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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.


The PSR chromosome is devoid of H3K27me1 but not H3K9me2,3 and H4K20me1.(A) chromosome spread showing the five normal chromosomes in the N. vitripennis genome (top of panel) and the PSR chromosome (bottom of panel, in white box). Right panels show a higher magnification of the PSR chromosome from left panel, hybridized with a DNA FISH probe that highlights a satellite sequence that is present across most of the larger arm (green arrowhead) and in a small region on the shorter arm (white arrowhead). (B,C,D) PSR stained for the three histone marks H3K9me2,3, H3K27me1, and H4K20me1, respectively. Middle and far right column are higher magnifications of PSR, with the middle panels depicting the histone mark and PSR FISH probe. The far right panels show the same images without the PSR FISH probe in order to clearly visualize whether PSR contains a given histone mark. PSR is circumscribed (white line) in middle and bottom rows for clarity. Scale bar equals 12 μM.
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f6: The PSR chromosome is devoid of H3K27me1 but not H3K9me2,3 and H4K20me1.(A) chromosome spread showing the five normal chromosomes in the N. vitripennis genome (top of panel) and the PSR chromosome (bottom of panel, in white box). Right panels show a higher magnification of the PSR chromosome from left panel, hybridized with a DNA FISH probe that highlights a satellite sequence that is present across most of the larger arm (green arrowhead) and in a small region on the shorter arm (white arrowhead). (B,C,D) PSR stained for the three histone marks H3K9me2,3, H3K27me1, and H4K20me1, respectively. Middle and far right column are higher magnifications of PSR, with the middle panels depicting the histone mark and PSR FISH probe. The far right panels show the same images without the PSR FISH probe in order to clearly visualize whether PSR contains a given histone mark. PSR is circumscribed (white line) in middle and bottom rows for clarity. Scale bar equals 12 μM.

Mentions: Any of the three perturbed histone marks on the PCM, or a combination of them, could play a role in blockage of chromosome resolution and paternal genome loss. Because PSR is excluded from this effect, we speculated that PSR would likely avoid any such histone mark alteration(s). To test this possibility, we closely scrutinized the PSR chromosome during metaphase, the time when all three perturbed histone marks are clearly visible on the PCM. In particular, we were able to clearly highlight the PSR chromosome by hybridization with a probe that recognizes repeat sequences that span most of PSR’s long arm and a small region on its short arm (Fig. 6). H3K9me2,3 appeared to be at levels on PSR that are higher than those present on the PCM but comparable to levels present on the pericentromeric regions of the maternal chromosomes (Fig. 6). However, strikingly, very low levels of H3K27me1 and H4K20me1 were present on PSR during the first mitotic division (Fig. 6). Thus, PSR has the unusual ability to largely exclude itself from these two marks. This finding implicates H3K27me1 and H4K20me1 as important, perhaps in conjunction with H3K9me2,3, for subsequent H3S10p and Condensin misbehavior. Additionally, largely reduced levels of H3K27me1 and H4K20me1 on PSR likely help it to resolve and segregate properly during the first mitosis, thereby avoiding self-elimination.


A ‘ selfish ’ B chromosome induces genome elimination by disrupting the histone code in the jewel wasp Nasonia vitripennis
The PSR chromosome is devoid of H3K27me1 but not H3K9me2,3 and H4K20me1.(A) chromosome spread showing the five normal chromosomes in the N. vitripennis genome (top of panel) and the PSR chromosome (bottom of panel, in white box). Right panels show a higher magnification of the PSR chromosome from left panel, hybridized with a DNA FISH probe that highlights a satellite sequence that is present across most of the larger arm (green arrowhead) and in a small region on the shorter arm (white arrowhead). (B,C,D) PSR stained for the three histone marks H3K9me2,3, H3K27me1, and H4K20me1, respectively. Middle and far right column are higher magnifications of PSR, with the middle panels depicting the histone mark and PSR FISH probe. The far right panels show the same images without the PSR FISH probe in order to clearly visualize whether PSR contains a given histone mark. PSR is circumscribed (white line) in middle and bottom rows for clarity. Scale bar equals 12 μM.
© Copyright Policy - open-access
Related In: Results  -  Collection

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f6: The PSR chromosome is devoid of H3K27me1 but not H3K9me2,3 and H4K20me1.(A) chromosome spread showing the five normal chromosomes in the N. vitripennis genome (top of panel) and the PSR chromosome (bottom of panel, in white box). Right panels show a higher magnification of the PSR chromosome from left panel, hybridized with a DNA FISH probe that highlights a satellite sequence that is present across most of the larger arm (green arrowhead) and in a small region on the shorter arm (white arrowhead). (B,C,D) PSR stained for the three histone marks H3K9me2,3, H3K27me1, and H4K20me1, respectively. Middle and far right column are higher magnifications of PSR, with the middle panels depicting the histone mark and PSR FISH probe. The far right panels show the same images without the PSR FISH probe in order to clearly visualize whether PSR contains a given histone mark. PSR is circumscribed (white line) in middle and bottom rows for clarity. Scale bar equals 12 μM.
Mentions: Any of the three perturbed histone marks on the PCM, or a combination of them, could play a role in blockage of chromosome resolution and paternal genome loss. Because PSR is excluded from this effect, we speculated that PSR would likely avoid any such histone mark alteration(s). To test this possibility, we closely scrutinized the PSR chromosome during metaphase, the time when all three perturbed histone marks are clearly visible on the PCM. In particular, we were able to clearly highlight the PSR chromosome by hybridization with a probe that recognizes repeat sequences that span most of PSR’s long arm and a small region on its short arm (Fig. 6). H3K9me2,3 appeared to be at levels on PSR that are higher than those present on the PCM but comparable to levels present on the pericentromeric regions of the maternal chromosomes (Fig. 6). However, strikingly, very low levels of H3K27me1 and H4K20me1 were present on PSR during the first mitotic division (Fig. 6). Thus, PSR has the unusual ability to largely exclude itself from these two marks. This finding implicates H3K27me1 and H4K20me1 as important, perhaps in conjunction with H3K9me2,3, for subsequent H3S10p and Condensin misbehavior. Additionally, largely reduced levels of H3K27me1 and H4K20me1 on PSR likely help it to resolve and segregate properly during the first mitosis, thereby avoiding self-elimination.

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.