Molecular cytogenetic dissection of human chromosomes 3 and 21 evolution

Abstract

Chromosome painting in placental mammalians illustrates that genome evolution is marked by chromosomal synteny conservation and that the association of chromosomes 3 and 21 may be the largest widely conserved syntenic block known for mammals. We studied intrachromosomal rearrangements of the syntenic block 3͞21 by using probes derived from chromosomal subregions with a resolution of up to 10 -15 Mbp. We demonstrate that the rearrangements visualized by chromosome painting, mostly translocations, are only a fraction of the actual chromosomal changes that have occurred during evolution. The ancestral segment order for both primates and carnivores is still found in some species in both orders. From the ancestral primate͞carnivore condition an inversion is needed to derive the pig homolog, and a fission of chromosome 21 and a pericentric inversion is needed to derive the Bornean orangutan condition. Two overlapping inversions in the chromosome 3 homolog then would lead to the chromosome form found in humans and African apes. This reconstruction of the origin of human chromosome 3 contrasts with the generally accepted scenario derived from chromosome banding in which it was proposed that only one pericentric inversion was needed. From the ancestral form for Old World primates (now found in the Bornean orangutan) a pericentric inversion and centromere shift leads to the chromosome ancestral for all Old World monkeys. Intrachromosomal rearrangements, as shown here, make up a set of potentially plentiful and informative markers that can be used for phylogenetic reconstruction and a more refined comparative mapping of the genome.

Recurrent Sites for New Centromere Seeding

“…1). The 3/21 association is well established in LCA (Cardone et al 2002) and in mammals (Muller et al 2000;Murphy et al 2001). In NWMs, the association of markers G, F, and chromosome 21 sequences form a separate chromosome (GF21 in Fig.…”

“…The evolution of chromosome 3 has been investigated by Muller et al (2000), who have already noted centromere position inconsistencies between OWM and great apes. Their assumption that the Bornean orangutan chromosome 3 arrangement was shared by a Catarrhini ancestor is not supported by the present analysis.…”

High-resolution comparative chromosome painting in the Arizona collared peccary (Pecari tajacu, Tayassuidae): a comparison with the karyotype of pig and sheep

“…The high number of small sheep chromosomes (2n = 54) compared to the in general larger pig chromosomes (2n = 38) made it possible to use these paints also as subregional probes and to delineate various intra-chromosomal rearrangements in the pig karyotype (Froenicke & Wienberg 2001). This approach has been successfully used in other species to define subregional homologies between and within members of various mammalian taxa (Yang et al 1999, Mü ller et al 2000, Murphy et al 2003, Biltueva et al 2004). …”

Hemiplasy and homoplasy in the karyotypic phylogenies of mammals

“…Syntenic blocks involving entire chromosomes, chromosomal arms, or large chromosomal segments are sometimes shared across even distantly-related mammalian species. Standard wisdom is that each such syntenic block is of monophyletic origin, because the independent assembly of a shared synteny in different lineages seems mechanistically highly implausible (14). In other words, shared syntenic associations are much more useful in defining clades than chromosomal reorganizations that disrupt an ancestral synteny, because the latter might recur by means of breakpoint reuse (15)(16)(17)(18), especially in regions of segmental duplications (19), high concentrations of repetitive elements, and fragile sites (18,20,21).…”