Loss of function of CENH3 causes genome instability in soybean
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ABSTRACT:
ORGANISM(S): Glycine max
PROVIDER: GSE244481 | GEO | 2023/10/07
REPOSITORIES: GEO
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Project description:Despite the essentiality for faithful chromosome segregation, centromere architectures are diverse among eukaryotes and embody two main configurations: mono- and holocentromeres, referring respectively to localized or unrestricted distribution of centromeric activity. Of the two, some holocentromeres offer the curious condition of having arisen independently in multiple insects, most of which have lost the otherwise essential centromere-specifying factor CenH3 (first described as CENP-A in humans). The loss of CenH3 raises intuitive questions about how holocentromeres are organized and regulated in CenH3-lacking insects. Here, we report the first chromatin-level description of CenH3-deficient holocentromeres by leveraging recently-identified centromere components and genomics approaches to map and characterize the holocentromeres of the silk moth Bombyx mori, a representative lepidopteran insect lacking CenH3. This uncovered a robust correlation between the distribution of centromere sites and regions of low chromatin activity along B. mori chromosomes. Transcriptional perturbation experiments recapitulated the exclusion of B. mori centromeres from active chromatin. Based on reciprocal centromere occupancy patterns observed along differentially-expressed orthologous genes of Lepidoptera, we further found that holocentromere formation in a manner that is recessive to chromatin dynamics is evolutionarily conserved. Our results help us discuss the plasticity of centromeres in the context of a role for the chromosome-wide chromatin landscape in conferring centromere identity rather than the presence of CenH3. Given the co-occurrence of CenH3 loss and holocentricity in insects, we further propose that the evolutionary establishment of holocentromeres in insects was facilitated through the loss of a CenH3-specified centromere.
2020-10-02 | GSE158902 | GEO
Project description:The centromere, as an essential element to control chromosome segregation, is epigenetically determined by CENH3-containing nucleosomes as a functional marker, therefore the accurate deposition of CENH3 is crucial to chromosome transmission. We characterized the deposition of CENH3 in maize by over-expression and mutational analysis. Our results revealed that over-expressing CENH3 in callus is lethal while over-expressing GFP-CENH3 and CENH3-YFP in callus and plants is not and can be partly deposited normally. Different mutations of GFP-CENH3 demonstrated that CENH3-Thr4 in the N terminus was needed for the deposition as a positive phosphorylation site and the last five amino acids in the C terminus are necessary for deposition. The C terminal tail of CENH3 is confirmed to be responsible for the interaction of CENH3 and histone H4, which indicates that CENH3 maintains deposition in centromeres via interacting with H4 to form stable nucleosomes. For GFP-CENH3 and CENH3-YFP, the fused tags at the termini probably affect the structure of CENH3 and reduce its interaction with other proteins, which in turn could decrease proper deposition. Taken together, multiple amino acids or motifs were shown to play essential roles in CENH3 deposition, which is suggested to be affected by numerous factors in maize.
2020-06-01 | GSE133578 | GEO
Project description:Many existing centromeres may have originated as neocentromeres that activated de novo from non-centromeric regions. However, the evolutionary path from a neocentromere to a mature centromere has been elusive. Here we analyzed the centromeres of six chromosomes that were transferred from maize into oat as the result of an inter-species cross. Centromere size and location were assayed by chromatin immunoprecipitation for the histone variant CENH3, which is a defining feature of functional centromeres. Maize and oat are highly divergent and differ in genome size by four fold. Two isolates of maize chromosome proved to contain neocentromeres in the sense that they had moved from the original site, whereas the remaining seven centromeres (1, 2, 5, 6, 8, 9 and 10) were retained in the same area in both species. In all cases the CENH3-binding domains were dramatically expanded to encompass a larger area in the oat background (~4 Mb) than the average centromere size in maize (~2 Mb). The expansion of maize centromeres appeared to be restricted by the transcription of genes located in regions flanking the original centromeres. The results from the current study provide evidence that (1) centromere size is regulated; (2) centromere sizes tend to be uniform within a species regardless of chromosome size or origin of the centromere; and (3) neocentromeres emerge and expand preferentially in gene poor regions. Our results, together with data from several animal species, suggest that centromere size expansion may be a key factor in the survival of neocentric chromosomes in natural populations.
