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A ‘ selfish ’ B chromosome induces genome elimination by disrupting the histone code in the jewel wasp Nasonia vitripennis

View Article: PubMed Central - PubMed

ABSTRACT

Intragenomic conflict describes a phenomenon in which genetic elements act ‘selfishly’ to gain a transmission advantage at the expense of the whole genome. A non-essential, selfish B chromosome known as Paternal Sex Ratio (PSR) induces complete elimination of the sperm-derived hereditary material in the jewel wasp Nasonia vitripennis. PSR prevents the paternal chromatin from forming chromosomes during the first embryonic mitosis, leading to its loss. Although paternally transmitted, PSR evades self-elimination in order to be inherited. We examined important post-translational modifications to the DNA packaging histones on the normal genome and the PSR chromosome in the fertilized embryo. Three histone marks – H3K9me2,3, H3K27me1, and H4K20me1 – became abnormally enriched and spread to ectopic positions on the sperm’s chromatin before entry into mitosis. In contrast, other histone marks and DNA methylation were not affected by PSR, suggesting that its effect on the paternal genome is specific to a subset of histone marks. Contrary to the paternally derived genome, the PSR chromosome was visibly devoid of the H3K27me1 and H4K20me1 marks. These findings strongly suggest that PSR causes paternal genome elimination by disrupting at least three histone marks following fertilization, while PSR avoids self-elimination by evading two of these marks.

No MeSH data available.


Acetylated histone H4 patterns are normal in PSR-carrying embryos.In wild type embryos, histone H4 acetylated at multiple Lysine residues is absent from the sperm’s chromatin immediately after fertilization. However, H4ac appears on the paternal chromatin as the sperm and egg nuclei migrate toward one another (pre-juxtaposition); the maternal nucleus and meiotic products (not shown) already show H4ac. This signal increases slightly more on the paternal set compared to the female set during metaphase, but by the end of the first mitosis both daughter nuclei contain similar levels of H4ac. In PSR-carrying embryos the patterns are indistinguishable. The paternal chromatin mass (PCM, indicated by white arrowhead in the bottom right panel) contains the same level of H4ac as the maternally derived nuclei (red arrowheads). PSR is highlighted by a sequence-specific FISH probe (green in panels of the bottom two rows). Scale bar equals 5 μM in the top left panel and 12 μM in the adjacent panel to the right, under pre-juxtaposition. p and m stand for paternal and maternal nuclei.
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f2: Acetylated histone H4 patterns are normal in PSR-carrying embryos.In wild type embryos, histone H4 acetylated at multiple Lysine residues is absent from the sperm’s chromatin immediately after fertilization. However, H4ac appears on the paternal chromatin as the sperm and egg nuclei migrate toward one another (pre-juxtaposition); the maternal nucleus and meiotic products (not shown) already show H4ac. This signal increases slightly more on the paternal set compared to the female set during metaphase, but by the end of the first mitosis both daughter nuclei contain similar levels of H4ac. In PSR-carrying embryos the patterns are indistinguishable. The paternal chromatin mass (PCM, indicated by white arrowhead in the bottom right panel) contains the same level of H4ac as the maternally derived nuclei (red arrowheads). PSR is highlighted by a sequence-specific FISH probe (green in panels of the bottom two rows). Scale bar equals 5 μM in the top left panel and 12 μM in the adjacent panel to the right, under pre-juxtaposition. p and m stand for paternal and maternal nuclei.

Mentions: We began by examining the pattern of acetylated histone H4 because in D. melanogaster this mark is one of the first to appear on the paternal chromatin as it becomes remodeled with conventional histones15. In wild type embryos, H4ac was present on the egg’s meiotic products (not shown) but not on the highly elongated sperm nucleus (Fig. 2). This mark began to appear on the paternal chromatin as the two nuclei migrated toward one another; at this time the sperm’s nucleus widened into a more oval-like shape, also indicative of chromatin remodeling (Fig. 2)16. During juxtaposition, H4ac became equally intense on both nuclei (Fig. 2). During metaphase this mark appeared slightly brighter on the paternal set, which could be identified as faintly more condensed than the maternal set (Fig. 2). However, at the end of this first mitotic division, the two diploid daughter nuclei appeared indistinguishable in H4ac intensity (Fig. 2). In PSR-carrying embryos, the H4ac patterns were very similar to those in wild type. Additionally, the H4ac mark was visibly indistinguishable between the paternal chromatin mass and the maternally derived nuclei at the end of the first mitosis (Fig. 2). Thus, PSR does not visibly affect H4ac on the paternal half of the genome. Normal behavior of this mark and the passage of the paternal set through the first S-phase7 indirectly suggest that protamine removal occurs properly. Additionally, we conclude that, because the antibody used to detect H4ac recognizes multiple acetylated Lysine residues on histone H4, it is likely that each of these individual marks are largely unperturbed by PSR.


