Feeding-dependent tentacle development in the sea anemone Nematostella vectensis

Ikmi, Aissam; Steenbergen, Peter J.; Anzo, Marie; McMullen, Mason R.; Stokkermans, Anniek; Ellington, Lacey R.; Gibson, Matthew C.

doi:10.1038/s41467-020-18133-0

Cited by 23 publications

(27 citation statements)

References 55 publications

(72 reference statements)

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“…These observed differences between Sym and Apo lacerates could also be explained by a lack of nutrients in general in Apo lacerates, not necessarily those specifically derived from symbionts. In the non-symbiotic anemone Nematostella vectensis , new tentacle growth in primary polyps is supported by localized nutrient-dependent cell proliferation ( Ikmi et al, 2020 ). In the absence of food sources ( i.e.…”

Section: Discussionmentioning

confidence: 99%

“…Despite these previous descriptions of pedal laceration, the process of how tentacles and mesenteries are patterned throughout development is unknown. Several studies in the non-symbiotic anemone Nematostella vectensis have characterized both tentacle and mesentery patterning during different stages of postembryonic development ( Genikhovich et al, 2015 ; He et al, 2018 ; Ikmi et al, 2020 ). During metamorphosis from larvae to primary polyp, Nematostella mesenteries are the first structures to develop followed by the four primary tentacles ( Genikhovich et al, 2015 ; He et al, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

“…During metamorphosis from larvae to primary polyp, Nematostella mesenteries are the first structures to develop followed by the four primary tentacles ( Genikhovich et al, 2015 ; He et al, 2018 ). As a young polyp, Nematostella tentacle growth is nutrient-dependent and is characterized by sequential, paired emergence around the directive axis in a stereotypical fashion ( Ikmi et al, 2020 ). It is unclear whether nutritional availability has a similar effect on tentacle and/or mesentery growth in Aiptasia lacerates.…”

Section: Introductionmentioning

confidence: 99%

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Tentacle patterning during Exaiptasia diaphana pedal lacerate development differs between symbiotic and aposymbiotic animals

Presnell

Wirsching

Weis

2022

PeerJ

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Exaiptasia diaphana, a tropical sea anemone known as Aiptasia, is a tractable model system for studying the cellular, physiological, and ecological characteristics of cnidarian-dinoflagellate symbiosis. Aiptasia is widely used as a proxy for coral-algal symbiosis, since both Aiptasia and corals form a symbiosis with members of the family Symbiodiniaceae. Laboratory strains of Aiptasia can be maintained in both the symbiotic (Sym) and aposymbiotic (Apo, without algae) states. Apo Aiptasia allow for the study of the influence of symbiosis on different biological processes and how different environmental conditions impact symbiosis. A key feature of Aiptasia is the ease of propagating both Sym and Apo individuals in the laboratory through a process called pedal laceration. In this form of asexual reproduction, small pieces of tissue rip away from the pedal disc of a polyp, then these lacerates eventually develop tentacles and grow into new polyps. While pedal laceration has been described in the past, details of how tentacles are formed or how symbiotic and nutritional state influence this process are lacking. Here we describe the stages of development in both Sym and Apo pedal lacerates. Our results show that Apo lacerates develop tentacles earlier than Sym lacerates, while over the course of 20 days, Sym lacerates end up with a greater number of tentacles. We describe both tentacle and mesentery patterning during lacerate development and show that they form through a single pattern in early stages regardless of symbiotic state. In later stages of development, Apo lacerate tentacles and mesenteries progress through a single pattern, while variable patterns were observed in Sym lacerates. We discuss how Aiptasia lacerate mesentery and tentacle patterning differs from oral disc regeneration and how these patterning events compare to postembryonic development in Nematostella vectensis, another widely-used sea anemone model. In addition, we demonstrate that Apo lacerates supplemented with a putative nutrient source developed an intermediate number of tentacles between un-fed Apo and Sym lacerates. Based on these observations, we hypothesize that pedal lacerates progress through two different, putatively nutrient-dependent phases of development. In the early phase, the lacerate, regardless of symbiotic state, preferentially uses or relies on nutrients carried over from the adult polyp. These resources are sufficient for lacerates to develop into a functional polyp. In the late phase of development, continued growth and tentacle formation is supported by nutrients obtained from either symbionts and/or the environment through heterotrophic feeding. Finally, we advocate for the implementation of pedal lacerates as an additional resource in the Aiptasia model system toolkit for studies of cnidarian-dinoflagellate symbiosis.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Tentacle patterning during Exaiptasia diaphana pedal lacerate development differs between symbiotic and aposymbiotic animals

