Genome Silencing and Elimination: Insights from a "Selfish" B Chromosome

Abstract

B chromosomes are non-essential components of numerous plant and animal genomes. Because many of these "extra" chromosomes enhance their own transmission in ways that are detrimental to the rest of the genome, they can be thought of as genome parasites. An extreme example is a paternally inherited B chromosome known as paternal sex ratio (PSR), which is found in natural populations of the jewel wasp Nasonia vitripennis. In order to ensure its own propagation, PSR severely biases the wasp sex ratio by converting diploid female-destined embryos into transmitting haploid males. This action occurs at the expense of the other paternally inherited chromosomes, which fail to resolve during the first round of division and are thus eliminated. Recent work has revealed that paternal genome elimination by PSR occurs through the disruption of a number of specific histone post-translational modifications, suggesting a central role for chromatin regulation in this phenomenon. In this review, we describe these recent advances in the light of older ones and in the context of what is currently understood about the molecular mechanisms of targeted genome silencing and elimination in other systems.

Keywords: B chromosome; Nasonia vitripennis; genome conflict; heterochromatin; histone modifications.

FIGURE 1

PSR-induced chromatin modifications in Nasonia vitripennis and other genome silencing or elimination events. (A) Schematic representation of histone post-translational modifications associated with PSR-induced genome elimination. In the center row, PSR is carried into the egg by the sperm. The two pronuclei come together and undergo one round of replication. As the two sets enter into the first mitosis, the maternal chromatin resolves normally into individual chromosomes while the paternal chromatin fails to resolve, becoming the paternal chromatin mass (PCM). The maternal chromosomes and the PSR chromosome, which is not blocked from resolving, segregate together, forming two haploid (1N) PSR+ nuclei. Top, a chromatin fiber from a region of euchromatin, which becomes phosphorylated at serine residue 10 of histone H3. This mark is associated with mitotic chromosome condensation (box in top right). Bottom, a chromatin fiber in euchromatin of the PCM. After fertilization, the paternal chromatin obtains abnormally high levels of di- and tri-methylated histone H3K9, mono-methylated histone H3K27, and mono-methylated histone H4K20. The H3S10p mark is also placed, but the combination of all four marks blocks normal chromosome resolution (box in bottom right). Chromatin marks that have been characterized on the Nasonia PCM are summarized in (B) along with what is known about these marks on the mammalian inactivated X chromosome (Barr body) (Hall and Lawrence, 2010) and the eliminated paternal chromosomes (EC) of Sciara (Goday and Ruiz, 2002; Greciano and Goday, 2006; Escribá et al., 2011). Symbols indicate that the specified modification is enriched (+), depleted (–), or unchanged (UC) on the eliminated or silenced chromosome(s) while “ND” indicates modifications for which there is no available data.

FIGURE 2

Hypothetical models for paternal genome elimination by PSR. (Top) The passive model for genome elimination in which PSR serves as a sink, titrating away one or more chromatin-associated factors that are critical for normal chromosome condensation and resolution. Depletion of these factors allows enzymes such as E(z), Su(var)3-9, and Pr-Set7 to abnormally modify regions of chromatin within the paternal pronucleus with marks such as H3K27me1, H3K9me2,3, and H4K20me1, respectively (also see Figure 1A). In the active model (Bottom), one or more PSR expressed factors actively interferes with the chromatin remodeling process. In this example, a PSR-expressed long non-coding RNA (lncRNA) associates with the euchromatin of the wasp’s normal chromosomes (but not PSR). There, these factors inappropriately recruit chromatin-modifying enzymes to these regions, marking the normal chromosomes for elimination. Either of these models could potentially take place during spermatogenesis or in the egg cytoplasm, immediately before the first embryonic mitosis.