Robertsonian chromosomes and the nuclear architecture of mouse meiotic prophase spermatocytes

Abstract

BackgroundThe nuclear architecture of meiotic prophase spermatocytes is based on higher-order patterns of spatial associations among chromosomal domains from different bivalents. The meiotic nuclear architecture depends on the chromosome characteristics and consequently is prone to modification by chromosomal rearrangements. In this work, we consider Mus domesticus spermatocytes with diploid chromosome number 2n = 40, all telocentric, and investigate a possible modification of the ancestral nuclear architecture due to the emergence of derived Rb chromosomes, which may be present in the homozygous or heterozygous condition.ResultsIn the 2n = 40 spermatocyte nuclei random associations mediated by pericentromeric heterochromatin among the 19 telocentric bivalents ocurr at the nuclear periphery. The observed frequency of associations among them, made distinguishable by specific probes and FISH, seems to be the same for pairs that may or may not form Rb chromosomes. In the homozygote Rb 2n = 24 spermatocytes, associations also mediated by pericentromeric heterochromatin occur mainly between the three telocentric or the eight metacentric bivalents themselves. In heterozygote Rb 2n = 32 spermatocytes all heterochromatin is localized at the nuclear periphery, yet associations are mainly observed among the three telocentric bivalents and between the asynaptic axes of the trivalents.ConclusionsThe Rb chromosomes pose sharp restrictions for interactions in the 2n = 24 and 2n = 32 spermatocytes, as compared to the ample possibilities for interactions between bivalents in the 2n = 40 spermatocytes. Undoubtedly the emergence of Rb chromosomes changes the ancestral nuclear architecture of 2n = 40 spermatocytes since they establish new types of interactions among chromosomal domains, particularly through centromeric and heterochromatic regions at the nuclear periphery among telocentric and at the nuclear center among Rb metacentric ones.

The Robertsonian phenomenon in the house mouse: mutation, meiosis and speciation

“…d, e Similar configurations are shown by quadrivalents meiosis, as shown for the recurrent reciprocal translocation t(11;22)(q23;q11) in humans (Ashley et al 2006). With regards meiosis in mice, the formation of new Rb fusions may occur during prophase I at the nuclear periphery between pericentromeric regions of telocentrics or in the nuclear interior with respect to WARTs between metacentric chromosomes (Berríos et al 2014). In summary, the architectural features together with the intense DNA nicking and repair activity (Neale and Keeney 2006) of first meiotic prophase can set the stage for new chromosome interactions and create the conditions for new chromosomal rearrangements.…”

“…This attempted pairing and its aftermath may lead to meiotic defects that include delayed and incomplete synapsis, heterologous interactions with other chromosomes and malsegregation during the first meiotic anaphase (Eaker et al 2001;Hauffe and Searle 1998;Johannisson and Winking 1994;Navarro et al 1991;Wallace et al 1992;Castiglia and Capanna 2000;Wallace et al 2002). More recently, other factors such as the alteration of the nuclear architecture or the disruption of the epigenetic programme during meiosis have also been considered as causes of meiotic breakdown in heterozygotes (Berríos et al 2014;Burgoyne et al 2009;Garagna et al 2001b;Homolka et al 2007;Kouznetsova et al 2009;Mahadevaiah et al 2008).…”

“…Additionally, the mechanical constraints induced by the semirigid nature of the SC may have an influence. Since the telocentrics and the metacentrics occupy different nuclear spaces, the synapsis of the trivalents (or quadrivalents) necessarily involves the movement of the metacentrics to the nuclear periphery as synapsis proceeds (Berríos et al 2014;Fernández-Donoso et al 2001). Thus, overcoming the physical resistance of trivalents and other multivalents against bending maybe an additional cause of delay in the completion of synapsis.…”

“…4a). First, the pericentromeric regions of metacentrics are mainly located in the nuclear interior, forming only a few chromocentres (two to three in spermatocytes carrying 2n=26 chromosomes) (Berríos et al 2014). Second, only the pericentromeric regions of telocentric chromosomes remain close to the nuclear periphery.…”

Chromatin Organization and Remodeling of Interstitial Telomeric Sites During Meiosis in the Mongolian Gerbil (Meriones unguiculatus)

“…Instead, we propose this could be a remnant of a previous evolutionary state of metacentric chromosomes. The three point attachment figures observed in squashed spermatocytes resemble those displayed by trivalents in Rb heterozygote mice (Berrios et al 2014). Considering that metacentric chromosomes in M. unguiculatus were most likely originated by Rb translocations (Benazzou et al 1982;Dobigny et al 2003), it emerges that this capability may be reminiscent of a (recent?)…”