Evidence that intergenic spacer repeats of Drosophila melanogaster rRNA genes function as X-Y pairing sites in male meiosis, and a general model for achiasmatic pairing.

McKee, Bruce D.; Habera, Ledare F.; Vrána, Jan

doi:10.1093/genetics/132.2.529

Cited by 118 publications

(13 citation statements)

References 49 publications

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“…[49,51]). There are specific sequences used to pair X and Y chromosomes [60], and improper chromatin separation due to divergence in these sequences has been shown to cause inviability in hybrids between D. melanogaster and D. simulans due to [50]. This latter scenario could potentially explain the sex-specific occurrence of hybrid sterility in those species with sex-chromosome-specific mechanisms of segregation.…”

Section: Discussionmentioning

confidence: 99%

A common suite of cellular abnormalities and spermatogenetic errors in sterile hybrid males inDrosophila

2020

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When two species interbreed, the resulting hybrid offspring are often sterile, with the heterogametic (e.g. XY) hybrid usually being more severely affected. The prevailing theory for this pattern of sterility evokes divergent changes in separate lineages having maladaptive interactions when placed together in a hybrid individual, with recessive factors on the sex chromosome interacting with dominant factors on the autosomes. The effect of these interactions on gametogenesis should not be uniform across species pairs unless genetic divergence follows the same paths in different lineages or if a specific stage of gametogenesis is more susceptible to detrimental genetic interactions. Here, we perform a detailed cellular characterization of hybrid male sterility across three recently diverged species pairs of Drosophila . Across all three pairs, sterile hybrid sperm are alive but exhibit rapid nuclear de-condensation with age, with active, but non-differentiated, mitochondria. Surprisingly, all three sets of interspecies hybrids produce half of the number of sperm per round of spermatogenesis, with each sperm cell containing two tails. We identify non-disjunction failures during meiosis I as the likely cause. Thus, errors during meiosis I may be a general phenomenon underlying Drosophila male sterility, indicating either a heightened sensitivity of this spermatogenic stage to failure, or a basis to sterility other than the prevailing model.

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Section: Discussionmentioning

confidence: 99%

A common suite of cellular abnormalities and spermatogenetic errors in sterile hybrid males inDrosophila

2020

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“…The repeat that is responsible for most of the size increase of Y M , and ranked second on Y L , is a 267--bp long satellite sequence that is homologous to the intergenic spacer region (IGS) of the rDNA cluster. In many Drosophila species, including D. melanogaster, the rDNA cluster is found on both the X and Y chromosome, and functions as a pairing site for the sex chromosomes during meiosis (36). A previous study has shown that the Y of D. pseudoobscura -which is not homologous to the Y of D. melanogaster -lacks functional rDNA clusters on the Y (37).…”

Section: Molecular Characterization Of Repeat Content Of Y Chromosomesmentioning

confidence: 99%

Transposable element accumulation drives size differences among polymorphic Y chromosomes in Drosophila

Nguyen

Bachtrog

2021

Preprint

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Y chromosomes of many species are gene poor and show low levels of nucleotide variation, yet often display high amounts of structural diversity. Dobzhansky cataloged several morphologically distinct Y chromosomes in Drosophila pseudoobscura that differ in size and shape, but the molecular causes of their dramatic size differences are unclear. Here we use cytogenetics and long-read sequencing to study the sequence content of polymorphic Y chromosomes in D. pseudoobscura. We show that Y chromosomes differ by almost 2-fold in size, ranging from 30 to 60 Mb. Most of this size difference is caused by a handful of active transposable elements (TEs) that have recently expanded on the largest Y chromosome, with different elements being responsible for Y expansion on differently sized D. pseudoobscura Ys. We show that Y chromosomes differ in their heterochromatin enrichment, expression of Y-enriched TEs, and also influence expression of dozens of autosomal and X-linked genes. Intriguingly, the same helitron element that showed the most drastic amplification on the largest Y in D. pseudoobscura independently amplified on a polymorphic large Y chromosome in D. affinis, suggesting that some TEs are inherently more prone to become deregulated on Y chromosomes.

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“…At least some of these amplified segments may be important in Y chromosome structure. MCKEE, HABERA and VRANA (1992) have recently suggested that the Drosophila simulans repeats are involved in the meiotic pairing of X and Y chromosomes.…”

Section: Y Chromosome Also Has Telomere-associatedmentioning

confidence: 99%

The Y chromosome of Drosophila melanogaster contains a distinctive subclass of Het-A-related repeats.

et al. 1993

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The HeT-A element is a transposable element with an apparent role in the structure of the telomeres of Drosophila melanogaster chromosomes. HeT-A transposition is the earliest event detected in healing of broken ends; HeT-A is also found on telomeres of unbroken chromosomes. Sequences with homology to HeT-A are never detected in euchromatic regions; however, clusters of HeT-A-related sequences occur in nontelomeric regions of the heterochromatic Y chromosome. Analysis of two of these Y-associated clusters shows them to be significantly different in structure from telomeric HeT-A elements, although the regions of shared sequence have > 80% sequence identity in all cases. Telomeric HeT-A elements occur in chains, with the elements in the same orientation but variably truncated at their external ends and irregularly interspersed with unrelated sequences. In contrast, the nontelomeric Y elements are regular tandem repeats of parts of the HeT-A sequence joined to unrelated sequences which are not the same in the two clusters studied. The sequence structures suggest that the nontelomeric clusters on the Y chromosome do not arise by the same transposition mechanism that forms the telomeric clusters; instead the clusters on the Y may arise by a mechanism that is used more generally in the evolution of Y chromosomes. Although the telomeric and nontelomeric clusters appear to be formed differently, both are enriched in parts of the HeT-A sequence which may be important in the structure of heterochromatin.

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Evidence that intergenic spacer repeats of Drosophila melanogaster rRNA genes function as X-Y pairing sites in male meiosis, and a general model for achiasmatic pairing.

Cited by 118 publications

References 49 publications

A common suite of cellular abnormalities and spermatogenetic errors in sterile hybrid males inDrosophila

A common suite of cellular abnormalities and spermatogenetic errors in sterile hybrid males inDrosophila

Transposable element accumulation drives size differences among polymorphic Y chromosomes in Drosophila

The Y chromosome of Drosophila melanogaster contains a distinctive subclass of Het-A-related repeats.

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