The backbone of the post-synaptic density originated in a unicellular ancestor of choanoflagellates and metazoans

<p>Abstract</p> <p>Background</p> <p>Comparative genomics of the early diverging metazoan lineages and of their unicellular sister-groups opens new window to reconstructing the genetic changes which preceded or accompanied the evolution of multicellular body plans. A recent analysis found that the genome of the nerve-less sponges encodes the homologues of most vertebrate post-synaptic proteins. In vertebrate excitatory synapses, these proteins assemble to form the post-synaptic density, a complex molecular platform linking membrane receptors, components of their signalling pathways, and the cytoskeleton. Newly available genomes from <it>Monosiga brevicollis </it>(a member of Choanoflagellata, the closest unicellular relatives of animals) and <it>Trichoplax adhaerens </it>(a member of Placozoa: besides sponges, the only nerve-less metazoans) offer an opportunity to refine our understanding of post-synaptic protein evolution.</p> <p>Results</p> <p>Searches for orthologous proteins and reconstruction of gene gains/losses based on the taxon phylogeny indicate that post-synaptic proteins originated in two main steps. The backbone scaffold proteins (Shank, Homer, DLG) and some of their partners were acquired in a unicellular ancestor of choanoflagellates and metazoans. A substantial additional set appeared in an exclusive ancestor of the Metazoa. The placozoan genome contains most post-synaptic genes but lacks some of them. Notably, the master-scaffold protein Shank might have been lost secondarily in the placozoan lineage.</p> <p>Conclusions</p> <p>The time of origination of most post-synaptic proteins was not concomitant with the acquisition of synapses or neural-like cells. The backbone of the scaffold emerged in a unicellular context and was probably not involved in cell-cell communication. Based on the reconstructed protein composition and potential interactions, its ancestral function could have been to link calcium signalling and cytoskeleton regulation. The complex later became integrated into the evolving synapse through the addition of novel functionalities.</p

Conserved expression of vertebrate microvillar gene homologs in choanocytes of freshwater sponges

International audienceBackground: The microvillus is a versatile organelle that serves important functions in disparate animal cell types. However, from a molecular perspective, the microvillus has been well studied in only a few, predominantly vertebrate, contexts. Little is known about how differences in microvillar structure contribute to differences in function, and how these differences evolved. We sequenced the transcriptome of the freshwater sponge, Ephydatia muelleri, and examined the expression of vertebrate microvillar gene homologs in choanocytes—the only microvilli-bearing cell type present in sponges. Sponges offer a distant phylogenetic comparison with vertebrates, and choanocytes are central to discussions about early animal evolution due to their similarity with choanoflagellates, the single-celled sister line-age of modern animals. Results: We found that, from a genomic perspective, sponges have conserved homologs of most vertebrate microvillar genes, most of which are expressed in choanocytes, and many of which exhibit choanocyte-specific or choanocyte-enriched expression. Possible exceptions include the cadherins that form intermicrovillar links in the enterocyte brush border and hair cell stereocilia of vertebrates and cnidarians. No obvious orthologs of these proteins were detected in sponges, but at least four candidate cadherins were identified as choanocyte-enriched and might serve this function. In contrast to the evidence for conserved microvillar structure in sponges and vertebrates, we found that choanoflagellates and ctenophores lack homologs of many fundamental microvillar genes, suggesting that microvillar structure may diverge significantly in these lineages, warranting further study. Conclusions: The available evidence suggests that microvilli evolved early in the prehistory of modern animals and have been repurposed to serve myriad functions in different cellular contexts. Detailed understanding of the sequence by which different microvilli-bearing cell/tissue types diversified will require further study of microvillar composition and development in disparate cell types and lineages. Of particular interest are the microvilli of choano-flagellates, ctenophores, and sponges, which collectively bracket the earliest events in animal evolution

The Hazards of Regeneration: From Morgan’s Legacy to Evo-Devo

International audienceAbstract In his prominent book Regeneration (1901), T.H. Morgan’s collected and synthesized theoretical and experimental findings from a diverse array of regenerating animals and plants. Through his endeavor, he introduced a new way to study regeneration and its evolution, setting a conceptual framework that still guides today’s research and that embraces the contemporary evolutionary and developmental approaches. In the first part of the chapter, we summarize Morgan’s major tenets and use it as a narrative thread to advocate interpreting regenerative biology through the theoretical tools provided by evolution and developmental biology, but also to highlight potential caveats resulting from the rapid proliferation of comparative studies and from the expansion of experimental laboratory models. In the second part, we review some experimental evo-devo approaches, highlighting their power and some of their interpretative dangers. Finally, in order to further understand the evolution of regenerative abilities, we portray an adaptive perspective on the evolution of regeneration and suggest a framework for investigating the adaptive nature of regeneration

The eventful history of nonembryonic development in tunicates

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New insights on ctenophore neural anatomy: immunofluorescence study in Pleurobrachia pileus (Müller, 1776).

