Impact of a selfish B chromosome on chromatin dynamics and nuclear organization in Nasonia

Abstract

Summary B chromosomes are centric chromosomal fragments present in thousands of eukaryotic genomes. Because most B chromosomes are non-essential, they can be lost without consequence. In order to persist, however, some B chromosomes can impose strong forms of intra-genomic conflict. An extreme case is the paternal sex ratio (PSR) B chromosome in the jewel wasp Nasonia vitripennis. Transmitted solely via the sperm, PSR 'imprints' the paternal chromatin so that it is destroyed during the first mitosis of the embryo. Owing to the haplo-diploid reproduction of N. vitripennis, PSR-induced loss of the paternal chromatin converts embryos that should become females into PSR-transmitting males. This conversion is key to the persistence of PSR, although the underlying mechanisms are largely unexplored. We assessed how PSR affects the paternal chromatin and then investigated how PSR is transmitted efficiently at the cellular level. We found that PSR does not affect progression of the paternal chromatin through the cell cycle but, instead, alters its normal Histone H3 phosphorylation and loading of the Condensin complex. PSR localizes to the outer periphery of the paternal nucleus, a position that we propose is crucial for it to escape from the defective paternal set. In sperm, PSR consistently localizes to the extreme anterior tip of the elongated nucleus, while the normal wasp chromosomes localize broadly across the nucleus. Thus, PSR may alter or bypass normal nuclear organizational processes to achieve its position. These findings provide new insights into how selfish genetic elements can impact chromatin-based processes for their survival.

Genome Silencing and Elimination: Insights from a “Selfish” B Chromosome

“…The first study of this kind addressed whether the PCM undergoes DNA replication (S-phase) and proper entry into the first mitotic division (Swim et al, 2012). By visualizing the active replication factor PCNA, it was found that the PCM successfully passes through the first S-phase.…”

“…As described above, paternal genome elimination involves alterations to the underlying chromatin structure (Swim et al, 2012; Aldrich et al, 2017). Generally speaking, one can imagine that PSR might exert this effect through either passive or active means ( Figure 2 ).…”

“…PSR is unique in this regard: it is transmitted to new progeny solely via sperm and therefore must counter its own loss by drastically altering the wasp’s sex ratio to produce all male broods. This effect is initiated soon after fertilization when all of the paternal chromosomes, with the exception of PSR itself, are eliminated as the mitotic divisions of early embryogenesis begin (Werren et al, 1981, 1987; Swim et al, 2012). Elimination of half the genome in many organisms would be lethal.…”

“…This effect results in complete loss of the PCM at this earliest developmental stage. Superficially the PCM resembles heterochromatin–the compact, transcriptionally silent portion of the interphase genome – because it undertakes a similarly bright cytologically condensed appearance when visualized with certain DNA stains (Reed, 1993; Swim et al, 2012). These characteristics raise a number of important questions regarding paternal genome elimination by PSR.…”

The Expanding Genetic Toolbox of the Wasp Nasonia vitripennis and Its Relatives

“…These tools also include the cellular and developmental genetics of pathologic interactions between Nasonia, its symbionts, and selfish genetic elements (Tram and Sullivan 2000;Ferree et al 2008;Swim et al 2012;Akbari et al 2013). In addition, Nasonia constitute an ideal model for understanding how parasitoids manipulate their hosts using a potent cocktail of biologically active molecules contained in venom (Danneels et al 2010;De Graaf et al 2010;Martinson et al 2014).…”