A ‘ selfish ’ B chromosome induces genome elimination by disrupting the histone code in the jewel wasp Nasonia vitripennis
Acetylated histone H4 patterns are normal in PSR-carrying embryos.In wild type embryos, histone H4 acetylated at multiple Lysine residues is absent from the sperm’s chromatin immediately after fertilization. However, H4ac appears on the paternal chromatin as the sperm and egg nuclei migrate toward one another (pre-juxtaposition); the maternal nucleus and meiotic products (not shown) already show H4ac. This signal increases slightly more on the paternal set compared to the female set during metaphase, but by the end of the first mitosis both daughter nuclei contain similar levels of H4ac. In PSR-carrying embryos the patterns are indistinguishable. The paternal chromatin mass (PCM, indicated by white arrowhead in the bottom right panel) contains the same level of H4ac as the maternally derived nuclei (red arrowheads). PSR is highlighted by a sequence-specific FISH probe (green in panels of the bottom two rows). Scale bar equals 5 μM in the top left panel and 12 μM in the adjacent panel to the right, under pre-juxtaposition. p and m stand for paternal and maternal nuclei.
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Related In: Results  -  Collection

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f2: Acetylated histone H4 patterns are normal in PSR-carrying embryos.In wild type embryos, histone H4 acetylated at multiple Lysine residues is absent from the sperm’s chromatin immediately after fertilization. However, H4ac appears on the paternal chromatin as the sperm and egg nuclei migrate toward one another (pre-juxtaposition); the maternal nucleus and meiotic products (not shown) already show H4ac. This signal increases slightly more on the paternal set compared to the female set during metaphase, but by the end of the first mitosis both daughter nuclei contain similar levels of H4ac. In PSR-carrying embryos the patterns are indistinguishable. The paternal chromatin mass (PCM, indicated by white arrowhead in the bottom right panel) contains the same level of H4ac as the maternally derived nuclei (red arrowheads). PSR is highlighted by a sequence-specific FISH probe (green in panels of the bottom two rows). Scale bar equals 5 μM in the top left panel and 12 μM in the adjacent panel to the right, under pre-juxtaposition. p and m stand for paternal and maternal nuclei.
Mentions: We began by examining the pattern of acetylated histone H4 because in D. melanogaster this mark is one of the first to appear on the paternal chromatin as it becomes remodeled with conventional histones15. In wild type embryos, H4ac was present on the egg’s meiotic products (not shown) but not on the highly elongated sperm nucleus (Fig. 2). This mark began to appear on the paternal chromatin as the two nuclei migrated toward one another; at this time the sperm’s nucleus widened into a more oval-like shape, also indicative of chromatin remodeling (Fig. 2)16. During juxtaposition, H4ac became equally intense on both nuclei (Fig. 2). During metaphase this mark appeared slightly brighter on the paternal set, which could be identified as faintly more condensed than the maternal set (Fig. 2). However, at the end of this first mitotic division, the two diploid daughter nuclei appeared indistinguishable in H4ac intensity (Fig. 2). In PSR-carrying embryos, the H4ac patterns were very similar to those in wild type. Additionally, the H4ac mark was visibly indistinguishable between the paternal chromatin mass and the maternally derived nuclei at the end of the first mitosis (Fig. 2). Thus, PSR does not visibly affect H4ac on the paternal half of the genome. Normal behavior of this mark and the passage of the paternal set through the first S-phase7 indirectly suggest that protamine removal occurs properly. Additionally, we conclude that, because the antibody used to detect H4ac recognizes multiple acetylated Lysine residues on histone H4, it is likely that each of these individual marks are largely unperturbed by PSR.

View Article: PubMed Central - PubMed

ABSTRACT

Intragenomic conflict describes a phenomenon in which genetic elements act ‘selfishly’ to gain a transmission advantage at the expense of the whole genome. A non-essential, selfish B chromosome known as Paternal Sex Ratio (PSR) induces complete elimination of the sperm-derived hereditary material in the jewel wasp Nasonia vitripennis. PSR prevents the paternal chromatin from forming chromosomes during the first embryonic mitosis, leading to its loss. Although paternally transmitted, PSR evades self-elimination in order to be inherited. We examined important post-translational modifications to the DNA packaging histones on the normal genome and the PSR chromosome in the fertilized embryo. Three histone marks – H3K9me2,3, H3K27me1, and H4K20me1 – became abnormally enriched and spread to ectopic positions on the sperm’s chromatin before entry into mitosis. In contrast, other histone marks and DNA methylation were not affected by PSR, suggesting that its effect on the paternal genome is specific to a subset of histone marks. Contrary to the paternally derived genome, the PSR chromosome was visibly devoid of the H3K27me1 and H4K20me1 marks. These findings strongly suggest that PSR causes paternal genome elimination by disrupting at least three histone marks following fertilization, while PSR avoids self-elimination by evading two of these marks.

No MeSH data available.