Integration of the Genetic Map and Genome Assembly of Fugu Facilitates Insights into Distinct Features of Genome Evolution in Teleosts and Mammals

Abstract

The compact genome of fugu (Takifugu rubripes) has been used widely as a reference genome for understanding the evolution of vertebrate genomes. However, the fragmented nature of the fugu genome assembly has restricted its use for comparisons of genome architecture in vertebrates. To extend the contiguity of the assembly to the chromosomal level, we have generated a comprehensive genetic map of fugu and anchored the scaffolds of the assembly to the 22 chromosomes of fugu. The map consists of 1,220 microsatellite markers that provide anchor points to 697 scaffolds covering 86% of the genome assembly (http://www.fugu-sg.org/). The integrated genome map revealed a higher recombination rate in fugu compared with other vertebrates and a wide variation in the recombination rate between sexes and across chromosomes of fugu. We used the extended assembly to explore recent rearrangement events in the lineages of fugu, Tetraodon, and medaka and compared them with rearrangements in three mammalian (human, mouse, and opossum) lineages. Between the two pufferfishes, fugu has experienced fewer chromosomal rearrangements than Tetraodon. The gene order is more highly conserved in the three teleosts than in mammals largely due to a lower rate of interchromosomal rearrangements in the teleosts. These results provide new insights into the distinct patterns of genome evolution between teleosts and mammals. The consolidated genome map and the genetic map of fugu are valuable resources for comparative genomics of vertebrates and for elucidating the genetic basis of the phenotypic diversity of ∼25 species of Takifugu that evolved within the last 5 My.

Constructing Genetic Linkage Maps Using the Whole Genome Sequence of Pacific Bluefin Tuna (<i>Thunnus orientalis</i>) and a Comparison of Chromosome Structure among Teleost Species

“…The numbers of linkage groups on the sex-specific maps agreed with the number of chromosome pairs suggested from microscopic observations [9]. Scaffolds integrated with linkage groups will have to be detected on chromosome samples using fluorescence in situ hybridization to reveal the relationships between linkage groups and chromosomes, as in other fish [12] [36]. It is also desirable to locate scaffolds or contigs that include unique repeats in telomeric or centromeric regions.…”

“…These studies suggest that the medaka genome has the conserved genomic structure of the MTZ ancestor (the last common ancestor of three fishes, medaka, Tetraodon, and zebrafish) and no major chromosomal rearrangements have occurred for more than 300 million years (My) [4] [25], whereas the zebrafish genome has experienced many interchromosomal rearrangements during evolution due to extensive translocations. A comparative genome study of fugu supported their hypothesis and discussed inter-chromosomal rearrangements in the fugu and Tetraodon lineages [12]. Tongue sole also experienced three major chromosomal fusion events after divergence from the common ancestor with medaka, Tetraodon, and fugu [26].…”

“…The draft genome sequence of this species is highly fragmented, and constructing a genetic linkage map is an effective way to link the sequence fragments. Genetic linkage maps have been used as an anchor for fish [11] [12], plants [13]- [16], and domestic animals [17]. A genetic linkage map is constructed by developing genetic markers on scaffolds and examining the linkage relationships between the markers.…”

Chromosome evolution in fishes: a new challenging proposal from Neotropical species

“…This indicates the stability of the genome of these fishes over long evolutionary time scales (Guyomard et al, 2012;Schartl et al, 2013). In addition a higher conserved gene order was observed in fishes than in mammals by genome comparison of three teleost species (fugu, Tetraodon, and medaka) with those of three mammalian lineages (human, mouse, and opossum), and authors reported these results as "largely due to a lower rate of interchromosomal rearrangements in the teleosts" (Kai et al, 2011).…”

Construction and Characterization of a Repetitive DNA Library in Parodontidae (Actinopterygii: Characiformes): A Genomic and Evolutionary Approach to the Degeneration of the W Sex Chromosome

“…38 Thus, numerous studies identified and physically mapped repetitive sequences to assist in the organization of chromosomal regions rich in repetitive DNA, particularly in heteromorphic sex chromosomes. [39][40][41] C o t-1 DNA is a useful tool to isolate highly and moderately repetitive DNAs, according to Ferreira and Martins 42 and Zhang et al 43 In this study, we described different types of repetitive sequences isolated from the Parodontidae C o t-1 library: satellite DNAs, minisatellite DNAs, microsatellite DNAs, DNA transposons, and retrotransposons. Physical mapping of the total C o t-1 probe revealed locations in the terminal regions of some autosomes, as well as in the proximal region of the short arm of the Z chromosome and in the long arm of the W chromosome of the Apareiodon sp.…”