The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons

Braasch, Ingo; Gehrke, Andrew R.; Smith, Jeramiah J.; Kawasaki, Kazuhiko; Manousaki, Tereza; Pasquier, Jérémy; Amores, Angel; Desvignes, Thomas; Batzel, Peter; Catchen, Julian M.; Berlin, Aaron M.; Campbell, Michael S.; Barrell, Daniel; Martin, Kyle J.; Mulley, John F.; Ravi, Vydianathan; Lee, Alison; Nakamura, Tetsuya; Chalopin, Domitille; Fan, Shaohua; Wcisel, Dustin J.; Cañestro, Cristian; Sydes, Jason; Beaudry, Felix E.G.; Sun, Yi; Hertel, Jana; Beam, Michael J.; Fasold, Mario; Ishiyama, Mikio; Johnson, Jeremy; Kehr, Stephanie; Lara, Marcia; Letaw, John; Litman, Gary W.; Litman, Ronda T.; Mikami, Masato; Ota, Toshitaka; Saha, Nil Ratan; Williams, Louise; Stadler, Peter F.; Wang, Han; Taylor, John S.; Fontenot, Quenton; Ferrara, Allyse; Searle, Stephen M. J.; Aken, Bronwen; Yandell, Mark; Schneider, Igor; Yoder, Jeffrey A.; Volff, Jean‐Nicolas; Meyer, Axel; Amemiya, Chris T.; Venkatesh, Byrappa; Holland, Peter; Guiguen, Yann; Bobe, Julien; Shubin, Neil H.; Palma, Federica Di; Alföldi, Jessica; Lindblad‐Toh, Kerstin; Postlethwait, John H.

doi:10.1038/ng.3526

Cited by 538 publications

(795 citation statements)

References 129 publications

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“…In chondrichthyans, we identified only two genes in the available transcriptomics and genomics data: the SPARC orthologue and one paralogue which we refer here as SPARC-L (formerly coined SPARC-L1 [60]). In the elephant shark genome, SPARC-L is located in a region of conserved synteny compared to the osteichthyan SPARC-L1/SPARC-L2 locus [5, 36, 61]. Our phylogenetic analyses support the notion that the chondrichthyan SPARC-L clade is the sister-group to the osteichthyan SPARC-L1/SPARC-L2 clade (Fig.…”

Section: Discussionsupporting

confidence: 75%

Evolution of dental tissue mineralization: an analysis of the jawed vertebrate SPARC and SPARC-L families

et al. 2018

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BackgroundThe molecular bases explaining the diversity of dental tissue mineralization across gnathostomes are still poorly understood. Odontodes, such as teeth and body denticles, are serial structures that develop through deployment of a gene regulatory network shared between all gnathostomes. Dentin, the inner odontode mineralized tissue, is produced by odontoblasts and appears well-conserved through evolution. In contrast, the odontode hypermineralized external layer (enamel or enameloid) produced by ameloblasts of epithelial origin, shows extensive structural variations. As EMP (Enamel Matrix Protein) genes are as yet only found in osteichthyans where they play a major role in the mineralization of teeth and others skeletal organs, our understanding of the molecular mechanisms leading to the mineralized odontode matrices in chondrichthyans remains virtually unknown.ResultsWe undertook a phylogenetic analysis of the SPARC/SPARC-L gene family, from which the EMPs are supposed to have arisen, and examined the expression patterns of its members and of major fibrillar collagens in the spotted catshark Scyliorhinus canicula, the thornback ray Raja clavata, and the clawed frog Xenopus tropicalis. Our phylogenetic analyses reveal that the single chondrichthyan SPARC-L gene is co-orthologous to the osteichthyan SPARC-L1 and SPARC-L2 paralogues. In all three species, odontoblasts co-express SPARC and collagens. In contrast, ameloblasts do not strongly express collagen genes but exhibit strikingly similar SPARC-L and EMP expression patterns at their maturation stage, in the examined chondrichthyan and osteichthyan species, respectively.ConclusionsA well-conserved odontoblastic collagen/SPARC module across gnathostomes further confirms dentin homology. Members of the SPARC-L clade evolved faster than their SPARC paralogues, both in terms of protein sequence and gene duplication. We uncover an osteichthyan-specific duplication that produced SPARC-L1 (subsequently lost in pipidae frogs) and SPARC-L2 (independently lost in teleosts and tetrapods).Our results suggest the ameloblastic expression of the single chondrichthyan SPARC-L gene at the maturation stage reflects the ancestral gnathostome situation, and provide new evidence in favor of the homology of enamel and enameloids in all gnathostomes.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1241-y) contains supplementary material, which is available to authorized users.

