The bowfin genome illuminates the developmental evolution of ray-finned fishes

Thompson, Andrew; Hawkins, M. Brent; Parey, Elise; Wcisel, Dustin J.; Ota, Toshitaka; Kawasaki, Kazuhiko; Funk, Emily; Losilla, Mauricio; Fitch, Olivia; Pan, Qiaowei; Féron, Romain; Louis, Alexandra; Montfort, Jérôme; Milhes, Marine; Racicot, Brett; Childs, Kevin L.; Fontenot, Quenton; Ferrara, Allyse; David, Solomon R.; McCune, Amy R.; Dornburg, Alex; Yoder, Jeffrey A.; Guiguen, Yann; Crollius, Hugues Roest; Berthelot, Camille; Harris, Matthew P.; Braasch, Ingo

doi:10.1038/s41588-021-00914-y

Cited by 54 publications

(96 citation statements)

References 122 publications

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“…2b ). Noticeably, these two chromosomes are also preserved in their ancestral condition in the bowfin, the sister group of gar, implying that this fusion occurred specifically in the gar lineage 27 .…”

Section: Resultsmentioning

confidence: 94%

The little skate genome and the evolutionary emergence of wing-like fin appendages

Marlétaz

Calle‐Mustienes

Acemel

et al. 2022

Preprint

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Skates are cartilaginous fish whose novel body plan features remarkably enlarged wing-like pectoral fins that allow them to thrive in benthic environments. The molecular underpinnings of this unique trait, however, remain elusive. Here we investigate the origin of this phenotypic innovation by developing the little skate Leucoraja erinacea as a genomically enabled model. Analysis of a high-quality chromosome-scale genome sequence for the little skate shows that it preserves many ancestral jawed vertebrate features compared with other sequenced genomes, including numerous ancient microchromosomes. Combining genome comparisons with extensive regulatory datasets in developing fins (gene expression, chromatin occupancy and three-dimensional (3D) conformation) we find skate-specific genomic rearrangements that alter the 3D regulatory landscape of genes involved in the planar cell polarity (PCP) pathway. Functional inhibition of PCP signaling resulted in marked reduction of anterior fin size, confirming this pathway as a major contributor of batoid fin morphology. We also identified a fin-specific enhancer that interacts with 3' HOX genes, consistent with the redeployment of Hox gene expression in anterior pectoral fins, and confirmed the potential of this element to activate transcription in the anterior fin using zebrafish reporter assays. Our findings underscore the central role of genome reorganizations and regulatory variation in the evolution of phenotypes, shedding light on the molecular origin of an enigmatic trait.

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Section: Resultsmentioning

confidence: 94%

The little skate genome and the evolutionary emergence of wing-like fin appendages

Marlétaz

Calle‐Mustienes

Acemel

et al. 2022

Preprint

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“…Besides acipenseriforms, three non-teleost fish lineages have extant members that have been utilized in comparative embryological studies and have published genomes - bichirs (Polypteriformes), gars (Lepisosteiformes), and bowfins (Amiiformes) ( Askary et al, 2016 ; Braasch et al, 2016 ; Minarik et al, 2017 ; Stundl et al, 2019 ; Funk et al, 2020 ; Stundl et al, 2020 ; Thompson et al, 2021 ; Bi et al, 2021 ). While bichirs and bowfins are evolutionarily very attractive and informative species with unique morphologies, the main challenge in targeted mutagenesis in these organisms is obtaining zygotes for injection.…”

Section: Discussionmentioning

confidence: 99%

Efficient CRISPR Mutagenesis in Sturgeon Demonstrates Its Utility in Large, Slow-Maturing Vertebrates

Štundl

Soukup

Franěk

et al. 2022

Front. Cell Dev. Biol.

