Sequencing of Supernumerary Chromosomes of Red Fox and Raccoon Dog Confirms a Non-Random Gene Acquisition by B Chromosomes

Abstract

B chromosomes (Bs) represent a variable addition to the main karyotype in some lineages of animals and plants. Bs accumulate through non-Mendelian inheritance and become widespread in populations. Despite the presence of multiple genes, most Bs lack specific phenotypic effects, although their influence on host genome epigenetic status and gene expression are recorded. Previously, using sequencing of isolated Bs of ruminants and rodents, we demonstrated that Bs originate as segmental duplications of specific genomic regions, and subsequently experience pseudogenization and repeat accumulation. Here, we used a similar approach to characterize Bs of the red fox (Vulpes vulpes L.) and the Chinese raccoon dog (Nyctereutes procyonoides procyonoides Gray). We confirm the previous findings of the KIT gene on Bs of both species, but demostrate an independent origin of Bs in these species, with two reused regions. Comparison of gene ensembles in Bs of canids, ruminants, and rodents once again indicates enrichment with cell-cycle genes, development-related genes, and genes functioning in the neuron synapse. The presence of B-chromosomal copies of genes involved in cell-cycle regulation and tissue differentiation may indicate importance of these genes for B chromosome establishment.

Keywords: genome instability; karyotype evolution; supernumerary chromosomes.

Figure 1

The region encompassing protooncogene KIT is present on B chromosomes (Bs) of the fox (VVUB2, 3, 5 and 6) and raccoon dog (NPPB1-8) visualized in UCSC genome browser (http://genome.ucsc.edu/). Coordinates are given for the dog (CanFam3.1) genome.

Figure 2

Numbers of additional copies for B chromosomal regions (identified by isolated chromosome sequencing) estimated based on whole-genome sequencing of the red fox individual with three Bs. Region parts with different copy numbers counted separately. Regions with copy number below three were lost from some of Bs, while regions with copy number above three were amplified within Bs. X—number of additional copies, Y—counts of regions.