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Section: Discussionsupporting

confidence: 75%

Evolution of dental tissue mineralization: an analysis of the jawed vertebrate SPARC and SPARC-L families

et al. 2018

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“…we used the spotted gar genome 72 to identify orthologous predicted enhancers. We downloaded human-spotted gar pairwise chain alignments and used our custom-made zebrafish-spotted gar pairwise chain alignments to respectively map human and zebrafish predicted enhancers on to the spotted gar genome.…”

Section: Defining Orthologous Enhancers and Target Genes Between Humanmentioning

confidence: 99%

Enhancer-gene maps in the human and zebrafish genomes using evolutionary linkage conservation

Clément

Torbey

Gilardi-Hebenstreit

et al. 2018

Preprint

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Gene regulation by enhancer sequences controls the spatiotemporal expression of target genes, often over long genomic distances. Current methods used to identify these interactions in the human genome require complex experimental setups and are restricted to specific cell types. Here we use PEGASUS, an approach that captures evolutionary signals 5 of synteny conservation to predict such interaction potentially in any biological context. We apply it to the human and zebrafish genomes and exploit the 1.3 million human and 55,000 zebrafish enhancers that we predicted to uncover fundamental principles of gene enhancer function in vertebrates. We show that the number of enhancers linked to a gene positively correlates with expression breadth in space and time and that the enhancer-target distance 10 is evolutionarily neutral. We uncover almost 2000 regulatory interactions ancestral to vertebrates, which are strongly enriched in core developmental processes. Using PEGASUS and its evolutionary view of enhancer-gene interactions, we provide a highly complementary resource to functional assays which uncovers key principles of enhancer biology.

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“…S1, S2, S4, S5) thought to be retained from the tsWGD. In particular, our new analyses, in contrast to past work considering teleost IGFBPs (Ocampo-Daza et al, 2011;Macqueen et al, 2013), included the spotted gar as a ray-finned fish outgroup to tsWGD (Braasch et al, 2016) -this species invariably branched with maximal statistical support outside two teleost IGFBP clades ('A' and 'B′ nomenclature), with all ray-finned fish being sister to a monophyletic clade of lobe-finned fish (Fig. 4, Fig.…”

Section: Phylogenetic Validation Of Sequence Capture Approach For Rebmentioning

confidence: 63%

Targeted sequencing for high-resolution evolutionary analyses following genome duplication in salmonid fish: Proof of concept for key components of the insulin-like growth factor axis

2016

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High-throughput sequencing has revolutionised comparative and evolutionary genome biology. It has now become relatively commonplace to generate multiple genomes and/or transcriptomes to characterize the evolution of large taxonomic groups of interest. Nevertheless, such efforts may be unsuited to some research questions or remain beyond the scope of some research groups. Here we show that targeted high-throughput sequencing offers a viable alternative to study genome evolution across a vertebrate family of great scientific interest. Specifically, we exploited sequence capture and Illumina sequencing to characterize the evolution of key components from the insulin-like growth (IGF) signalling axis of salmonid fish at unprecedented phylogenetic resolution. The IGF axis represents a central governor of vertebrate growth and its core components were expanded by whole genome duplication in the salmonid ancestor ~95Ma. Using RNA baits synthesised to genes encoding the complete family of IGF binding proteins (IGFBP) and an IGF hormone (IGF2), we captured, sequenced and assembled orthologous and paralogous exons from species representing all ten salmonid genera. This approach generated 299 novel sequences, most as complete or near-complete protein-coding sequences. Phylogenetic analyses confirmed congruent evolutionary histories for all nineteen recognized salmonid IGFBP family members and identified novel salmonid-specific IGF2 paralogues. Moreover, we reconstructed the evolution of duplicated IGF axis paralogues across a replete salmonid phylogeny, revealing complex historic selection regimes - both ancestral to salmonids and lineage-restricted - that frequently involved asymmetric paralogue divergence under positive and/or relaxed purifying selection. Our findings add to an emerging literature highlighting diverse applications for targeted sequencing in comparative-evolutionary genomics. We also set out a viable approach to obtain large sets of nuclear genes for any member of the salmonid family, which should enable insights into the evolutionary role of whole genome duplication before additional nuclear genome sequences become available.

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The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons

Cited by 538 publications

References 129 publications

Evolution of dental tissue mineralization: an analysis of the jawed vertebrate SPARC and SPARC-L families

Evolution of dental tissue mineralization: an analysis of the jawed vertebrate SPARC and SPARC-L families

Enhancer-gene maps in the human and zebrafish genomes using evolutionary linkage conservation

Targeted sequencing for high-resolution evolutionary analyses following genome duplication in salmonid fish: Proof of concept for key components of the insulin-like growth factor axis

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