Defective satellite DNA clustering into chromocenters underlies hybrid incompatibility in Drosophila.
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ABSTRACT:
SUBMITTER: Jagannathan M
PROVIDER: S-EPMC8557456 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Dobzhansky-Muller incompatibilities represent a major driver of reproductive isolation between species. They are caused when two or more interacting components encoded by alleles from different species cannot function properly when mixed. At incipient stages of speciation, complex incompatibilities involving multiple genetic loci with weak effects are frequently observed, but the underlying mechanisms remain elusive. We observed perturbed proteostasis leading to compromised mitosis and meiosis in Saccharomyces cerevisiae hybrid lines carrying one or two chromosomes from Saccharomyces bayanus var uvarum. Levels of proteotoxicity are correlated with the number of protein complexes on replaced chromosomes and can be alleviated or aggravated, respectively, by up- or down-regulating the ubiquitin-proteasomal degradation machinery. Using proteomic approaches, we detect destabilized multi-protein complexes in a hybrid line. However, hybrid fitness can be significantly improved by rescuing small ribosomal subunits, a primary destabilized complex. Our findings reveal the general role of impaired protein complex assembly in complex incompatibilities.
2022-07-05 | PXD028358 | Pride
Project description:Satellite DNA spans megabases of eukaryotic sequence and evolves rapidly.1-6 Paradoxically, satellite-rich genomic regions mediate strictly conserved, essential processes such as chromosome segregation and nuclear structure.7-10 A leading resolution to this paradox posits that satellite DNA and satellite-associated chromosomal proteins coevolve to preserve these essential functions.11 We experimentally test this model of intragenomic coevolution by conducting the first evolution-guided manipulation of both chromosomal protein and DNA satellite. The 359bp satellite spans an 11 Mb array in Drosophila melanogaster that is absent from its sister species, Drosophila simulans.12-14 This species-specific DNA satellite colocalizes with the adaptively evolving, ovary-enriched protein, maternal haploid (MH), the Drosophila homolog of Spartan.15 To determine if MH and 359bp coevolve, we swapped the D. simulans version of MH ("MH[sim]") into D. melanogaster. MH[sim] triggers ovarian cell death, reduced ovary size, and loss of mature eggs. Surprisingly, the D. melanogaster mh-null mutant has no such ovary phenotypes,15 suggesting that MH[sim] is toxic in a D. melanogaster background. Using both cell biology and genetics, we discovered that MH[sim] poisons oogenesis through a DNA-damage pathway. Remarkably, deleting the D. melanogaster-specific 359bp satellite array completely restores mh[sim] germline genome integrity and fertility, consistent with a history of coevolution between these two fast-evolving loci. Germline genome integrity and fertility are also restored by overexpressing topoisomerase II (Top2), suggesting that MH[sim] interferes with Top2-mediated processing of 359bp. The observed 359bp-MH[sim] cross-species incompatibility supports a model under which seemingly inert repetitive DNA and essential chromosomal proteins must coevolve to preserve germline genome integrity.
| S-EPMC9283324 | biostudies-literature
Project description:Understanding the molecular basis of hybrid incompatibilities is a fundamental pursuit in evolutionary genetics. In crosses between Drosophila melanogaster females and Drosophila simulans males, an interaction between at least three genes is necessary for hybrid male lethality: Hmr mel, Lhr sim, and gfzf sim. Although HMR and LHR physically bind each other and function together in a single complex, the connection between gfzf and either of these proteins remains mysterious. Here, we show that GFZF localizes to many regions of the genome in both D. melanogaster and D. simulans, including at telomeric retrotransposon repeats. We find that GFZF localization at telomeres is significantly different between these two species, reflecting the rapid evolution of telomeric retrotransposon copy number composition between the two species. Next, we show that GFZF and HMR normally do not colocalize in D. melanogaster. In interspecies hybrids, however, HMR shows extensive mis-localization to GFZF sites, thus uncovering a new molecular interaction between these hybrid incompatibility factors. We find that spreading of HMR to GFZF sites requires gfzf sim but not Lhr sim, suggesting distinct roles for these factors in the hybrid incompatibility. Finally, we find that overexpression of HMR and LHR within species is sufficient to mis-localize HMR to GFZF binding sites, indicating that HMR has a natural low affinity for GFZF sites. Together, these studies provide the first insights into the different properties of gfzf between D. melanogaster and D. simulans, and uncover a molecular interaction between gfzf and Hmr in the form of altered protein localization.
| S-EPMC6657725 | biostudies-literature
Project description:Using Drosophila SL2 cells we induced overxpression of the HMR protein and generated genome-wide binding profiles by performing ChIP-Seq with anti-HMR antibody.
