Genes with spiralian-specific protein motifs are expressed in spiralian ciliary bands

Hiebert, Laurel S.; Klann, Marleen; Passamaneck, Yale J.; Bastin, Benjamin; Schneider, Stephan; Martindale, Mark Q.; Seaver, Elaine C.; Maslakova, Svetlana A.; Lambert, J. David

doi:10.1038/s41467-020-17780-7

Cited by 23 publications

(27 citation statements)

References 72 publications

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“…We observed consistent expression of tektin homologs in the ciliary band cluster across the two stages in C. teleta, and these homologs were previously reported in ciliary bands of P. dumerlii and another annelid Hydroides elegans (Arenas-Mena et al, 2007;Achim et al, 2018). Recent reports show the expression of tektin homologs in the P. dumerilii prototroch, ciliated apical organ, telotroch and two pairs of paratrochs, and axonemal dyenin homologs in all ciliary structures of the mollusk Tritia obsoleta (Wu L. et al, 2020), similar to our findings in C. teleta. This suggests that a role of tektin homologs in the ciliary bands of annelid larval trocophores may have been a conserved feature.…”

Section: Evolutionary Comparisons Of C Teleta Cell Types With Other Annelidssupporting

confidence: 88%

“…This suggests that a role of tektin homologs in the ciliary bands of annelid larval trocophores may have been a conserved feature. A recent report by Wu L. et al (2020) uncovered two spiralian-specific genes expressed in the ciliary bands of most spiralians called lophotrochin and trochin. These genes along with the markers identified in our study provide a valuable resource in further characterization of the origin of ciliary bands within Spiralia.…”

Section: Evolutionary Comparisons Of C Teleta Cell Types With Other Annelidsmentioning

confidence: 99%

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Resolving Transcriptional States and Predicting Lineages in the Annelid Capitella teleta Using Single-Cell RNAseq

Sur

Meyer

2021

Front. Ecol. Evol.

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Evolution and diversification of cell types has contributed to animal evolution. However, gene regulatory mechanisms underlying cell fate acquisition during development remains largely uncharacterized in spiralians. Here we use a whole-organism, single-cell transcriptomic approach to map larval cell types in the annelid Capitella teleta at 24- and 48-h post gastrulation (stages 4 and 5). We identified eight unique cell clusters (undifferentiated precursors, ectoderm, muscle, ciliary-band, gut, neurons, neurosecretory cells, and protonephridia), thus helping to identify uncharacterized molecular signatures such as previously unknown neurosecretory cell markers in C. teleta. Analysis of coregulatory programs in individual clusters revealed gene interactions that can be used for comparisons of cell types across taxa. We examined the neural and neurosecretory clusters more deeply and characterized a differentiation trajectory starting from dividing precursors to neurons using Monocle3 and velocyto. Pseudotime analysis along this trajectory identified temporally-distinct cell states undergoing progressive gene expression changes over time. Our data revealed two potentially distinct neural differentiation trajectories including an early trajectory for brain neurosecretory cells. This work provides a valuable resource for future functional investigations to better understanding neurogenesis and the transitions from neural precursors to neurons in an annelid.

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Section: Evolutionary Comparisons Of C Teleta Cell Types With Other Annelidssupporting

confidence: 88%

Section: Evolutionary Comparisons Of C Teleta Cell Types With Other Annelidsmentioning

confidence: 99%

Resolving Transcriptional States and Predicting Lineages in the Annelid Capitella teleta Using Single-Cell RNAseq

Sur

Meyer

2021

Front. Ecol. Evol.

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“…We observed consistent expression of tektin homologs in the ciliary band cluster across the two stages in C. teleta , and these homologs were previously reported in ciliary bands of P. dumerlii and another annelid Hydroides elegans (Arenas-Mena et al, 2007; Kaia Achim, 2017). Recent reports show the expression of tektin homologs in the P. dumerilii prototroch, ciliated apical organ, telotroch and two pairs of paratrochs, and axonemal dyenin homologs in all ciliary structures of the mollusk Tritia obsoleta (Wu et al, 2020b), similar to our findings in C. teleta . This suggests that a role of tektin homologs in the ciliary bands of annelid larval trocophores may have been a conserved feature.…”

Section: Discussionsupporting

confidence: 91%

“…This suggests that a role of tektin homologs in the ciliary bands of annelid larval trocophores may have been a conserved feature. A recent report by Wu et al, 2020b uncovered two spiralian-specific genes expressed in the ciliary bands of most spiralians called lophotrochin and trochin . These genes along with the markers identified in our study provide a valuable resource in further characterization of the origin of ciliary bands within Spiralia.…”

