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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.


Haplodiploidy and its alteration by PSR.(Top) Mated N. vitripennis females naturally fertilize ~80% of eggs, which develop as diploid female embryos from genetic contribution of the sperm and egg nuclei (blue and red dots, respectively). The unfertilized eggs develop as haploid male embryos, with genetic contribution from only the egg. (Bottom) Females when mated with PSR-carrying males still fertilize ~80% of their eggs. However, the sperm-contributed genome, which harbors the paternally-transmitted PSR chromosome (green dot), fails to condense into chromosomes during the first mitosis and is lost during subsequent divisions. In contrast, the PSR chromosome associates with the egg-derived chromatin and segregates successfully. These events convert all fertilized eggs, which should become female, into PSR-transmitting male embryos.
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f1: Haplodiploidy and its alteration by PSR.(Top) Mated N. vitripennis females naturally fertilize ~80% of eggs, which develop as diploid female embryos from genetic contribution of the sperm and egg nuclei (blue and red dots, respectively). The unfertilized eggs develop as haploid male embryos, with genetic contribution from only the egg. (Bottom) Females when mated with PSR-carrying males still fertilize ~80% of their eggs. However, the sperm-contributed genome, which harbors the paternally-transmitted PSR chromosome (green dot), fails to condense into chromosomes during the first mitosis and is lost during subsequent divisions. In contrast, the PSR chromosome associates with the egg-derived chromatin and segregates successfully. These events convert all fertilized eggs, which should become female, into PSR-transmitting male embryos.

Mentions: In order to better understand the nature of paternal genome elimination by PSR, we used fluorescent-based tools to microscopically visualize the dynamics of several key post-translational histone modifications in young wild type and PSR-carrying embryos. In haplodiploid reproduction, females lay a combination of fertilized and unfertilized eggs, which normally develop into females and males, respectively822 (Fig. 1). Because PSR-induced genome elimination only occurs in fertilized embryos (Fig. 1), we excluded from our analyses unfertilized embryos. Instead, we focused entirely on fertilized embryos. Additionally, we compared the pattern of each chromatin mark on the PSR-carrying paternal set relative to patterns on (i) the maternal set in the same PSR-carrying embryos and (ii) the paternal set in wild type embryos, both of which should show normal patterns.


A ‘ selfish ’ B chromosome induces genome elimination by disrupting the histone code in the jewel wasp Nasonia vitripennis
Haplodiploidy and its alteration by PSR.(Top) Mated N. vitripennis females naturally fertilize ~80% of eggs, which develop as diploid female embryos from genetic contribution of the sperm and egg nuclei (blue and red dots, respectively). The unfertilized eggs develop as haploid male embryos, with genetic contribution from only the egg. (Bottom) Females when mated with PSR-carrying males still fertilize ~80% of their eggs. However, the sperm-contributed genome, which harbors the paternally-transmitted PSR chromosome (green dot), fails to condense into chromosomes during the first mitosis and is lost during subsequent divisions. In contrast, the PSR chromosome associates with the egg-derived chromatin and segregates successfully. These events convert all fertilized eggs, which should become female, into PSR-transmitting male embryos.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5304203&req=5

f1: Haplodiploidy and its alteration by PSR.(Top) Mated N. vitripennis females naturally fertilize ~80% of eggs, which develop as diploid female embryos from genetic contribution of the sperm and egg nuclei (blue and red dots, respectively). The unfertilized eggs develop as haploid male embryos, with genetic contribution from only the egg. (Bottom) Females when mated with PSR-carrying males still fertilize ~80% of their eggs. However, the sperm-contributed genome, which harbors the paternally-transmitted PSR chromosome (green dot), fails to condense into chromosomes during the first mitosis and is lost during subsequent divisions. In contrast, the PSR chromosome associates with the egg-derived chromatin and segregates successfully. These events convert all fertilized eggs, which should become female, into PSR-transmitting male embryos.
Mentions: In order to better understand the nature of paternal genome elimination by PSR, we used fluorescent-based tools to microscopically visualize the dynamics of several key post-translational histone modifications in young wild type and PSR-carrying embryos. In haplodiploid reproduction, females lay a combination of fertilized and unfertilized eggs, which normally develop into females and males, respectively822 (Fig. 1). Because PSR-induced genome elimination only occurs in fertilized embryos (Fig. 1), we excluded from our analyses unfertilized embryos. Instead, we focused entirely on fertilized embryos. Additionally, we compared the pattern of each chromatin mark on the PSR-carrying paternal set relative to patterns on (i) the maternal set in the same PSR-carrying embryos and (ii) the paternal set in wild type embryos, both of which should show normal patterns.

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.