Coelacanth genome sequence reveals the evolutionary history of vertebrate genes

Abstract

The coelacanth is one of the nearest living relatives of tetrapods. However, a teleost species such as zebrafish or Fugu is typically used as the outgroup in current tetrapod comparative sequence analyses. Such studies are complicated by the fact that teleost genomes have undergone a whole-genome duplication event, as well as individual gene-duplication events. Here, we demonstrate the value of coelacanth genome sequence by complete sequencing and analysis of the protocadherin gene cluster of the Indonesian coelacanth, Latimeria menadoensis. We found that coelacanth has 49 protocadherin cluster genes organized in the same three ordered subclusters, ␣, ␤, and ␥, as the 54 protocadherin cluster genes in human. In contrast, whole-genome and tandem duplications have generated two zebrafish protocadherin clusters comprised of at least 97 genes. Additionally, zebrafish protocadherins are far more prone to homogenizing gene conversion events than coelacanth protocadherins, suggesting that recombination-and duplication-driven plasticity may be a feature of teleost genomes. Our results indicate that coelacanth provides the ideal outgroup sequence against which tetrapod genomes can be measured. We therefore present L. menadoensis as a candidate for whole-genome sequencing.[Supplemental material is available online at www.genome.org and http://www-shgc.stanford.edu/myerslab/. The BAC sequence data from this study have been submitted to GenBank under accession nos. AC150283, AC150284, and AC150308-AC150310.]A primary aim of vertebrate comparative genomics is to reconstruct the evolutionary history of vertebrate genomes. To this end, genome sequence is currently being obtained from organisms at critical positions in the vertebrate phylogeny. Notably absent from the list of planned or completed genomes, however, is a species on a lineage arising between ray-finned fishes and tetrapods, when vertebrates were about to undergo an adaptive transformation. The sarcopterygian fishes, coelacanths and lungfish, are the only extant taxa that occupy this unique phylogenetic position (Gorr et al. 1991;Zardoya andMeyer 1996, 1997). As the nearest living relatives of the tetrapod ancestor, these species provide access to the phenotypic and genomic transitions leading to the emergence of tetrapods.Despite substantial sequence analysis, it is unclear whether coelacanths or lungfish are more closely related to tetrapods (Takezaki et al. 2004). However, lungfish have very large genomes (>100 Gb), making them poor candidates for genomic sequencing. Coelacanths, although abundant in the fossil record, were believed to be extinct before a living specimen was identified in 1938 by Marjorie Latimer and J.L.B. Smith (Smith 1939). The two modern coelacanth species that are known, Latimeria chalumnae and Latimeria menadoensis, are remarkably similar to their fossil relatives, showing little morphological change over 360 million years (Smith 1939;Forey 1998;Holder et al. 1999). In addition, the L. menadoensis genome is smaller than the human or mouse ...

Coelacanth genomes reveal signatures for evolutionary transition from water to land

“…In addition, the likelihood-ratio test confirmed that the branch length for coelacanths is significantly shorter than those of the three other vertebrates (P < 0.01; Supplemental Information 6.1). Our data provide genome-wide confirmation of previous studies that used a small number of selected gene sets (Noonan et al 2004;Amemiya et al 2010;Higasa et al 2012).…”

“…The evolutionary rate of the coelacanth genome has been debated for many years (Noonan et al 2004;Amemiya et al 2010;Higasa et al 2012). With the entire genome available, we first compared a set of 5247 orthologous genes for coelacanth and four other vertebrates-human, chicken, frog, and zebrafish-and then constructed a maximum-likelihood tree to evaluate the difference in evolutionary rates among vertebrates (Fig.…”

Evolution of GPCR: Change and continuity

“…An additional whole genome duplication may have occurred in the teleost lineage after its split from the tetrapod lineage, from which only a subset has been retained in modern teleost genomes [64]. Coelacanth, that is considered a close relative to tetrapods, however shows no evidence for whole genome duplication [65]. It is interesting that after whole genome duplication events, nonchemosensory GPCR genes were retained with a higher probability than expected [66].…”

Elephant shark sequence reveals unique insights into the evolutionary history of vertebrate genes: A comparative analysis of the protocadherin cluster

“…It is composed of tandem arrays of paralogous genes that are highly susceptible to lineage-specific gene losses, tandem duplications, and gene conversion (2)(3)(4)(5)(6)(7). These clustered genes are distinct from nonclustered protocadherin genes by possessing a large coding exon that codes for the entire extracellular domain, the transmembrane domain, and a small portion of the cytoplasmic domain, whereas the extracellular domain of the nonclustered protocadherins is usually encoded by multiple exons (8).…”