2013-09-01 | GSE47342 | GEO
Project description:Plant and animal centromeres comprise megabases of highly repeated satellite sequences, yet centromere function can be specified epigenetically on single-copy DNA by the presence of nucleosomes containing a centromere-specific variant of histone H3 (cenH3). We determined the positions of cenH3 nucleosomes in rice (Oryza sativa), which has centromeres composed of both the 155-bp CentO repeat and single-copy non-CentO sequences. We find that cenH3 nucleosomes protect 90-100 bp of DNA from micrococcal nuclease digestion, sufficient for only a single wrap of DNA around the cenH3 nucleosome core. cenH3 nucleosomes are translationally phased with 155-bp periodicity on CentO repeats, but not on non-CentO sequences. CentO repeats have a ~10-bp periodicity in WW dinucleotides and in micrococcal nuclease cleavage, providing evidence for rotational phasing of cenH3 nucleosomes on CentO, and suggesting that satellites evolve for translational and rotational stabilization of centromeric nucleosomes. Examination of measured size of rice centromere nucleosome
2013-11-06 | E-GEOD-50755 | biostudies-arrayexpress
Project description:Plant and animal centromeres comprise megabases of highly repeated satellite sequences, yet centromere function can be specified epigenetically on single-copy DNA by the presence of nucleosomes containing a centromere-specific variant of histone H3 (cenH3). We determined the positions of cenH3 nucleosomes in rice (Oryza sativa), which has centromeres composed of both the 155-bp CentO repeat and single-copy non-CentO sequences. We find that cenH3 nucleosomes protect 90-100 bp of DNA from micrococcal nuclease digestion, sufficient for only a single wrap of DNA around the cenH3 nucleosome core. cenH3 nucleosomes are translationally phased with 155-bp periodicity on CentO repeats, but not on non-CentO sequences. CentO repeats have a ~10-bp periodicity in WW dinucleotides and in micrococcal nuclease cleavage, providing evidence for rotational phasing of cenH3 nucleosomes on CentO, and suggesting that satellites evolve for translational and rotational stabilization of centromeric nucleosomes.
2013-11-06 | GSE50755 | GEO
Project description:In organisms ranging from vertebrates to plants, major components of centromeres are rapidly-evolving repeat sequences, such as tandem repeats (TRs) and transposable elements (TEs). These repeats harbor centromere-specific histone H3 (CENH3), which also evolves rapidly. Complete centromere structures recently determined in human and Arabidopsis suggest frequent integration and purging of retrotransposons within the TR regions of centromeres. Despite the high impact of “centrophilic” retrotransposons on the paradox of rapid centromere evolution, the mechanisms involved in centromere targeting remain poorly understood in any organism. Here we show that both Ty3 and Ty1/Copia LTR elements rapidly turnover within the centromeric TRs of Arabidopsis species. We demonstrate that the Ty1/Copia element Tal1 (Transposon of Arabidopsis lyrata 1) integrates de novo into regions occupied by CENH3 in A. thaliana, and that ectopic expansion of the CENH3 region results in spread of Tal1 integration regions. The integration spectra of chimeric TEs revealed the key structural variations responsible for the contrasting chromatin targeting specificities to centromeres versus gene-rich regions, which have recurrently converted during the evolution of these TEs. Our findings reveal the impact of centromeric chromatin on TE-mediated rapid centromere evolution, with relevance across eukaryotic genomes.