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In the last decade, the CRISPR/Cas9 bacterial virus defense system has been adapted as a user-friendly, efficient, and precise method for targeted mutagenesis in eukaryotes. Though CRISPR/Cas9 has proven effective in a diverse range of organisms, it is still most often used to create mutant lines in lab-reared genetic model systems. However, one major advantage of CRISPR/Cas9 mutagenesis over previous gene targeting approaches is that its high efficiency allows the immediate generation of near-null mosaic mutants. This feature could potentially allow genotype to be linked to phenotype in organisms with life histories that preclude the establishment of purebred genetic lines; a group that includes the vast majority of vertebrate species. Of particular interest to scholars of early vertebrate evolution are several long-lived and slow-maturing fishes that diverged from two dominant modern lineages, teleosts and tetrapods, in the Ordovician, or before. These early-diverging or “basal” vertebrates include the jawless cyclostomes, cartilaginous fishes, and various non-teleost ray-finned fishes. In addition to occupying critical phylogenetic positions, these groups possess combinations of derived and ancestral features not seen in conventional model vertebrates, and thus provide an opportunity for understanding the genetic bases of such traits. Here we report successful use of CRISPR/Cas9 mutagenesis in one such non-teleost fish, sterlet Acipenser ruthenus, a small species of sturgeon. We introduced mutations into the genes Tyrosinase, which is needed for melanin production, and Sonic hedgehog, a pleiotropic developmental regulator with diverse roles in early embryonic patterning and organogenesis. We observed disruption of both loci and the production of consistent phenotypes, including both near-null mutants’ various hypomorphs. Based on these results, and previous work in lamprey and amphibians, we discuss how CRISPR/Cas9 F0 mutagenesis may be successfully adapted to other long-lived, slow-maturing aquatic vertebrates and identify the ease of obtaining and injecting eggs and/or zygotes as the main challenges.

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“…In addition, FishmiRNA annotations rely on small RNA sequencing expression data to first, identify miRNA gene loci and second, to detect the most abundantly expressed mature miRNAs, leading to data-supported annotation of both the 5p and 3p strands for the majority of genes (76% across the database). The novel annotation of four teleost species and of the bowfin, Amia calva , a second holostean outgroup to the teleosts ( Thompson et al 2021 ), further increased confidence in the inferred TH-LCA miRNA gene repertoire and in intermediate teleost ancestors. This ancestral reconstruction approach, a cornerstone of the FishmiRNA database, allows the retracing of gene evolution across lineages.…”

Section: New Approachesmentioning

confidence: 93%

FishmiRNA: An Evolutionarily Supported MicroRNA Annotation and Expression Database for Ray-Finned Fishes

Desvignes

Bardou

Montfort

et al. 2022

Molecular Biology and Evolution

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microRNAs are important post-transcriptional regulators of gene expression involved in countless biological processes and are widely studied across metazoans. While miRNA research continues to grow, the large community of fish miRNA researchers lacks exhaustive resources consistent among species. To fill this gap, we developed FishmiRNA, an evolutionarily supported microRNA annotation and expression database for ray-finned fishes: www.fishmirna.org. The self-explanatory database contains detailed, manually-curated miRNA annotations with orthology relationships rigorously established by sequence similarity and conserved syntenies, and expression data provided for each detected mature miRNA. In just few clicks, users can download the annotation and expression database in several convenient formats either in its entirety or a subset. Simple filters and BLAST search options also permit the simultaneous exploration and visual comparison of expression data for up to any ten mature miRNAs across species and organs. FishmiRNA was specifically designed for ease of use to reach a wide audience.

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The bowfin genome illuminates the developmental evolution of ray-finned fishes

Cited by 54 publications

References 122 publications

The little skate genome and the evolutionary emergence of wing-like fin appendages

The little skate genome and the evolutionary emergence of wing-like fin appendages

Efficient CRISPR Mutagenesis in Sturgeon Demonstrates Its Utility in Large, Slow-Maturing Vertebrates

FishmiRNA: An Evolutionarily Supported MicroRNA Annotation and Expression Database for Ray-Finned Fishes

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