Mechanisms of tentacle morphogenesis in the sea anemone<i>Nematostella vectensis</i>

Fritz, Ashleigh E.; Ikmi, Aissam; Seidel, Christopher; Paulson, Ariel; Gibson, Matthew C.

doi:10.1242/dev.088260

Cited by 39 publications

(48 citation statements)

References 69 publications

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“…DAPT treatment during regeneration led to a block in tentacle formation (Fig. 4A and B), a phenotype also known from other cnidarians (DuBuc et al, 2014; Fritz et al, 2013; Marlow et al, 2012; Münder et al, 2013). However, as shown above, the acetylated tubulin positive oral nervous system in regenerating, Notch inhibited polyps was normal (Fig 3B).…”

Section: Resultssupporting

confidence: 58%

“…In hydrozoan cnidarians, however, neurons develop from non-epithelial, migratory stem cells, called i-cells, which are segregated during gastrulation (Gahan et al, 2016; Hager and David, 1997; Leclere et al, 2012; Miljkovic-Licina et al, 2007). Pharmacological inhibition of Notch signaling in adult Hydra , a hydrozoan cnidarian, revealed no effect on the numbers of adult neurons (Käsbauer et al, 2007; Khalturin et al, 2007), but this treatment did affect nematocyte differentiation and tentacle development (Käsbauer et al, 2007; Khalturin et al, 2007; Münder et al, 2013), defects that were also observed in Nematostella following pharmacological Notch inhibition (DuBuc et al, 2014; Fritz et al, 2013; Marlow et al, 2012). Hence, the role of Notch in tentacle morphogenesis and nematogenesis seems to be conserved in cnidarians, but its function in neural development requires further research across the phylum.…”

Section: Introductionmentioning

confidence: 97%

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Functional studies on the role of Notch signaling in Hydractinia development

Gahan

Schnitzler

DuBuc

et al. 2017

Developmental Biology

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The function of Notch signaling was previously studied in two cnidarians, Hydra and Nematostella, representing the lineages Hydrozoa and Anthozoa, respectively. Using pharmacological inhibition in Hydra and a combination of pharmacological and genetic approaches in Nematostella, it was shown in both animals that Notch is required for tentacle morphogenesis and for late stages of stinging cell maturation. Surprisingly, a role for Notch in neural development, which is well documented in bilaterians, was evident in embryonic Nematostella but not in adult Hydra. Adult neurogenesis in the latter seemed to be unaffected by DAPT, a drug that inhibits Notch signaling. To address this apparent discrepancy we studied the role of Notch in Hydractinia echinata, an additional hydrozoan, in all life stages. Using CRISPR-Cas9 mediated mutagenesis, transgenesis, and pharmacological interference we show that Notch is dispensable for Hydractinia normal neurogenesis in all life stages but is required for the maturation of stinging cells and for tentacle morphogenesis. Our results are consistent with a conserved role for Notch in morphogenesis and nematogenesis across Cnidaria, and a lineage specific loss of Notch dependence in neurogenesis in hydrozoans.

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Section: Resultssupporting

confidence: 58%

Section: Introductionmentioning

confidence: 97%

Functional studies on the role of Notch signaling in Hydractinia development

Gahan

Schnitzler

DuBuc

et al. 2017

Developmental Biology

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“…Within 48 hours post-fertilization, the embryo develops into a fully ciliated, free-swimming planula larva and starts to escape from its surrounding gelatin matrix. By day seven, elongated planulae settle down and metamorphose into polyps bearing four tentacles [220, 221]. Under optimal conditions, it takes 2 to 3 months for a juvenile polyp to reach sexual maturity.…”

Section: Nematostella Vectensis: Born To Be a Starletmentioning

confidence: 99%

Non-model model organisms

et al. 2017

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Model organisms are widely used in research as accessible and convenient systems to study a particular area or question in biology. Traditionally only a handful of organisms have been widely studied, but modern research tools are enabling researchers to extend the set of model organisms to include less-studied and more unusual systems. This Forum highlights a range of 'non-model model organisms' as emerging systems for tackling questions across the whole spectrum of biology (and beyond), the opportunities and challenges, and the outlook for the future.

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“…In the recent years, Nematostella vectensis has become an established cnidarian model in developmental biology due to its relative ease of laboratory spawning 14,15 , tractable developmental biology 16–20 , extensive regenerative capacity 21–24 , and robust molecular-genetic approaches 25–29 . Nematostella polyps can harbor a variable number of tentacles ranging from four to eighteen, but the common number in adulthood is sixteen 4,10 . During development, four tentacle buds simultaneously form in the swimming larvae and give rise to the initial appendages of the primary polyp 4 .…”

Section: Introductionmentioning

confidence: 99%

Feeding-dependent tentacle development in the sea anemoneNematostella vectensis

Ikmi

Steenbergen

Anzo

et al. 2020

Preprint

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In cnidarians, axial patterning is not restricted to embryonic development but continues throughout a prolonged life history filled with unpredictable environmental changes. How this developmental capacity copes with fluctuations of food availability and whether it recapitulates embryonic mechanisms remain poorly understood. To address these questions, we utilize the tentacles of the sea anemone Nematostella vectensis as a novel paradigm for developmental patterning across distinct life history stages. As a result of embryonic development, Nematostella polyps feature four primary tentacles, while adults have 16 or more. By analyzing over 1000 growing polyps, we find that tentacle progression is remarkably stereotyped and occurs in a feeding-dependent manner. Mechanistically, we show that discrete Fibroblast growth factor receptor b (Fgfrb)-positive ring muscles prefigure the sites of new tentacles in unfed polyps. In response to feeding, a Target of Rapamycin (TOR)-dependent mechanism controls the expansion of Fgfrb expression in oral tissues which defines tentacle primordia. Using a combination of genetic, cellular and molecular approaches, we demonstrate that FGFRb regionally enhances TOR signaling activity and promotes polarized growth, a spatial pattern that is restricted to polyp but not to embryonic tentacle primordia. These findings reveal an unexpected plasticity of tentacle development, and show that the crosstalk between TOR-mediated nutrient signaling and FGFRb pathway couples post-embryonic body patterning with food availability.3

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Mechanisms of tentacle morphogenesis in the sea anemoneNematostella vectensis

Cited by 39 publications

References 69 publications

Functional studies on the role of Notch signaling in Hydractinia development

Functional studies on the role of Notch signaling in Hydractinia development

Non-model model organisms

Feeding-dependent tentacle development in the sea anemoneNematostella vectensis

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