The subtelomeric region is important for chromosome recognition and pairing during meiosis

Abstract

The process of meiosis results in the formation of haploid daughter cells, each of which inherit a half of the diploid parental cells' genetic material. The ordered association of homologues (identical chromosomes) is a critical prerequisite for a successful outcome of meiosis. Homologue recognition and pairing are initiated at the chromosome ends, which comprise the telomere dominated by generic repetitive sequences, and the adjacent subtelomeric region, which harbours chromosome-specific sequences. In many organisms telomeres are responsible for bringing the ends of the chromosomes close together during early meiosis, but little is known regarding the role of the subtelomeric region sequence during meiosis. Here, the observation of homologue pairing between a pair of Hordeum chilense chromosomes lacking the subtelomeric region on one chromosome arm indicates that the subtelomeric region is important for the process of homologous chromosome recognition and pairing.

Figure 1. In situ hybridisation-based detection of telomeres and the H. chilense chromosome 3H^ch subtelomeric regions in addition line root tip metaphase spreads.

(a) The line carrying the version of chromosome 3H^ch in which a deletion on the long arm has removed neither the long arm telomere nor the subtelomeric region, (b) the line carrying the version of chromosome 3H^ch in which a deletion on the short arm has removed the subtelomeric region. The 3H^ch chromosomes (indicated by a white arrow) can be distinguished by the presence of signal following hybridisation with HvT01, as confirmed by probing with labelled H. chilense genomic DNA. Bar: 10 µm.

Figure 2. The behaviour of the chromosome 3H^ch homologues during pachytene.

Telomeres, subtelomeric regions (first line) and centromeres (second line) of the two homologues are indicated by a white arrow. Solid and broken lines in the diagrams represent the paired and unpaired regions of the homologous chromosomes, respectively. (a) In the line carrying the version of chromosome 3H^ch in which a deletion on the long arm has removed neither the long arm telomere nor the subtelomeric region, the two homologues are fully paired, while (b) in the line carrying the version of chromosome 3H^ch in which a deletion on the short arm has removed the subtelomeric region, they are only associated along the distal region of the long arm, leaving the centromeric region and the short arm unpaired. (c) At a later stage during meiosis, pairing is extended in the line carrying the version of chromosome 3H^ch in which a deletion on the short arm has removed the subtelomeric region. The homologues are fully associated along their long arm and the pairing signal has been transmitted through the centromeres, although the short arms remain largely unpaired. (d) At an even later stage, the homologues become fully associated. Bar: 10 µm.

Figure 3. The behaviour of the chromosome 3H^ch homologues (labelled by genomic in situ hybridisation) during metaphase I.

(a) In the line carrying the version of chromosome 3H^ch in which a deletion on the long arm has removed neither the long arm telomere nor the subtelomeric region, the homologues form a ring bivalent (see inset), reflecting chiasma formation on both arms.(b) In the line carrying the version of chromosome 3H^ch in which a deletion on the short arm has removed the subtelomeric region, a rod bivalent forms, reflecting the lack of chiasma formation on the short arm (arrowed). Scale bar 10 µm.

Figure 4. Immunolocalisation of ZYP1, MLH1 and CENH3 in the pachytene meiocyte of the line carrying the version of chromosome 3H^ch in which a deletion on the short arm has removed the subtelomeric region (the same preparations were assayed as described in Fig. 2d).

(a) ZYP1 is deposited along the synapsed homologues chromosomes, even in the short arm of the barley chromosome (green arrow) were the subtelomeric region is absent. (b) Foci of MLH1 deposition only show along the long arms having the subtelomeric region (red arrow). The large red signals relate to sites of CENH3 deposition and mark the centromere. (c) A merged image of (a) and (b). Bar: 10 µm.