Genomics and development of Nematostella vectensis and other anthozoans

Rentzsch, Fabian; Technau, Ulrich

doi:10.1016/j.gde.2016.05.024

Cited by 32 publications

(30 citation statements)

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“…The development of new molecular tools in a handful of hydrozoan and anthozoan species has already provided new insights into several long-standing evolutionary and developmental questions (Houliston et al, 2010; Technau and Steele, 2011; Galliot, 2012; Nebel and Bosch, 2012; Plickert et al, 2012; Sinigaglia et al, 2013; Layden et al, 2016; Rentzsch and Technau, 2016). Those tools, in combination with “omics” and functional genomics approaches (Momose and Houliston, 2007; Rentzsch et al, 2008; Amiel et al, 2009; Chera et al, 2009; Genikhovich and Technau, 2009; Boehm et al, 2012; Röttinger et al, 2012; Layden et al, 2013; Lapébie et al, 2014; Bradshaw et al, 2015) as well as with the recently developed techniques for genome editing (Ikmi et al, 2014) are now opening new opportunities to functionally and thoroughly address the developmental and regenerative program of cnidarian muscles systems, but also the role(s) that epitheliomuscular cells, muscle fibers and muscle contraction can play on the regeneration process.…”

Section: Discussionmentioning

confidence: 99%

“…A handful of cnidarians has emerged in the past decades as experimental models in molecular, cell and developmental biology, providing insights into the evolution of developmental programs, including regeneration, stem cell biology and the evolution of key bilaterian traits (Kraus et al, 2007, 2016; Momose and Houliston, 2007; Amiel et al, 2009; Chera et al, 2009; Boehm et al, 2012; Layden et al, 2012; Röttinger et al, 2012; Sinigaglia et al, 2013; Leclère and Rentzsch, 2014; Abrams et al, 2015; Bradshaw et al, 2015; Helm et al, 2015; reviewed in Technau and Steele, 2011; Layden et al, 2016; Leclère et al, 2016; Rentzsch and Technau, 2016). The main, but not exclusive, cnidarian models are the medusozoan hydrozoans Hydra, Hydractinia, Podocoryna and Clytia (reviewed in Houliston et al, 2010; Galliot, 2012; Plickert et al, 2012; Gahan et al, 2016; Leclère et al, 2016) as well as the anthozoans Nematostella vectensis (reviewed in Layden et al, 2016; Rentzsch and Technau, 2016) and the coral Acropora (Shinzato et al, 2011; Hayward et al, 2015; Okubo et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…The main, but not exclusive, cnidarian models are the medusozoan hydrozoans Hydra, Hydractinia, Podocoryna and Clytia (reviewed in Houliston et al, 2010; Galliot, 2012; Plickert et al, 2012; Gahan et al, 2016; Leclère et al, 2016) as well as the anthozoans Nematostella vectensis (reviewed in Layden et al, 2016; Rentzsch and Technau, 2016) and the coral Acropora (Shinzato et al, 2011; Hayward et al, 2015; Okubo et al, 2016). …”

Section: Introductionmentioning

confidence: 99%

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Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Leclère

Röttinger

2017

Front. Cell Dev. Biol.

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The ability to perform muscle contractions is one of the most important and distinctive features of eumetazoans. As the sister group to bilaterians, cnidarians (sea anemones, corals, jellyfish, and hydroids) hold an informative phylogenetic position for understanding muscle evolution. Here, we review current knowledge on muscle function, diversity, development, regeneration and evolution in cnidarians. Cnidarian muscles are involved in various activities, such as feeding, escape, locomotion and defense, in close association with the nervous system. This variety is reflected in the large diversity of muscle organizations found in Cnidaria. Smooth epithelial muscle is thought to be the most common type, and is inferred to be the ancestral muscle type for Cnidaria, while striated muscle fibers and non-epithelial myocytes would have been convergently acquired within Cnidaria. Current knowledge of cnidarian muscle development and its regeneration is limited. While orthologs of myogenic regulatory factors such as MyoD have yet to be found in cnidarian genomes, striated muscle formation potentially involves well-conserved myogenic genes, such as twist and mef2. Although satellite cells have yet to be identified in cnidarians, muscle plasticity (e.g., de- and re-differentiation, fiber repolarization) in a regenerative context and its potential role during regeneration has started to be addressed in a few cnidarian systems. The development of novel tools to study those organisms has created new opportunities to investigate in depth the development and regeneration of cnidarian muscle cells and how they contribute to the regenerative process.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Leclère

Röttinger

2017

Front. Cell Dev. Biol.