Section: Discussionmentioning

confidence: 99%

Resolving transcriptional states and predicting lineages in the annelidCapitella teletausing single-cell RNAseq

Sur

Meyer

2020

Preprint

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Evolution and diversification of cell types has contributed to animal evolution. However, gene regulatory mechanisms underlying cell fate acquisition during development remains largely uncharacterized in spiralians. Here we use a whole-organism, single-cell transcriptomic approach to map larval cell types in the annelid Capitella teleta at 24- and 48-hours post gastrulation (stages 4 and 5). We identified eight unique cell clusters (undifferentiated precursors, ectoderm, muscle, ciliary-band, gut, neurons, neurosecretory cells and protonephridia), thus helping to identify previously uncharacterized molecular signatures such as novel neurosecretory cell markers. Analysis of coregulatory programs in individual clusters revealed gene interactions that can be used for comparisons of cell types across taxa. We examined the neural and neurosecretory clusters more deeply and characterized a differentiation trajectory starting from dividing precursors to neurons using Monocle3 and velocyto. Pseudotime analysis along this trajectory identified temporally-distinct cell states undergoing progressive gene expression changes over time. Our data revealed two potentially distinct neural differentiation trajectories including an early trajectory for brain neurosecretory cells. This work provides a valuable resource for future functional investigations to better understanding neurogenesis and the transitions from neural precursors to neurons in an annelid.

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“…derived from specific cells -trochoblasts (Kleinenberg, 1886). A prototroch seems to be a highly conserved structure that is present in Annelida, Mollusca, Entoprocta, Ectoprocta, Nemertea, and Rotifera (Ivanova-Kazas, 1995;Rouse, 1999Rouse, , 2000Nielsen, 2004;Marinković et al, 2020;Wu et al, 2020).…”

Section: Feeding Experimentsmentioning

confidence: 99%

Ciliary bands in the prostomium region of Dimorphilus gyrociliatus (Annelida: Dinophiliformia) and their involvement in food uptake

Fofanova

Voronezhskaya

2021

Invertzool

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A prototroch is a characteristic larval idiosyncratic structure conserved among Lophotrochozoa. It appears as the first prominent structure during embryogenesis, serves for swimming and filter-feeding, then degenerates or is modified after metamorphosis. Using cutting-edge confocal laser scanning microscopy, we investigated the detailed structure of the Dimorphilus gyrociliatus prototroch area and demonstrated that it is much more complex than previously thought. The first row of ciliated cells differentiates at the trochophore stage. By juvenile stage, three rows of ciliated cells are located in the prostomium region: an anterior row of cells with long (14-16 µm) cilia, an intermediate row of cells with short (3-4 µm) cilia, and a posterior row of cells with cilia of middle length (9-10 µm). Each ciliated row consists of two bands of cilia-bearing cells. We suggest that the anterior row represents what is commonly considered a prototroch. At the same time, the intermediate row is considered homologous to the adoral ciliary zone, and the posterior row is considered homologous to the metatroch. Older individuals retain this ciliated apparatus until the last days of their life. With age, cilia in prototroch and metatroch become twice shorter; and the prototroch gets wider, at the end consisting of four lines of ciliated cells. Interestingly, under the inhibition of muscle contraction, the freshly hatched juveniles maintain the ability to uptake food particles. These findings confirm earlier observations showing that D. gyrociliatus uses its complex ciliated apparatus in the prostomial region for filter-feeding in addition to bulbus-scrabbing. Thus, we clarified the organization of the ciliary bands of D. gyrociliatus located in the prostomial region, documented their persistence during ontogenesis, as well as confirmed the participation of the ciliary apparatus in active food intake. These data support the paedomorphic character demonstrated for Dimorphilus gyrociliatus.

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Genes with spiralian-specific protein motifs are expressed in spiralian ciliary bands

Cited by 23 publications

References 72 publications

Resolving Transcriptional States and Predicting Lineages in the Annelid Capitella teleta Using Single-Cell RNAseq

Resolving Transcriptional States and Predicting Lineages in the Annelid Capitella teleta Using Single-Cell RNAseq

Resolving transcriptional states and predicting lineages in the annelidCapitella teletausing single-cell RNAseq

Ciliary bands in the prostomium region of Dimorphilus gyrociliatus (Annelida: Dinophiliformia) and their involvement in food uptake

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