The effect of heterochromatin on synapsis of the sex chromosomes of <i>Peromyscus </i>(Rodentia, Cricetidae)

Abstract

The pairing behavior of the sex chromosomes in male and female individuals representing seven species of Peromyscus was analyzed by electron microscopy of silver-stained zygotene and pachytene configurations. Six species possess submetacentric or metacentric X chromosomes with heterochromatic short arms. Sex-chromosome pairing in these species is initiated during early pachynema at an interstitial position on the X and Y axes. Homologous synapsis then progresses in a unidirectional fashion towards the telomeres of the X short arm and the corresponding arm of the heterochromatic Y chromosome. The distinctive pattern of synaptic initiation allowed a late-synapsing bivalent in fetal oocytes to be tentatively identified as that of the X chromosomes. In contrast to the other species, Peromyscus megalops possesses an acrocentric X chromosome and a very small Y chromosome. Sex-chromosome pairing in this species is initiated at the proximal telomeric region during late zygonema, and then proceeds interstitially towards the distal end of the Y chromosome. These observations suggest that the presence of X short-arm heterochromatin and corresponding Y heterochromatin interferes with late-zygotene alignment of the pairing initiation sites, thereby delaying XY synaptic initiation until early pachynema. The pairing initiation sites are conserved in the vicinity of the X and Y centromeres in Peromyscus, and consequently the addition of heterochromatin during sex-chromosome evolution essentially displaces these sites to an interstitial position.

Synaptonemal complex karyotype of the pachytene spermatocytes and oocytes of the Turkish hamster (Mesocricetus brandti)

“…These variations can be seen as loss of SC formation in the XY (SELUJA et al 1984), loss of pairing (SoLARI and BIANCHI 1975) or even delay in XY synaptic initiation (HALE 1991). In the present study, the presence of two forms of the X chromosome, a submetacentric Xt and a metacentric X2 as well as of the Y chromosome, a submetacentric Y 1 and a metacentric Y 2 produced the complex pairing of the sex bivalents.…”

The analysis of synaptonemal complex formation inTrichomys apereoides(Rodentia, Echimyidae) with detailed XY pairing

“…Some examples of total pairing of Y and X axes have been observed but in these cases there was interstitial initiation synapsis (SCHMID et al 1987;HALE et al 1991), as well as the occurrence of initiation sites of XY synapsis at terminal regions with partial synapsis between the X andY axes . Generally, sex chromosomes synapse to form a length of SC along homologous segments (MosES et al 1979;SoLARI 1988;DAI et al 1994).…”

“…Generally, sex chromosomes synapse to form a length of SC along homologous segments (MosES et al 1979;SoLARI 1988;DAI et al 1994). In some cases, theY chromosome synapses overall with part of the X (SCHMID et al 1987;HALE et al 1991). In other cases, there is a lack of true synapsis between the sex chromosomes (SoLARI and BIANCHI 1975;CARNERO et al 1991).…”

Sex Chromosomes, Heterochromatin, and Retrotransposon Accumulation in Deer Mice

“…In Peromyscus, the heterochromatic short arm ofthe X chromosome and a corresponding arm of the heterochromatic Y chromosome comprise the pseudoautosomal region (Hale and Greenbaum, 1986;Sudman and Greenbaum, 1990;Hale et al, 1991;Fig. I).…”

“…While the euchromatic portion of the X chromosomes is invariant among Peromyscus species, the size of the heterochromatic short arm is highly variable. The size of the Y chromosome, as well as the relative lengths of its pseudoautosomal and Y-specific arms, are extremely variable among deer mouse species (Hale et al, 1991, and references therein).…”