Tracking genome organization in rodents by Zoo-FISH

Abstract

The number of rodent species examined by modern comparative genomic approaches, particularly chromosome painting, is limited. The use of human whole-chromosome painting probes to detect regions of homology in the karyotypes of the rodent index species, the mouse and rat, has been hindered by the highly rearranged nature of their genomes. In contrast, recent studies have demonstrated that non-murid rodents display more conserved genomes, underscoring their suitability for comparative genomic and higher-order systematic studies. Here we provide the first comparative chromosome maps between human and representative rodents of three major rodent lineages Castoridae, Pedetidae and Dipodidae. A comprehensive analysis of these data and those published for Sciuridae show (1) that Castoridae, Pedetidae and Dipodidae form a monophyletic group, and (2) that the European beaver Castor fiber (Castoridae) and the birch mouse Sicista betulina (Dipodidae) are sister species to the exclusion of the springhare Pedetes capensis (Pedetidae), thus resolving an enduring trifurcation in rodent higher-level systematics. Our results together with published data on the Sciuridae allow the formulation of a putative rodent ancestral karyotype (2n = 50) that is thought to comprise the following 26 human chromosomal segments and/or segmental associations: HSA1pq, 1q/10p, 2pq, 2q, 3a, 3b/19p, 3c/21, 4b, 5, 6, 7a, 7b/16p, 8p/4a/8p, 8q, 9/11, 10q, 12a/22a, 12b/22b, 13, 14/15, 16q/19q, 17, 18, 20, X and Y. These findings provide insights into the likely composition of the ancestral rodent karyotype and an improved understanding of placental genome evolution.

Chromosomal evolution in Rodentia

“…HSA 1/10 was not present in the Cavia karyotype. Finally, we conclude that the putative ancestral karyotype of Anomaluromorpha, Hystricomorpha, Myomorpha and Castorimorpha had a 2n¼60 (or 2n¼62 if the HSA 1/10 association in myomorphs and sciuromorphs is convergent) that consisted of HSA 1, 1/7, 1/10, 2, 2, 3, 3/19, 3/21, 4, 4, 4/8, 5, 5, 6, 6, 7, 8, 9/11, 10/16, 11, 12/22 (twice), 13, 14/15, 15, 16/ 19, 17, 18, 20, X and Y. The following rearrangements offer a striking confirmation of the close evolutionary relationship of Myomorpha and Castorimorpha: HSA 5/17 (it is absent in Mus and Rattus, but present in Sicista), HSA 11/15 and fission of HSA 14/15 (Graphodatsky et al, 2008). However, the use of different methods of analysis (DNA sequences for myomorph genomes and chromosome painting for castorimorphs) could give inconsistent results because of resolution differences of the analyses.…”

“…Castor fiber is the only species investigated by comparative chromosome painting (Beklemisheva et al, 2011). Characteristic placental associations such as HSA 7/16, 14/15, 16/19 (as well as some regarded as core to Glires, that is, HSA 1/ 10, 9/11) were not detected in the beaver genome supporting their placement (and that of the whole suborder) into a distinct clade (Supplement Data 3) (Graphodatsky et al, 2008).…”

“…There are no descriptions or comparisons of banded chromosomes between representatives of this group. The karyotype of only one species-Pedetes capensis-has been investigated using human painting probes (Graphodatsky et al, 2008). Surprisingly, some characteristic human chromosomal associations were not detected in P. capensis, that is, the HSA 7/16, and 16/19 as well as core glires HSA 1/10, 9/11 (Supplement Data 3).…”

“…An Ancestral Karyotype of Rodentia (RAK) was proposed (Graphodatsky et al, 2008) that suggested the associations HSA 8/12 and 15/20 may define rodents. Originally, HSA 1/10p and 9/11 were considered ancestral for Glires (the cohort combining Rodentia and Lagomorpha).…”

“…The fusion HSA 8/12 (resulting in the HSA 8/ 4/8/12/22 association) could be the single rearrangement distinguishing the Ancestral Sciuromorpha Karyotype from RAK. All sciurids share following associations: HSA 1/8, 2/17, 7/22, 10/13, 15/20 (Richard et al, 2003;Li et al, 2004Li et al, , 2006aGraphodatsky et al, 2008;Beklemisheva et al, 2011). Thus, only five fusions are needed to explain the derivation of the Sciuridae Ancestral Karyotype from that of the putative ancestral Sciuromorpha karyotype.…”