2024-08-08 | GSE263225 | GEO
Project description:In organisms ranging from vertebrates to plants, major components of centromeres are rapidly-evolving repeat sequences, such as tandem repeats (TRs) and transposable elements (TEs). These repeats harbor centromere-specific histone H3 (CENH3), which also evolves rapidly. Complete centromere structures recently determined in human and Arabidopsis suggest frequent integration and purging of retrotransposons within the TR regions of centromeres. Despite the high impact of “centrophilic” retrotransposons on the paradox of rapid centromere evolution, the mechanisms involved in centromere targeting remain poorly understood in any organism. Here we show that both Ty3 and Ty1/Copia LTR elements rapidly turnover within the centromeric TRs of Arabidopsis species. We demonstrate that the Ty1/Copia element Tal1 (Transposon of Arabidopsis lyrata 1) integrates de novo into regions occupied by CENH3 in A. thaliana, and that ectopic expansion of the CENH3 region results in spread of Tal1 integration regions. The integration spectra of chimeric TEs revealed the key structural variations responsible for the contrasting chromatin targeting specificities to centromeres versus gene-rich regions, which have recurrently converted during the evolution of these TEs. Our findings reveal the impact of centromeric chromatin on TE-mediated rapid centromere evolution, with relevance across eukaryotic genomes.
2024-08-08 | GSE263224 | GEO
Project description:Centromeres are essential to ensure proper chromosome segregation in eukaryotes. Their definition relies on the presence of a centromere-specific H3 histone variant CenH3, known as CENP-A in mammals. Its overexpression in aggressive cancers raises questions concerning its effect on chromatin dynamics and contribution to tumorigenesis. We find that CenH3 overexpression in human cells leads to ectopic enrichment at sites of active histone turnover. Furthermore, in over-expressing conditions, we see the formation of a novel heterotypic particle (CenH3-H4/H3.3-H4) that occludes CTCF binding, but this occlusion has only a minor effect on gene expression. Ectopic localization and CTCF occlusion depends on the H3.3 chaperone DAXX, rather than its dedicated chaperone HJURP. This DAXX-dependent occlusion also occurs in naturally overexpressing cancer cells. Furthermore, our cellular model reveals a DAXX-dependent survival advantage when challenged by DNA damage. Our findings illustrate how changes in histone variant levels can disrupt chromatin dynamics in disease and provides a possible mechanism for cell resistance to anti-cancer treatments. Examination of CenH3 ChIP-seq and RNA-seq transcriptional programs in two conditions - WT and CenH3 over-expressing.
2014-02-12 | E-GEOD-42951 | biostudies-arrayexpress
Project description:To determine the centromere of the maize B chromosome, we used previously published anti-CENH3-ChIP-seq data from TB-9Sb, which contain a complete functional B centromere. Distribution of centromere-specific DNA repeats, including CentC, CRM element and B-repeat, were observed in the proximal end of the assembled maize B chromosome, and this region was shown to be associated with CENH3 nucleosomes. Furthermore, six small scaffolds with sizes ranging from 10 to 174 kilobase display CENH3 enrichment, also with the distribution of these repeat sequences. These results were consistent with previously cytogenetic observation. Therefore, approximately 520 kb centromeric regions were determined in the assembled maize B chromosome.
2021-05-22 | GSE152074 | GEO
Project description:Centromeres are essential to ensure proper chromosome segregation in eukaryotes. Their definition relies on the presence of a centromere-specific H3 histone variant CenH3, known as CENP-A in mammals. Its overexpression in aggressive cancers raises questions concerning its effect on chromatin dynamics and contribution to tumorigenesis. We find that CenH3 overexpression in human cells leads to ectopic enrichment at sites of active histone turnover. Furthermore, in over-expressing conditions, we see the formation of a novel heterotypic particle (CenH3-H4/H3.3-H4) that occludes CTCF binding, but this occlusion has only a minor effect on gene expression. Ectopic localization and CTCF occlusion depends on the H3.3 chaperone DAXX, rather than its dedicated chaperone HJURP. This DAXX-dependent occlusion also occurs in naturally overexpressing cancer cells. Furthermore, our cellular model reveals a DAXX-dependent survival advantage when challenged by DNA damage. Our findings illustrate how changes in histone variant levels can disrupt chromatin dynamics in disease and provides a possible mechanism for cell resistance to anti-cancer treatments.
2014-02-12 | GSE42951 | GEO