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“…http://dx.doi.org/10.1101/201103 doi: bioRxiv preprint first posted online Oct. 11, 2017; emerging as a powerful approach for unbiased de novo discovery and detailed molecular characterization of transcriptional states and cell types in mammalian tissues (Jaitin et al, 2014; La Manno et al, 2016;Shekhar et al, 2016; Tasic et al, 2016;Wurtzel et al, 2015; Zeisel et al, 2015). Nevertheless, systematic single cell expression profiling of whole adult non-model organisms remains a challenge yet to be explored.We focused our whole-organism scRNA-seq efforts on the cnidarian Nematostella (Rentzsch and Technau, 2016), hoping to rely on the relatively well-established understanding of basic cell types and developmental processes in this species, and to expand them using unbiased and highresolution analysis. We were particularly interested in the organization of neuronal cell types in Nematostella, given the important role of Nematostella in evolutionary studies of the nervous system (Marlow et al, 2009;Nakanishi et al, 2012).…”

mentioning

confidence: 99%

“…We focused our whole-organism scRNA-seq efforts on the cnidarian Nematostella (Rentzsch and Technau, 2016), hoping to rely on the relatively well-established understanding of basic cell types and developmental processes in this species, and to expand them using unbiased and highresolution analysis. We were particularly interested in the organization of neuronal cell types in Nematostella, given the important role of Nematostella in evolutionary studies of the nervous system (Marlow et al, 2009;Nakanishi et al, 2012).…”

mentioning

confidence: 99%

Cnidarian cell type diversity revealed by whole-organism single-cell RNA-seq analysis

Sebé-Pedrós

Chomsky

Saudememont

et al. 2017

Preprint

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A hallmark of animal evolution is the emergence and diversification of cell type-specific transcriptional states. But systematic and unbiased characterization of differentiated gene regulatory programs was so far limited to specific tissues in a few model species. Here, we perform whole-organism single cell transcriptomics to map cell types in the cnidarian Nematostella vectensis, a non-bilaterian animal that display complex tissue-level bodyplan organization. We uncover high diversity of transcriptional states in Nematostella, demonstrating cell type-specific expression for 35% of the genes and 51% of the transcription factors (TFs) detected. We identify eight broad cell clusters corresponding to cell classes such as neurons, muscles, cnidocytes, or digestive cells. These clusters comprise multiple cell modules expressing diverse and specific markers, uncovering in particular a rich repertoire of cells associated with neuronal markers. TF expression and sequence analysis defines the combinatorial code that underlies this cell-specific expression. It also reveals the existence of a complex regulatory lexicon of TF binding motifs encoded at both enhancer and promoters of Nematostella tissue-specific genes. Whole organism single cell RNA-seq is thereby established as a tool for comprehensive study of genome regulation and cell type evolution.Non-bilaterian animal lineages, including cnidarians, ctenophores, sponges and placozoans, have simple body plans and have been historically considered to contain limited numbers of cell types (Valentine, 2003). In cnidarians, these cells include a small number of morphologically distinct neurons, gland cells, muscle cells, epidermis, and gut (Frank and Bleakney, 1976;Hand and Uhlinger, 1992;Hyman, 1940). This presumed simplicity in the number of cnidarian cell types stands in marked contrast to their genomic complexity. Indeed, multiple genomic features, such as the gene repertoire, syntenic gene blocks, and intronic structure, are more similar between cnidarians and vertebrates than to model bilaterian invertebrates like D. melanogaster or C. elegans (Putnam et al., 2007;Technau and Schwaiger, 2015). Recently, it was shown that these similarities extend to the regulatory landscape of Nematostella genes (Schwaiger et al., 2014). However, the extent to which these genomic features participate in regulating complex cell type hierarchies remains largely unknown.Gene expression profiling by in situ hybridization allows for comparative study of cell types and tissue organisation in different species, providing insights into their evolution (Steinmetz et al., 2012). But these approaches require a priori selection of candidate gene markers; they are difficult to scale towards multiple expressed genes simultaneously; and they are not readily applicable to all species or life stages, in particular adult specimens. On the other hand, techniques for genome-wide profiling of gene expression were so far dependent on established staging and tissue dissection procedures. Single-cell RNA ...

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Wound healing across the animal kingdom: Crosstalk between the immune system and the extracellular matrix

Gómez

Sabin

Echeverri

2020

Developmental Dynamics

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Tissue regeneration is widespread in the animal kingdom. To date, key roles for different molecular and cellular programs in regeneration have been described, but the ultimate blueprint for this talent remains elusive. In animals capable of tissue regeneration, one of the most crucial stages is wound healing, whose main goal is to close the wound and prevent infection. In this stage, it is necessary to avoid scar formation to facilitate the activation of the immune system and remodeling of the extracellular matrix, key factors in promoting tissue regeneration. In this review, we will discuss the current state of knowledge regarding the role of the immune system and the interplay with the extracellular matrix to trigger a regenerative response.

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Genomics and development of Nematostella vectensis and other anthozoans

Cited by 32 publications

References 89 publications

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Cnidarian cell type diversity revealed by whole-organism single-cell RNA-seq analysis

Wound healing across the animal kingdom: Crosstalk between the immune system and the extracellular matrix

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