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Biology subjects

Oel, A. P.

Publications and source records attributed to Oel, A. P..

6 recordsLinked to original sources

A whole-body cell type atlas mapped into an electron microscopy volume of an annelid worm

Differential gene expression establishes the distinct physiology and morphology of cell types in an animal body. Single-cell sequencing and volume EM represent milestones toward the characterization of cell types, yet are difficult to combine for a comprehensive view on the cellular genotype-phenotype link. Here, we map a whole-body single-cell transcriptome into the PlatyBrowser, a multimodal cellular atlas for the marine annelid Platynereis dumerilii, and establish this combination uniquely for an entire animal. We learn that, in the 6-days-old worm, the majority of genes are tightly co-regulated to jointly implement one of eight major cellular morphotypes representing epidermis, gut, vasculature, myofibres, glia, motile cilia, glands, or neurons. Focusing on neurons, we uncover 14 families that by transcription factor identity, axonal projection, or sensory-secretory apparatus resemble conserved neuron types found in vertebrates, insects, or nematodes. We hypothesize that these existed in urbilaterian ancestors and represent the ancient core of nervous system centralization.

evolutionary biology↗

Comparative analysis of convergent jellyfish eyes reveals extensive differences in expression of vision-related genes

Quantifying gene expression across convergent origins of traits clarifies the degree to which those traits arise from shared versus distinct genetic programs, revealing how gene re-use relates to the repeatability of evolution. Eyes are important traits that evolved in many distantly related lineages, including at least nine times within cnidarians. Here, we investigate gene expression in eye-bearing and non-visual tissues from three cnidarian species representing long-diverged lineages where eyes evolved convergently (Cubozoa, Scyphozoa, and Hydrozoa). We find gene expression in eye-bearing tissues to be mostly lineage-specific, with only a small proportion of genes having convergent expression across species. Nevertheless, all species express homologs of deeply conserved vision-related genes known from Bilateria, which likely reflects deep homology (parallel evolution across vast phylogenetic distances) of a metazoan phototransduction toolkit. A gene tree analysis of opsins--the prototypical animal photosensors--shows that convergent eyes recruited different opsin paralogs, with the potential exception of an opsin ortholog shared between scyphozoan and cubozoan eyes. Our results suggest that eyes have mostly lineage-specific patterns of gene expression, yet some key phototransduction components are repeatedly recruited across multiple independent eye origins in Medusozoa.

evolutionary biology↗

Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas

The vertebrate brain emerged more than [~]500 million years ago in common evolutionary ancestors. To systematically trace its cellular and molecular origins, we established a spatially resolved cell type atlas of the entire brain of the sea lamprey - a jawless species whose phylogenetic position affords the reconstruction of ancestral vertebrate traits - based on extensive single-cell RNA-seq and in situ sequencing data. Comparisons of this atlas to neural data from the mouse and other jawed vertebrates unveiled various shared features that enabled the reconstruction of the core cell type composition, tissue structures, and gene expression programs of the ancestral brain. However, our analyses also revealed key tissues and cell types that arose later in evolution. For example, the ancestral vertebrate brain was likely devoid of cerebellar cell types and oligodendrocytes (myelinating cells); our data suggest that the latter emerged from astrocyte-like evolutionary precursors on the jawed vertebrate lineage. Our work illuminates the cellular and molecular architecture of the ancestral vertebrate brain and provides a foundation for exploring its diversification during evolution.

evolutionary biology↗

Nrl is dispensable for specification of rod photoreceptors in adult zebrafish contrasting a deeply conserved requirement earlier in ontogeny

