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Oliveri, P.

Publications and source records attributed to Oliveri, P..

7 recordsLinked to original sources

Monoaminergic neurons share transcriptional identity across Bilaterian animals

The evolutionary conservation of cell types over deep time has long been theorised but remains difficult to demonstrate. Monoaminergic neurons, which produce molecules such as serotonin and dopamine, are central to animal behaviour and cognition, yet their evolutionary origins remain unresolved. Here, we analysed single-cell transcriptomes from 16 metazoan species spanning eight phyla. Using a novel integration method, Orthogroup Recoding, together with experimental validation, we show that monoaminergic neurons form consistent transcriptional clusters across Bilateria. These clusters share a regulatory signature involving conserved transcription factors, including homologues of Fev, Lmx1b, Fer2, Insm, and Isl, suggesting a common regulatory program. This signature extends beyond the brain including other monoaminergic cells, such as the gut enterochromaffin cells and larval sensory neurons. By contrast, non-bilaterian lineages lack the coordinated expression of the transcription factors and the biosynthetic machinery that regulate monoamine production. Our observations support the existence of a shared set of TFs that define monoaminergic identity across in bilaterians.

bioinformatics↗

Functional characterization of luciferase in a brittle star indicates parallel evolution influenced by genomic availability of haloalkane dehalogenase

Determining why convergent traits use distinct versus shared genetic components is crucial for understanding how evolutionary processes generate and sustain biodiversity. However, the factors dictating the genetic underpinnings of convergent traits remain incompletely understood. Here, we use heterologous protein expression, biochemical assays, and phylogenetic analyses to confirm the origin of a luciferase gene from haloalkane dehalogenases in the brittle star Amphiura filiformis. Through database searches and gene tree analyses, we also show a complex pattern of presence and absence of haloalkane dehalogenases across organismal genomes. These results first confirm parallel evolution across a vast phylogenetic distance, because octocorals like Renilla also use luciferase derived from haloalkane dehalogenases. This parallel evolution is surprising, even though previously hypothesized, because many organisms that also use coelenterazine as the bioluminescence substrate evolved completely distinct luciferases. The inability to detect haloalkane dehalogenases in the genomes of several bioluminescent groups suggests that the distribution of this gene family influences its recruitment as a luciferase. Together, our findings highlight how biochemical function and genomic availability help determine whether distinct or shared genetic components are used during the convergent evolution of traits like bioluminescence.

evolutionary biology↗

The brittle star genome illuminates the genetic basis of animal appendage regeneration

Species within nearly all extant animal lineages are capable of regenerating body parts. However, it remains unclear whether the gene expression programme controlling regeneration is evolutionarily conserved. Brittle stars are a species-rich class of echinoderms with outstanding regenerative abilities, but investigations into the genetic bases of regeneration in this group have been hindered by the limited genomic resources. Here, we report a chromosome-scale genome assembly for the brittle star Amphiura filiformis. We show that the brittle star genome is the most rearranged amongst echinoderms sequenced to date, featuring a reorganised Hox cluster reminiscent of the rearrangements observed in sea urchins. In addition, we performed an extensive profiling of gene expression during brittle star adult arm regeneration and identified sequential waves of gene expression governing wound healing, proliferation and differentiation. We conducted comparative transcriptomic analyses with other invertebrate and vertebrate models for appendage regeneration and uncovered hundreds of genes with conserved expression dynamics, particularly during the proliferative phase of regeneration. Our findings emphasise the crucial importance of echinoderms to detect long-range expression conservation between vertebrates and classical invertebrate regeneration model systems.

evolutionary biology↗

The development and neuronal complexity of bipinnaria larvae of the sea star Asterias rubens

Free-swimming planktonic larvae are a key stage in the development of many marine phyla, and studies of these organisms have contributed to our understanding of major genetic and evolutionary processes. Although transitory, these larvae often attain a remarkable degree of tissue complexity, with well-defined musculature and nervous systems. Amongst the best studied are larvae belonging to the phylum Echinodermata, but with work largely focused on the pleuteus larvae of sea urchins (class Echinoidea). The greatest diversity of larval strategies amongst echinoderms is found in the class Asteroidea (sea-stars), organisms that are rapidly emerging as experimental systems for genetic and developmental studies. However, the bipinnaria larvae of sea stars have only been studied in detail in a small number of species and the full complexity of the nervous system is, in particular, poorly understood. Here we have analysed embryonic development and bipinnaria larval anatomy in the common North Atlantic sea-star Asterias rubens, employing use of a variety of staining methods in combination with confocal microscopy. Importantly, the complexity of the nervous system of bipinnaria larvae was revealed in greater detail than ever before, with identification of at least three centres of neuronal complexity: the anterior apical organ, oral region and ciliary bands. Furthermore, the anatomy of the musculature and sites of cell division in bipinnaria larvae were analysed. Comparisons of developmental progression and molecular anatomy across the Echinodermata provided a basis for hypotheses on the shared evolutionary and developmental processes that have shaped this group of animals. We conclude that bipinnaria larvae appear to be remarkably conserved across ~200 million years of evolutionary time and may represent a strong evolutionary and/or developmental constraint for species utilizing this larval strategy.

