Understanding Animal Evolution: The Added Value of Sponge Transcriptomics and Genomics

Renard, Emmanuelle; Leys, Sally P.; Wörheide, Gert; Borchiellini, Carole

doi:10.1002/bies.201700237

Cited by 36 publications

(27 citation statements)

References 120 publications

(195 reference statements)

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“…An initially surprising finding from early genome and transcriptome sequencing of sponges was that, despite having vast morphological differences with other animals, they also have highly conserved homologs of most developmental regulatory genes (Nichols, Dirks, Pearse, & King, ; Renard et al, ; Srivastava et al, ). Furthermore, it has been shown that these genes have spatiotemporal expression patterns consistent with conserved roles in developmental patterning.…”

Section: Plasticity May Predominate Over Genetic Patterning In Spongementioning

confidence: 99%

The significance of sponges for comparative studies of developmental evolution

Colgren

Nichols

2019

WIREs Developmental Biology

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Sponges, ctenophores, placozoans, and cnidarians have key evolutionary significance in that they bracket the time interval during which organized animal tissues were first assembled, fundamental cell types originated (e.g., neurons and myocytes), and developmental patterning mechanisms evolved. Sponges in particular have often been viewed as living surrogates for early animal ancestors, largely due to similarities between their feeding cells (choanocytes) with choanoflagellates, the unicellular/colony‐forming sister group to animals. Here, we evaluate these claims and highlight aspects of sponge biology with comparative value for understanding developmental evolution, irrespective of the purported antiquity of their body plan. Specifically, we argue that sponges strike a different balance between patterning and plasticity than other animals, and that environmental inputs may have prominence over genetically regulated developmental mechanisms. We then present a case study to illustrate how contractile epithelia in sponges can help unravel the complex ancestry of an ancient animal cell type, myocytes, which sponges lack. Sponges represent hundreds of millions of years of largely unexamined evolutionary experimentation within animals. Their phylogenetic placement lends them key significance for learning about the past, and their divergent biology challenges current views about the scope of animal cell and developmental biology. This article is characterized under: Comparative Development and Evolution > Evolutionary Novelties Comparative Development and Evolution > Body Plan Evolution

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Section: Plasticity May Predominate Over Genetic Patterning In Spongementioning

confidence: 99%

The significance of sponges for comparative studies of developmental evolution

Colgren

Nichols

2019

WIREs Developmental Biology

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“…With regard to the evolution of poriferan-TSP, our analysis demonstrated that all three categories of TSP-related proteins are expressed in this phylum. As others have noted more generally, there was very high in-clade sequence variation between different classes of Porifera (Renard et al. 2018).…”

Section: Discussionmentioning

confidence: 65%

Emergence of a Thrombospondin Superfamily at the Origin of Metazoans

Shoemark

Ziegler

Watanabe

et al. 2019

Molecular Biology and Evolution

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Extracellular matrix (ECM) is considered central to the evolution of metazoan multicellularity; however, the repertoire of ECM proteins in nonbilaterians remains unclear. Thrombospondins (TSPs) are known to be well conserved from cnidarians to vertebrates, yet to date have been considered a unique family, principally studied for matricellular functions in vertebrates. Through searches utilizing the highly conserved C-terminal region of TSPs, we identify undisclosed new families of TSP-related proteins in metazoans, designated mega-TSP, sushi-TSP, and poriferan-TSP, each with a distinctive phylogenetic distribution. These proteins share the TSP C-terminal region domain architecture, as determined by domain composition and analysis of molecular models against known structures. Mega-TSPs, the only form identified in ctenophores, are typically >2,700 aa and are also characterized by N-terminal leucine-rich repeats and central cadherin/immunoglobulin domains. In cnidarians, which have a well-defined ECM, Mega-TSP was expressed throughout embryogenesis in Nematostella vectensis , with dynamic endodermal expression in larvae and primary polyps and widespread ectodermal expression in adult Nematostella vectensis and Hydra magnipapillata polyps. Hydra Mega-TSP was also expressed during regeneration and siRNA-silencing of Mega-TSP in Hydra caused specific blockade of head regeneration. Molecular phylogenetic analyses based on the conserved TSP C-terminal region identified each of the TSP-related groups to form clades distinct from the canonical TSPs. We discuss models for the evolution of the newly defined TSP superfamily by gene duplications, radiation, and gene losses from a debut in the last metazoan common ancestor. Together, the data provide new insight into the evolution of ECM and tissue organization in metazoans.

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“…Their body differs from those of all other metazoan, because instead of having true muscles and neurons, the sponges basically have a choanoderm (internal flagellated epithelium; [the term epithelium is used in this work in accordance to the definition proposed by Nickel, Scheer, Hammel, Herzen, and Beckmann () that sponges have epithelium sensu lato ]), a pinacoderm (coating epithelium) lining the wall of the canals of the aquiferous system, and a mesohyl between these two layers, which comprises mobile cells, skeletal material (spicules), and protein fibers (Langenbruch, ; Leys & Hill, ). Nonetheless, although morphologically simple, the genome, transcriptome, life cycle, and other aspects of their biology were characterized as more complex than expected (Dunn, Leys, & Haddock, ; Leys & Hill, ; Renard, Leys, Wörheide, & Borchiellini, ). The filter‐feeding habit of sponges is crucial for the health and economy of marine environments, by transferring nutrients from the water column to the benthic communities (benthic‐pelagic coupling), interfering in the carbon and silicon cycles, and due to their constant cell changes, providing particulate organic carbon that will serve as food for microorganisms present in water and boost the trophic nets (Becerro, ; de Goeij et al, ).…”

Section: Introductionmentioning

confidence: 98%

Anatomy and ultrastructure of the tropical sponge Cladocroce caelum (Haplosclerida, Demospongiae)

Hora

Cavalcanti

Lanna

2018

Journal of Morphology

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The main characteristic of sponges (Porifera) is the presence of the aquiferous system-a system formed by canals and choanocyte chambers, in which the sponges carry out most of their physiological functions. Despite of the importance for the biology of the group, the knowledge about this structure is still incipient, even when morphological investigations are taken in account.Here, we investigated the anatomy and ultrastructure of the tropical demosponge Cladocroce caelum (Haplosclerida, Demospongiae) using light and electron microscopy. In the studied region, specimens of this species were repent or repent-branched, possessing one to several oscula. A uniform and reduced atrium was found just below each osculum. There was a thin ectosome and the choanosome presented meager mesohyl, but a high number of choanocyte chambers. The choanocyte chambers were rounded, and, as in other haplosclerids, they are found separated from the mesohyl by endopinacocytes, "hanging" in the inhalant canals. Even though the utility of the general organization of the aquiferous system has been advocated as a possible tool to understand the phylogeny of the group, we found that these characters might not be as useful as expected. The size of the particles ingested by the sponge and the amount of bacteria to sustain their bodies are discussed. In addition, we found that the density of choanocyte chambers was reduced when the specimens were carrying out the spermatogenesis, indicating that the reproduction may impair the filtering activity of the sponge. Our findings consist in a first step to better comprehend the physiology, development, and adaptation to the environmental conditions where the species is found.

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Understanding Animal Evolution: The Added Value of Sponge Transcriptomics and Genomics

Cited by 36 publications

References 120 publications

The significance of sponges for comparative studies of developmental evolution

The significance of sponges for comparative studies of developmental evolution

Emergence of a Thrombospondin Superfamily at the Origin of Metazoans

Anatomy and ultrastructure of the tropical sponge Cladocroce caelum (Haplosclerida, Demospongiae)

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