2019-01-01 | GSE118291 | GEO
Project description:Lethality in hybrids between Drosophila melanogaster and its sibling species Drosophila simulans is caused in part by the interaction of the genes Hybrid male rescue (Hmr) and Lethal hybrid rescue (Lhr). Hmr and Lhr have diverged under positive selection in the hybridizing species. Here we test whether positive selection of Hmr is confined only to D. melanogaster and D. simulans. We find that Hmr has continued to diverge under recurrent positive selection between the sibling species D. simulans and Drosophila mauritiana and along the lineage leading to the melanogaster subgroup species pair Drosophila yakuba and Drosophila santomea. Hmr encodes a member of the Myb/SANT-like domain in ADF1 (MADF) family of transcriptional regulators. We show that although MADF domains from other Drosophila proteins have predicted ionic properties consistent with DNA binding, the MADF domains encoded by different Hmr orthologs have divergent properties consistent with binding to either the DNA or the protein components of chromatin. Our results suggest that Hmr may be functionally diverged in multiple species.
| S-EPMC2727392 | biostudies-literature
Project description:BACKGROUND: Hybrid incompatibilities such as sterility and lethality are commonly modeled as being caused by interactions between two genes, each of which has diverged separately in one of the hybridizing lineages. The gene Lethal hybrid rescue (Lhr) encodes a rapidly evolving heterochromatin protein that causes lethality of hybrid males in crosses between Drosophila melanogaster females and D. simulans males. Previous genetic analyses showed that hybrid lethality is caused by D. simulans Lhr but not by D. melanogaster Lhr, confirming a critical prediction of asymmetry in the evolution of a hybrid incompatibility gene. RESULTS: Here we have examined the functional properties of Lhr orthologs from multiple Drosophila species, including interactions with other heterochromatin proteins, localization to heterochromatin, and ability to complement hybrid rescue in D. melanogaster/D. simulans hybrids. We find that these properties are conserved among most Lhr orthologs, including Lhr from D. melanogaster, D. simulans and the outgroup species D. yakuba. CONCLUSIONS: We conclude that evolution of the hybrid lethality properties of Lhr between D. melanogaster and D. simulans did not involve extensive loss or gain of functions associated with protein interactions or localization to heterochromatin.
| S-EPMC3060119 | biostudies-other
Project description:Interspecific hybrid lethality and sterility are a consequence of divergent evolution between species and serve to maintain the discrete identities of species. The evolution of hybrid incompatibilities has been described in widely accepted models by Dobzhansky and Muller where lineage-specific functional divergence is the essential characteristic of hybrid incompatibility genes. Experimentally tractable models are required to identify and test candidate hybrid incompatibility genes. Several Drosophila melanogaster genes involved in hybrid incompatibility have been identified but none has yet been shown to have functionally diverged in accordance with the Dobzhansky-Muller model. By introducing transgenic copies of the X-linked Hybrid male rescue (Hmr) gene into D. melanogaster from its sibling species D. simulans and D. mauritiana, we demonstrate that Hmr has functionally diverged to cause F1 hybrid incompatibility between these species. Consistent with the Dobzhansky-Muller model, we find that Hmr has diverged extensively in the D. melanogaster lineage, but we also find extensive divergence in the sibling-species lineage. Together, these findings implicate over 13% of the amino acids encoded by Hmr as candidates for causing hybrid incompatibility. The exceptional level of divergence at Hmr cannot be explained by neutral processes because we use phylogenetic methods and population genetic analyses to show that the elevated amino-acid divergence in both lineages is due to positive selection in the distant past-at least one million generations ago. Our findings suggest that multiple substitutions driven by natural selection may be a general phenomenon required to generate hybrid incompatibility alleles.
| S-EPMC423131 | biostudies-literature
Project description:Hybrid incompatibility (HI) genes are frequently observed to be rapidly evolving under selection. This observation has led to the attractive conjecture that selection-derived protein-sequence divergence is culpable for incompatibilities in hybrids. The Drosophila simulans HI gene Lethal hybrid rescue (Lhr) is an intriguing case, because despite having experienced rapid sequence evolution, its HI properties are a shared function inherited from the ancestral state. Using an unusual D. simulans Lhr hybrid rescue allele, Lhr(2), we here identify a conserved stretch of 10 amino acids in the C terminus of LHR that is critical for causing hybrid incompatibility. Altering these 10 amino acids weakens or abolishes the ability of Lhr to suppress the hybrid rescue alleles Lhr(1) or Hmr(1), respectively. Besides single-amino-acid substitutions, Lhr orthologs differ by a 16-aa indel polymorphism, with the ancestral deletion state fixed in D. melanogaster and the derived insertion state at very high frequency in D. simulans. Lhr(2) is a rare D. simulans allele that has the ancestral deletion state of the 16-aa polymorphism. Through a series of transgenic constructs we demonstrate that the ancestral deletion state contributes to the rescue activity of Lhr(2). This indel is thus a polymorphism that can affect the HI function of Lhr.