developmental biology↗

Post-metamorphic skeletal growth in the sea urchin Paracentrotus lividus and implications for body plan evolution

Understanding the molecular and cellular processes that underpin animal development are crucial for understanding the diversity of body plans found on the planet today. Because of their abundance in the fossil record, and tractability as a model system in the lab, skeletons provide an ideal experimental model to understand the origins of animal diversity. We herein use molecular and cellular markers to understand the growth and development of the juvenile sea urchin (echinoid) skeleton. We developed a detailed staging scheme based off of the first [~]four weeks of post-metamorphic life of the regular echinoid Paracentrotus lividus. We paired this scheme with immunohistochemical staining for neuronal, muscular, and skeletal tissues, and fluorescent assays of skeletal growth and cell proliferation to understand the molecular and cellular mechanisms underlying skeletal growth and development of the sea urchin body plan. Our experiments highlight the role of skeletogenic proteins in accretionary skeletal growth and cell proliferation in the addition of new metameric tissues. Furthermore, our work provides a framework for understanding the developmental evolution of sea urchin body plans on macroevolutionary timescales.

developmental biology↗

FGF signalling plays similar roles in development and regeneration of the skeleton in the brittle star Amphiura filiformis

Regeneration is an adult developmental process considered to be an epiphenomenon of embryonic development. Although several studies have shown that various embryonic genes are expressed during regeneration, there have been no large-scale, direct and functional comparative studies between the development and regeneration of a specific structure in one animal. Here, we use the brittle star Amphiura filiformis to characterise the role of the FGF signalling pathway during skeletal development and regeneration. In both processes, we find the ligands expressed in ectodermal cells flanking underlying mesodermal cells, and the receptors expressed specifically by these skeletogenic cells. Perturbation of FGF but not VEGF signalling during skeletogenesis completely inhibited skeleton formation in both embryogenesis and regeneration, without affecting other key developmental processes like cell migration or proliferation. Transcriptome-wide differential analysis identified a highly similar cohort of skeletogenic differentiation genes downstream of the FGF signalling pathway, whereas upstream transcription factors involved in the initial specification of the skeletogenic lineage where unaffected. Comparison to the sea urchin indicated that many of the affected genes are associated with differentiation. Moreover, several genes showed no homology to a cohort from other species, leading to the discovery of brittle star specific, downstream skeletogenic genes. In conclusion, our results show that the FGF pathway is crucial for skeletogenesis in the brittle star, as it is in other deuterostomes, and for the first time provide evidence for the re-deployment of a gene regulatory module during both regeneration and development.

developmental biology↗

Developmental transcriptomics of the brittle star Amphiura filiformis reveals gene regulatory network rewiring in echinoderm larval skeleton evolution

Amongst the echinoderms the class Ophiuroidea is of particular interest for its phylogenetic position, ecological importance, developmental and regenerative biology. However, compared to other echinoderms, notably echinoids (sea urchins), relatively little is known about developmental changes in gene expression in ophiuroids. To address this issue we have generated and assembled a large RNAseq data set of four key stages of development in the brittle star Amphiura filiformis and a de novo reference transcriptome of comparable quality to that of a model echinoderm - the sea urchin Strongyloncentrotus purpuratus. Furthermore, we provide access to the new data via a web interface: http://www.echinonet.eu/shiny/Amphiura_filiformis/. With a focus on skeleton development, we have identified highly conserved genes associated with the development of a biomineralized skeleton. We also identify important class-specific characters, including the independent duplication of the msp130 class of genes in different echinoderm classes and the unique occurrence of spicule matrix (sm) genes in echinoids. Using a new quantification pipeline for our de novo transcriptome, validated with other methodologies, we find major differences between brittle stars and sea urchins in the temporal expression of many transcription factor genes. This divergence in developmental regulatory states is more evident in early stages of development when cell specification begins, than when cells initiate differentiation. Our findings indicate that there has been a high degree of gene regulatory network rewiring in the evolution of echinoderm larval development.\n\nData DepositionsAll sequence reads are available at Genbank SRR4436669 - SRR4436674. Any sequence alignments used are available by the corresponding author upon request.

evolutionary biology↗