Protein immunolocalization supports the presence of identical mechanisms of XY body formation in eutherians and marsupials

Abstract

The meiotic sex chromosomes of the American marsupials Monodelphis dimidiata and Didelphis albiventris were studied with electron microscopy (EM) and with immunofluorescence localization of meiotic proteins SYCP1 and SYCP3, and proteins essential for meiotic sex chromosome inactivation (MSCI), gamma-H2AX and BRCA1. The chromatin of the non-synaptic X and Y chromosomes contains gamma-H2AX, first as foci and then as homogeneous staining at late stages. The thick and split X and Y axes are labelled with BRCA1 except at one terminus. The bulgings of the axes contain SYCP1 as well as the inner side of the dense plate. The evenly spaced and highly packed chromatin fibres of the conjoined XY body in these species have the same behaviour and the same components (gamma-H2AX in the chromatin, BRCA1 in the axes) as in the XY body of eutherian species. These observations and recent data from the literature suggest that XY body formation is ancestral to the metatherian-eutherian divergence.

The XY Body of the Cat (<b><i>Felis catus</i></b>): Structural Differentiations and Protein Immunolocalization

“…The latter structural localization has been previously reported in other mammalian species in normal conditions (in marsupials [Page et al, 2006b;Franco et al, 2007]), in null-mutant mouse models having mutations of cohesin-complex genes, in which SYCP1 is illegitimately found between sister-chromatid axes in univalent chromosomes [reviewed in Biswas et al, 2016], and in non-meiotic cells when transfected with SYCP1 (and SYCE3) constructs [Öllinger et al, 2005;Hernández-Hernández et al, 2016]. On the basis of these observations, we suggest that the presence of SYCP1 foci at the bulged, split regions of the X axis containing SYCP3 is not related to the assembly of a functional SC, but instead to the affinity of specific domains of both proteins that associate under the steric, proper conditions.…”

“…The localization of special SYCP3-containing structures connecting the X and Y chromosome axes during the pachytene and later stages of first meiosis has already been observed in other mammals (in marsupials [Page et al, 2003;Franco et al, 2007]; in gerbils [de la Fuente et al, 2007;Franco, 2012]). In marsupials, the lack of a homologous region in the X and Y chromosomes [Hore et al, 2007] results in the abolition of a typical SC and a regular chiasma between them.…”

“…It has been reported in marsupials [Solari and Bianchi, 1975;Franco et al, 2007], in armadillos [Sciurano et al, 2006[Sciurano et al, , 2012, and in rodents [del Mazo and Gil-Alberdi, 1986;Koykul and Basrur, 1995;Echeverría et al, 2003;Sciurano et al, 2013]. However, the functional significance of these splittings remains largely unknown.…”

Two-Step Imprinted X Inactivation: Repeat versus Genic Silencing in the Mouse

“…The absence of a marsupial Xist suggests that an alternative means of silencing the X must occur in mammals. Since the discovery of meiotic sex chromosome inactivation (MSCI) in the male germ line of both eutherian and marsupial mammals (14,23,32,43,58), several groups have hypothesized a link between MSCI and the imprinting of X P (10,24,26,35,39). Recent reports that XY silencing persists into the long postmeiotic period of spermatogenesis (16,42,62) support the idea that zygotic X P silencing is built in part on MSCI and its aftereffects in the paternal germ line.…”

The great escape

“…the same time that XY chromosomes emerged after the divergence of the therian ancestor from the monotreme lineage. 2 Indeed, MSCI occurs in marsupials, [22][23][24] and its underlying mechanism has been conserved throughout the course of evolution. Accumulating evidence has revealed a significant influence of meiotic sex chromosome inactivation (MSCI) on the evolution of the genome in terms of gene contents and expression.…”