| S-EPMC3454889 | biostudies-other
Project description:Chromocenters are defined as a punctate condensed blocks of chromatin in the interphase cell nuclei of certain cell types with unknown biological significance. In recent years a progress in revealing of chromocenters protein content has been made although the details of DNA content within constitutive heterochromatin still remain unclear. It is known that these regions are enriched in tandem repeats (TR) and transposable elements. Quick improvement of genome sequencing does not help to assemble the heterochromatic regions due to lack of appropriate bioinformatics techniques.Chromocenters DNA have been isolated by a biochemical approach from mouse liver cells nuclei and sequenced on the Illumina MiSeq resulting in ChrmC dataset. Analysis of ChrmC dataset by the bioinformatics tools available revealed that the major component of chromocenter DNA are TRs: ~?66% MaSat and ~?4% MiSat. Other previously classified TR families constitute ~?1% of ChrmC dataset. About 6% of chromocenters DNA are mostly unannotated sequences. In the contigs assembled with IDBA_UD there are many fragments of heterochromatic Y-chromosome, rDNA and other pseudo-genes and non-coding DNA. A protein coding sfi1 homolog gene fragment was also found in contigs. The Sfi1 homolog gene is located on the chromosome 11 in the reference genome very close to the Golden Pass Gap (a ~?3 Mb empty region reserved to the pericentromeric region) and proves the purity of chromocenters isolation. The second major fraction are non-LTR retroposons (SINE and LINE) with overwhelming majority of LINE - ~?11% of ChrmC. Most of the LINE fragments are from the ~?2 kb region at the end of the 2nd ORF and its' flanking region. The precise LINEs' segment of ~?2 kb is the necessary mouse constitutive heterohromatin component together with TR. The third most abundant fraction are ERVs. The ERV distribution in chromocenters differs from the whole genome: IAP (ERV2 class) is the most numerous in ChrmC while MaLR (ERV3 class) prevails in the reference genome. IAP and its LTR also prevail in TR containing contigs extracted from the WGS dataset. In silico prediction of IAP and LINE fragments in chromocenters was confirmed by direct fluorescent in situ hybridization (FISH).Our data of chromocenters' DNA (ChrmC) sequencing demonstrate that IAP with LTR and a precise ~?2 kb fragment of LINE represent a substantial fraction of mouse chromocenters (constitutive hetero?hromatin) along with TRs.
| S-EPMC5819297 | biostudies-literature
Project description:Two genes encoding protein components of the nuclear pore complex Nup160 and Nup96 cause lethality in F2-like hybrid genotypes between Drosophila simulans and Drosophila melanogaster. In particular, D. simulans Nup160 and Nup96 each cause inviability when hemizygous or homozygous in species hybrids that are also hemizygous (or homozygous) for the D. melanogaster X chromosome. The hybrid lethality of Nup160, however, is genetically complex, depending on one or more unknown additional factors in the autosomal background. Here we study the genetics and evolution of Nup160-mediated hybrid lethality in three ways. First, we test for variability in Nup160-mediated hybrid lethality within and among the three species of the D. simulans clade- D. simulans, D. sechellia, and D. mauritiana. We show that the hybrid lethality of Nup160 is fixed in D. simulans and D. sechellia but absent in D. mauritiana. Second, we explore how the hybrid lethality of Nup160 depends on other loci in the autosomal background. We find that D. simulans Nup160-mediated hybrid lethality does not depend on the presence of D. melanogaster Nup96, and we find that D. simulans and D. mauritiana are functionally differentiated at Nup160 as well as at other autosomal factor(s). Finally, we use population genetics data to show that Nup160 has experienced histories of recurrent positive selection both before and after the split of the three D. simulans clade species ?240,000 years ago. Our genetic results suggest that a hybrid lethal Nup160 allele evolved before the split of the three D. simulans clade species, whereas the other autosomal factor(s) evolved more recently.
| S-EPMC4574247 | biostudies-literature