Presnell

Wirsching

Weis

2022

PeerJ

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“…In the future, it will be uttermost interesting to determine if and how TOR is involved in these adaptive growth patterns, and genetic screens will be invaluable tools to gain further knowledge. Interestingly, a very recent report showed that the sea anemone Nematostella vectensis also produces new tentacles throughout its life cycle in a nutrient-regulated manner and under the control of TOR [108]. This could suggest a convergent evolution during the independent acquisition of multicellularity by plants and early animals, which rewired the primordial TOR signaling pathway to promote organ inception in a nutrient-driven manner.…”

Section: Conclusion and Future Prospectsmentioning

confidence: 99%

The Plant Target of Rapamycin: A Conduc TOR of Nutrition and Metabolism in Photosynthetic Organisms

Ingargiola

Duarte

Robaglia

et al. 2020

Genes

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Living organisms possess many mechanisms to sense nutrients and favorable conditions, which allow them to grow and develop. Photosynthetic organisms are very diverse, from green unicellular algae to multicellular flowering plants, but most of them are sessile and thus unable to escape from the biotic and abiotic stresses they experience. The Target of Rapamycin (TOR) signaling pathway is conserved in all eukaryotes and acts as a central regulatory hub between growth and extrinsic factors, such as nutrients or stress. However, relatively little is known about the regulations and roles of this pathway in plants and algae. Although some features of the TOR pathway seem to have been highly conserved throughout evolution, others clearly differ in plants, perhaps reflecting adaptations to different lifestyles and the rewiring of this primordial signaling module to adapt to specific requirements. Indeed, TOR is involved in plant responses to a vast array of signals including nutrients, hormones, light, stresses or pathogens. In this review, we will summarize recent studies that address the regulations of TOR by nutrients in photosynthetic organisms, and the roles of TOR in controlling important metabolic pathways, highlighting similarities and differences with the other eukaryotes.

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“…1 a). Interestingly, in cnidarians, there are some lineages that show bilateral symmetry [ 1 , 4 , 5 , 9 – 11 ] (Fig. 1 a).…”

Section: Introductionmentioning

confidence: 99%

Polymorphism in the symmetries of gastric pouch arrangements in the sea anemone D. lineata

et al. 2021

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Symmetry in the arrangement of body parts is a distinctive phylogenetic feature of animals. Cnidarians show both bilateral and radial symmetries in their internal organs, such as gastric pouches and muscles. However, how different symmetries appear during the developmental process remains unknown. Here, we report intraspecific variations in the symmetric arrangement of gastric pouches, muscles, and siphonoglyphs, the Anthozoan-specific organ that drives water into the organism, in D. lineata (Diadumenidae, Actiniaria). We found that the positional arrangement of the internal organs was apparently constrained to either biradial or bilateral symmetries depending on the number of siphonoglyphs. Based on the morphological observations, a mathematical model of internal organ positioning was employed to predict the developmental backgrounds responsible for the biradial and bilateral symmetries. In the model, we assumed that the specification of gastric pouches is orchestrated by lateral inhibition and activation, which results in different symmetries depending on the number of siphonoglyphs. Thus, we propose that a common developmental program can generate either bilateral or biradial symmetries depending on the number of siphonoglyphs formed in the early developmental stages.

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Feeding-dependent tentacle development in the sea anemone Nematostella vectensis

Cited by 23 publications

References 55 publications

Tentacle patterning during Exaiptasia diaphana pedal lacerate development differs between symbiotic and aposymbiotic animals

Tentacle patterning during Exaiptasia diaphana pedal lacerate development differs between symbiotic and aposymbiotic animals

The Plant Target of Rapamycin: A Conduc TOR of Nutrition and Metabolism in Photosynthetic Organisms

Polymorphism in the symmetries of gastric pouch arrangements in the sea anemone D. lineata

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