Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity

Ozment, Ethan; Tamvacakis, Arianna N; Rosiles-Loeza, Pablo Yamild; Escobar-Hernández, Esteban Elías; Nakanishi, Norihiko

doi:10.7554/elife.74336

Cited by 14 publications

(8 citation statements)

References 115 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Stinging by mobile cnidarians could be subject to different physical demands, such as mechanical disturbance from increased turbulence that could necessitate distinct molecular control. Furthermore, stinging can be influenced by acute factors such as physiological state and various sensory cues, including chemicals, touch, or light ( Pantin, 1942 ; Giebel et al, 1988 ; Thorington and Hessinger, 1988 ; Watson and Hessinger, 1989 ; Plachetzki et al, 2012 ; Ozment et al, 2021 ; Aguilar-Camacho et al, 2023 ). Thus, further inquiry into modulation of stinging across physiological states such as nutritional condition, altered symbiotic relationships, or developmental stages ( Sandberg et al, 1971 ; Columbus-Shenkar et al, 2018 ) could reveal dynamic regulation by synaptic connections, hormones, or modulation of transcriptional or translational programs ( Westfall et al, 1998 ; Westfall et al, 2002 ; Westfall, 2004 ; Weir et al, 2020 ).…”

Section: Discussionmentioning

confidence: 99%

Molecular tuning of sea anemone stinging

Allard

et al. 2023

eLife

View full text Add to dashboard Cite

Jellyfish and sea anemones fire single-use, venom-covered barbs to immobilize prey or predators. We previously showed that the anemone Nematostella vectensis uses a specialized voltage-gated calcium (CaV) channel to trigger stinging in response to synergistic prey-derived chemicals and touch (Weir et al., 2020). Here we use experiments and theory to find that stinging behavior is suited to distinct ecological niches. We find that the burrowing anemone Nematostella uses uniquely strong CaV inactivation for precise control of predatory stinging. In contrast, the related anemone Exaiptasia diaphana inhabits exposed environments to support photosynthetic endosymbionts. Consistent with its niche, Exaiptasia indiscriminately stings for defense and expresses a CaV splice variant that confers weak inactivation. Chimeric analyses reveal that CaVβ subunit adaptations regulate inactivation, suggesting an evolutionary tuning mechanism for stinging behavior. These findings demonstrate how functional specialization of ion channel structure contributes to distinct organismal behavior.

show abstract

Section: Discussionmentioning

confidence: 99%

Molecular tuning of sea anemone stinging

Allard

et al. 2023

eLife

View full text Add to dashboard Cite

show abstract

“…3D, F ), and includes the previously mentioned neuronal population “eN.1” and a population of hair cells ( Fig. S3V-W , (Ozment et al, 2021)).…”

Section: Resultsmentioning

confidence: 99%

“…W) The Insm-negative/POU4-positive domain includes distinct cell populations such as endomesodermal neurons and hair cells. The hair cell marker is polycystin 1 (Ozment et al 2021).…”

Section: Supplemental Figuresmentioning

confidence: 99%

Single cell transcriptomics identifies conserved regulators of neurosecretory lineages

Steger

Cole

Denner

et al. 2022

Preprint

View full text Add to dashboard Cite

SUMMARYCommunication in bilaterian nervous systems is mediated by electrical and secreted signals, however, the evolutionary origin and relation of neurons to other secretory cell types has not been elucidated. Here we use developmental single cell RNA-sequencing in the cnidarian Nematostella vectensis, representing an early evolutionary lineage with a simple nervous system. Validated by transgenics, we demonstrate that neurons, stinging cells, and gland cells arise from a common multipotent progenitor population. We identify the conserved transcription factor gene SoxC as a key upstream regulator of all neurosecretory lineages and demonstrate that SoxC knockdown eliminates both neuronal and secretory cell types. While in vertebrates and many other bilaterians neurogenesis is largely restricted to early developmental stages, we show that in the sea anemone differentiation of neurosecretory cells is maintained throughout all life stages, and follows the same molecular trajectories from embryo to adulthood, ensuring lifelong homeostasis of neurosecretory cell lineages.

show abstract

“…Our analyses indicate that both POU and NRL peak in expression in day 1 planulae. POU transcription factors are ancient (69) and have been implicated in stem cell regulation in H. symbiolongicarpus (70) and in the specification of hair cells in N. vectensis (71). Also highly differentially expressed in day 1 planulae are single transcripts corresponding to human paralogs NR2E1 and NR2E3, and CRX, VSX, and RAX (Fig 3), respectively.…”

Section: Developmental Transcriptomics Implicate Photosensation and S...mentioning

confidence: 99%

Phototactic preference and its genetic basis in the planulae of the colonial Hydrozoan Hydractinia symbiolongicarpus

Birch,

McGee,

Provencher

et al. 2024

Preprint

View full text Add to dashboard Cite

Background Marine organisms with sessile adults commonly possess motile larval stages that make settlement decisions based on integrating environmental sensory cues. Phototaxis, the movement toward or away from light, is a common behavioral characteristic of aquatic and marine metazoan larvae, as well as of algae, protists, and fungi. In cnidarians, behavioral genomic investigations of motile planulae larvae have been conducted in anthozoans (corals and sea anemones) and scyphozoans (true jellyfish), but such studies are presently lacking in hydrozoans. Here, we examined the behavioral genomics of phototaxis in planulae of the hydrozoan Hydractinia symbiolongicarpus. Results A behavioral phototaxis study of day 3 planulae indicated preferential phototaxis to green (523 nm) and blue (470 nm) wavelengths of light, but not red (625 nm) wavelengths. A developmental transcriptome study where planula larvae were collected from four developmental time points for RNA-seq revealed that many genes critical to the physiology and development of ciliary photosensory systems are dynamically expressed in planula development and correspond to the expression of phototactic behavior. Microscopical investigations using immunohistochemistry and in situ hybridization demonstrated that several transcripts with predicted function in photoreceptors, including cnidops class opsin, CNG ion channel, and CRX-like transcription factor, localize to ciliated bipolar sensory neurons of the aboral sensory neural plexus, which is associated with the direction of phototaxis and the site of settlement. Conclusions The phototactic preference displayed by planulae is consistent with the shallow sandy marine habitats they experience in nature. Our genomic investigations add further evidence of similarities between cnidops-mediated photoreceptors of hydrozoans and other cnidarians and ciliary photoreceptors as found in the eyes of humans and other bilaterians, suggesting aspects of their shared evolutionary history.

show abstract

Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity

Cited by 14 publications

References 115 publications

Molecular tuning of sea anemone stinging

Molecular tuning of sea anemone stinging

Single cell transcriptomics identifies conserved regulators of neurosecretory lineages

Phototactic preference and its genetic basis in the planulae of the colonial Hydrozoan Hydractinia symbiolongicarpus

Contact Info

Product

Resources

About