Centromere repositioning

Abstract

Primate pericentromeric regions recently have been shown to exhibit extraordinary evolutionary plasticity. In this paper we report an additional peculiar feature of these regions that we discovered while analyzing, by FISH, the evolutionary conservation of primate phylogenetic chromosome IX. If the position of the centromere is not taken into account, a relatively small number of rearrangements must be invoked to account for interspecific differences. Conversely, if the centromere is included, a paradox emerges: The position of the centromere seems to have undergone, in some species, an evolutionary history independent from the surrounding markers. A significant number of additional rearrangements must be proposed to reconcile the order of the markers with centromere position. Alternatively, the evolutionary emergence of neocentromeres can be postulated.

Figure 1

Examples of DAPI-banded phylogenetic chromosome IX from each species under study (a). Chromosome IX in AGE, SSC, and CJA is part of a larger chromosome. In all cases, however, the chromosome IX is uninterrupted. Brackets indicate the portion of chromosome IX. Some chromosomes are presented in an inverted orientation, with respect to the position of the centromere, to match the orientation reported in Fig. 2. The actual chromosome number in each species is reported on the right of the species acronym. (b) FISH signal of the 12 probes on human chromosome 9. The examples have been arranged from left to right in increasing mapping distance from 9pter. (c) Example of FISH signals (green) of PCP 29, specific for human 9q, on PCR (left) and SSC (right). (d) Example of a cohybridization experiment performed to establish the relative order of probes M (red) and N (green) in PCR and CMO. The DAPI-banded chromosome IX without signals is on the left, to better show the morphology and centromere position. (e) The splitting of probe B in PTR and CJA (see text). The arrows point to the centromere.

Figure 2

The diagram schematically summarizes the results obtained by hybridizing the 12 markers on each species under study. GGO and PPY turned out to be identical and have been grouped together. Regions homologous to the human 9p (red) and 9q (green) are shown on the left of each ideogram, indicating the G-banding pattern (right). The cytogenetic material not detailed from different chromosome(s) present in AGE, SSC, and CJA is in brown. Close horizontal lines indicate heterochromatin blocks. The hypothesized pericentric or paracentirc inversions are indicated by square parentheses spanning the inverted cytogenetic segment. The split signals of marker B (YAC 945F5) are indicated as B′ and B′′. In both cases, signal of B′′ is much stronger than that of B′ (see text and Fig. 1e).

Figure 3

Schematical description of the most parsimonious series of hypothetical rearrangements that would be needed to reconcile the observed marker order and the position of the centromeres. These rearrangements are based on the assumption that the centromere in PCA was positioned telomeric to marker A. This conclusion is drawn exclusively from the constraint imposed by the maximum parsimony. The inversions are indicated by brackets. The inversions not present in Fig. 2 have been specifically introduced to account for the paradoxal position of the centromere. In AGE and SSC the centromere is positioned at the boundary between chromosome IX and the chromosome segment brought there by an interchromosomal rearrangement. We cannot exclude the possibility that the centromere of these two species has originated from a different chromosome. The orientation of the chromosomes has been reported to match the orientation reported in Fig. 2.