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Salinity-mediated limitation of asexual reproduction in the colonial ascidian Polyandrocarpa zorritensis

International audienceAscidians are among the most common invasive marine invertebrates worldwide. Many species of non-indigenous ascidians (NIAs) have successfully colonized the Mediterranean Sea, notably within anthropized coastal lagoons and harbors. Although invasive species are generally characterized by their broad ecological tolerance, different ascidian species exhibit varied responses to biotic and abiotic environmental stressors, including temperature and salinity. Acquiring a better understanding about of the impact of such parameters on ascidian life history is crucial for predicting the invasive potential of NIAs. In this study, we investigated the impact of various salinities on the reproduction of the colonial ascidian Polyandorcarpa zorritensis, a species indigenous to Peru and a thriving invader. P. zorritensis undergoes asexual reproduction via a peculiar form of budding named vasal budding and produces resistant spherules, which likely facilitated its dissemination over long distances. Despite its widespread distribution along the Pacific and Atlantic coasts, it is only found in a few Mediterranean coastal areas with a low salinity. We tested the impact of different salinity conditions on the sexual and asexual reproduction rates of P. zorritensis in a controlled laboratory setting. Our experiments showed that the rate of asexual reproduction in colonies bred at 29 or 36 ppt salinity levels, corresponding to the natural range inhabited by P. zorritensis, was higher than those grown in 40 ppt salinity, commonly found in Mediterranean marinas and harbors. The results suggest that, although P. zorritensis has been present in the Mediterranean for several decades, its potential for invasion could be constrained by an intolerance to high salinity

Comparing dormancy in two distantly related tunicates reveals morphological, molecular, and ecological convergences and repeated co-option

Abstract Many asexually-propagating marine invertebrates can survive extreme environmental conditions by developing dormant structures, i.e., morphologically simplified bodies that retain the capacity to completely regenerate a functional adult when conditions return to normal. Here, we examine the environmental, morphological, and molecular characteristics of dormancy in two distantly related clonal tunicate species: Polyandrocarpa zorritensis and Clavelina lepadiformis. In both species, we report that the dormant structures are able to withstand harsher temperature and salinity conditions compared to the adults. The dormant structures are the dominant forms these species employ to survive adverse conditions when the zooids themselves cannot survive. While previous work shows C. lepadiformis dormant stage is present in winters in the Atlantic Ocean and summers in the Mediterranean, this study is the first to show a year-round presence of P. zorritensis dormant forms in NW Italy, even in the late winter when all zooids have disappeared. By finely controlling the entry and exit of dormancy in laboratory-reared individuals, we were able to select and characterize the morphology of dormant structures associated with their transcriptome dynamics. In both species, we identified putative stem and nutritive cells in structures that resemble the earliest stages of asexual propagation. By characterizing gene expression during dormancy and regeneration into the adult body plan (i.e., germination), we observed that genes which control dormancy and environmental sensing in other metazoans, notably HIF-α and insulin signaling genes, are also expressed in tunicate dormancy. Germination-related genes in these two species, such as the retinoic acid pathway, are also found in other unrelated clonal tunicates during asexual development. These results are suggestive of repeated co-option of conserved eco-physiological and regeneration programs for the origin of novel dormancy-germination processes across distantly related animal taxa

Somatic stem cells express Piwi and Vasa genes in an adult ctenophore : ancient association of " germline genes " with stemness.

International audienceStem cells are essential for animal development and adult tissue homeostasis, and the quest for an ancestral gene fingerprint of sternness is a major challenge for evolutionary developmental biology. Recent studies have indicated that a series of genes, including the transposon silencer Piwi and the translational activator Vasa, specifically involved in germline determination and maintenance in classical bilaterian models (e.g., vertebrates, fly, nematode), are more generally expressed in adult multipotent stem cells in other animals like flatworms and hydras. Since the progeny of these multipotent stem cells includes both somatic and germinal derivatives, it remains unclear whether Vasa, Piwi, and associated genes like Bruno and PL10 were ancestrally linked to sternness, or to germinal potential. We have investigated the expression of Vasa, two Piwi paralogues, Bruno and PL10 in Pleurobrachia pileus, a member of the early-diverging phylum Ctenophora, the probable sister group of cnidarians. These genes were all expressed in the male and female germlines, and with the exception of one of the Piwi paralogues, they showed similar expression patterns within somatic territories (tentacle root, comb rows, aboral sensory complex). Cytological observations and EdU DNA-labelling and long-term retention experiments revealed concentrations of stem cells closely matching these gene expression areas. These stem cell pools are spatially restricted, and each specialised in the production of particular types of somatic cells. These data unveil important aspects of cell renewal within the ctenophore body and suggest that Piwi, Vasa, Bruno, and PL10 belong to a gene network ancestrally acting in two distinct contexts: (i) the germline and (ii) stem cells, whatever the nature of their progeny

Novel budding mode in Polyandrocarpa zorritensis: a model for comparative studies on asexual development and whole body regeneration

Abstract Background In tunicates, the capacity to build an adult body via non-embryonic development (NED), i.e., asexual budding and whole body regeneration, has been gained or lost several times across the whole subphylum. A recent phylogeny of the family Styelidae revealed an independent acquisition of NED in the colonial species Polyandrocarpa zorritensis and highlighted a novel budding mode. In this paper, we provide the first detailed characterization of the asexual life cycle of P. zorritensis. Results Bud formation occurs along a tubular protrusion of the adult epidermis, the stolon, in a vascularized area defined as budding nest. The bud arises through a folding of the epithelia of the stolon with the contribution of undifferentiated mesenchymal cells. This previously unreported mode of bud onset leads to the formation of a double vesicle, which starts to develop into a zooid through morphogenetic mechanisms common to other Styelidae. The budding nest can also continue to accumulate nutrients and develop into a round-shaped structure, designated as spherule, which represents a dormant form able to survive low temperatures. Conclusions To understand the mechanisms of NED and their evolution, it is fundamental to start from a robust phylogenetic framework in order to select relevant species to compare. The anatomical description of P. zorritensis NED provides the foundation for future comparative studies on plasticity of budding and regeneration in tunicates