The transcription factor NRL (Neural Retinal Leucine-zipper) has been canonized, appropriately enough, as the master regulator of photoreceptor cell fate in the retina. NRL is necessary and sufficient to specify rod cell fate and to preclude cone cell fate in mice. By engineering zebrafish we tested if NRL function has conserved roles beyond mammals or beyond nocturnal species, i.e. in a vertebrate possessing a greater and more typical diversity of cone sub-types. Here, transgenic expression of a Nrl homolog from zebrafish or mouse was sufficient to convert developing zebrafish cones into rod photoreceptors. Zebrafish nrl-/- mutants lacked rods (and had excess UV-sensitive cones) as young larvae, thus the conservation of Nrl function between mice and zebrafish appears sound. These data inform hypotheses of photoreceptor evolution through the Nocturnal Bottleneck, suggesting that a capacity to favor nocturnal vision is a property of NRL that predates the emergence of early mammals. Strikingly, however, rods were abundant in adult nrl-/- null mutant zebrafish. Rods developed in adults despite Nrl protein being undetectable. Therefore a yet-to-be-revealed non-canonical pathway independent of nrl is able to specify the fate of some rod photoreceptors.Highlights- Nrl is conserved and sufficient to specify rod photoreceptors in zebrafish retina- Nrl is necessary for rod photoreceptors in early ontogeny of zebrafish larvae- Zebrafish Nrl is functionally conserved with mouse and human NRL- Remarkably, Nrl is dispensable for rod specification in adult zebrafishCompeting Interest StatementThe authors have declared no competing interest.View Full Text

developmental biology↗

Characterization of eyes, photoreceptors and opsins in developmental stages of the chaetognath Spadella cephaloptera

The phylogenetic position of chaetognaths has been debated for decades, however recently they have been grouped into the Gnathifera, sister taxon to the Lophotrochozoa. Chaetognaths possess photoreceptor cells that are anatomically unique and arranged remarkably different in the eyes of the various species. Studies investigating eye development and underlying gene regulatory networks are so far missing. In order to gain insights into the development and the molecular toolkit of chaetognath photoreceptors and eyes a new transcriptome of the epibenthic species Spadella cephaloptera was searched for opsins. Our screen revealed single-copies of xenopsin and peropsin and gene expression analyses demonstrated that only xenopsin is expressed in photoreceptor cells of the developing lateral eyes. Adults likewise exhibit two xenopsin+ photoreceptor cells in each of their lateral eyes. Beyond that, a single cryptochrome gene was uncovered and found co-expressed with xenopsin in some photoreceptor cells of the lateral developing eye. In addition, it is co-expressed with peropsin in the cerebral ganglia, a condition reminiscent of a non-visual photoreceptive zone in the apical nervous system of the annelid Platynereis dumerilii that performs circadian entrainment and melatonin release. Cryptochrome expression was also detected in cells of the corona ciliata, a circular organ in the posterior dorsal head region that has been attributed several functions arguing for an involvement of this organ in circadian entrainment. Our study demonstrates the importance to investigate representatives of the Gnathifera, a clade that has been neglected with respect to developmental studies and that might contribute to unravel the evolution of spiralian and bilaterian body plans.

zoology↗

nkx3.2 mutant zebrafish accommodate the jaw joint loss through a phenocopy of the head shapes of Paleozoic agnathans

The vertebrate jaw is a versatile feeding apparatus that facilitated explosive diversification. To function, it requires a joint between the upper and lower jaws, so jaw joint defects - such as osteoarthritis or even ankylosis - are often highly disruptive and difficult to study. To describe consequences of jaw-joint dysfunction, we engineered two independent null alleles of a single jaw-joint marker gene, nkx3.2, in zebrafish. These mutations caused zebrafish to become functionally jawless via fusion of the upper and lower jaw cartilages (ankylosis). Despite lacking jaw joints, nkx3.2 mutants survive to adulthood and accommodate this defect by: a) remodeling their skulls; and b) altering their behavior from suction feeding to ram feeding. As a result of remodeling, nkx3.2 mutants developed superficial similarities to the skull shapes observed in two lineages of ancient jawless vertebrates (anaspids and furcacaudiid thelodonts), including: a fixed open gape, reduced snout, and enlarged branchial region. However, no homology exists in individual skull elements between these taxa, and most of the modified elements in the mutant zebrafish occur outside known expression domains of nkx3.2. Therefore, we interpret the adult nkx3.2 phenotype not as a reversal to an ancestral state, but as convergence due to similar functional requirement of feeding without moveable jaws. This remarkable convergence strongly suggests that jaw movements themselves dramatically influence the development of jawed vertebrate skulls, which implies that functionally viable skull morphologies are finite, with or without functional jaws. Because nkx3.2 null zebrafish display prominent joint ankylosis, drastically modified skull shape, and altered feeding behaviors, these mutants provide a unique model with which to investigate mechanisms of skeletal remodeling and joint diseases.

evolutionary biology↗