvement of mobile elements. Here, in Drosophila lines transformed with the hobo transposable element, and followed for 100 generations, we show the appearance of ¢ve di¡erent inversions with hobo inserts at breakpoints. Almost all breakpoints occurred in hobo insertion sites detected in previous generations. Therefore, it can be assumed that such elements are responsible for restructuring genomes in natural populations.

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Section: Resultsmentioning

confidence: 46%

Hobo transposons causing chromosomal breakpoints

Ladevèze

Aulard

et al. 1998

Proc. R. Soc. Lond. B

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“…Transposable or repetitive elements may be involved in the genesis of rearrangements in Drosophila chromosomes through recombination between offset copies of an element in reverse orientation (Potter 1982;Collins and Rubin 1984;Engels and Preston 1984;Blackman et al 1987;Lim 1988;Krimbas 1992;Lyttle and Haymer 1992;Sheen et al 1993;Ladeveze et al 1998;Caceres et al 1999;Mathiopoulos et al 1999;Evgen'ev et al 2000;Casals et al 2003). The differences in gene order observed between D. melanogaster and D. pseudoobscura reflect the rearrangement history since the two species diverged from a common ancestor (known rearrangements since the species diverged are depicted in Supplemental Fig.…”

Section: Chromosomal Rearrangementsmentioning

confidence: 99%

“…Previous investigations have identified specific cases of transposons and repetitive sequences at inversion breakpoints (Lyttle and Haymer 1992;Caceres et al 1999;Mathiopoulos et al 1999;Evgen'ev et al 2000;Casals et al 2003), and in other cases, repetitive elements have not been seen at inversion breakpoints (Wesley and Eanes 1994;Cirera et al 1995). This study provides evidence that repetitive sequences can effect rearrangements on the genome scale, and may be the cause of the majority of inversions.…”

mentioning

confidence: 97%

Comparative genome sequencing ofDrosophila pseudoobscura: Chromosomal, gene, andcis-element evolution

Richards¹,

Liu²,

Bettencourt³

et al. 2005

Genome Res.

478

506

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We have sequenced the genome of a second Drosophila species, Drosophila pseudoobscura, and compared this to the genome sequence of Drosophila melanogaster, a primary model organism. Throughout evolution the vast majority of Drosophila genes have remained on the same chromosome arm, but within each arm gene order has been extensively reshuffled, leading to a minimum of 921 syntenic blocks shared between the species. A repetitive sequence is found in the D. pseudoobscura genome at many junctions between adjacent syntenic blocks. Analysis of this novel repetitive element family suggests that recombination between offset elements may have given rise to many paracentric inversions, thereby contributing to the shuffling of gene order in the D. pseudoobscura lineage. Based on sequence similarity and synteny, 10,516 putative orthologs have been identified as a core gene set conserved over 25-55 million years (Myr) since the pseudoobscura/melanogaster divergence. Genes expressed in the testes had higher amino acid sequence divergence than the genome-wide average, consistent with the rapid evolution of sex-specific proteins. Cis-regulatory sequences are more conserved than random and nearby sequences between the species-but the difference is slight, suggesting that the evolution of cis-regulatory elements is flexible. Overall, a pattern of repeat-mediated chromosomal rearrangement, and high coadaptation of both male genes and cis-regulatory sequences emerges as important themes of genome divergence between these species of Drosophila.

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“…Also, the five families of Ty retrotransposons have been important in restructuring the Saccharomyces cerevisiae genome (4). In wild populations of Drosophila melanogaster, the hobo element has been implicated in the origin of endemic inversions (5) and in Drosophila buzzatii, the breakpoints (BPs) of a cosmopolitan inversion contain large insertions corresponding to a TE (6). The frequency and relative importance of TE-induced rearrangements in natural populations have, however, been difficult to establish in any satisfactory quantitative way.…”

mentioning

confidence: 99%

Mobile elements and chromosomal evolution in the virilis group of Drosophila

Evgen’ev

Zelentsova

Poluectova

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

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Species of the virilis group of Drosophila differ by multiple inversions and chromosome fusions that probably accompanied, or led to, speciation. Drosophila virilis has the primitive karyotype for the group, and natural populations are exceptional in having no chromosomal polymorphisms. We report that the genomic locations of Penelope and Ulysses transposons are nonrandomly distributed in 12 strains of D. virilis. Furthermore, Penelope and Ulysses insertion sites in D. virilis show a statistically significant association with the breakpoints of inversions found in other species of the virilis group. Sixteen newly induced chromosomal rearrangements were isolated from the progeny of D. virilis hybrid dysgenic crosses, including 12 inversions, 2 translocations, and 2 deletions. Penelope and Ulysses were associated with the breakpoints of over half of these new rearrangements. Many rearrangement breakpoints also coincide with the chromosomal locations of Penelope and Ulysses insertions in the parental strains and with breakpoints of inversions previously established for other species of the group. Analysis of homologous sequences from D. virilis and Drosophila lummei indicated that Penelope insertion sites were closely, but not identically, located at the nucleotide sequence level. Overall, these results indicate that Penelope and Ulysses insert in a limited number of genomic locations and are consistent with the possibility that these elements play an important role in the evolution of the virilis species group. B esides inducing many types of small mutations, such as insertions and deletions, transposable elements (TEs) are well known to promote the formation of inversions and other large and small chromosomal rearrangements (e.g., ref. 1). A growing body of evidence suggests that TEs mediate genome restructuring in natural populations of a wide variety of species. For example, in hominids, a Y chromosome inversion was mediated by recombination between LINE-1 elements before the radiation of extant human populations (2), and TEs appear to have played a role in mediating some of the major restructuring of the human sex chromosomes that has taken place during the last 300 million years (3). Also, the five families of Ty retrotransposons have been important in restructuring the Saccharomyces cerevisiae genome (4). In wild populations of Drosophila melanogaster, the hobo element has been implicated in the origin of endemic inversions (5) and in Drosophila buzzatii, the breakpoints (BPs) of a cosmopolitan inversion contain large insertions corresponding to a TE (6). The frequency and relative importance of TE-induced rearrangements in natural populations have, however, been difficult to establish in any satisfactory quantitative way. One likely reason is that instability and rapid divergence of TEs make their identification at rearrangement BPs increasingly difficult with the passage of time (7).In contrast to the rich karyotypic variation found in most of the 12 species of the D. virilis species group, one member, D. ...

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The role of the transposable element hobo in the origin of endemic inversions in wild populations of Drosophila melanogaster

Cited by 59 publications

References 68 publications

Hobo transposons causing chromosomal breakpoints

Hobo transposons causing chromosomal breakpoints

Comparative genome sequencing ofDrosophila pseudoobscura: Chromosomal, gene, andcis-element evolution

Mobile elements and chromosomal evolution in the virilis group of Drosophila

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