Expression of smooth muscle-like effectors and core cardiomyocyte regulators in the contractile papillae of Ciona

Abstract

Background The evolution of vertebrate smooth muscles is obscured by lack of identifiable smooth muscle-like cells in tunicates, the invertebrates most closely related to vertebrates. A recent evolutionary model was proposed in which smooth muscles arose before the last bilaterian common ancestor, and were later diversified, secondarily lost or modified in the branches leading to extant animal taxa. However, there is currently no data from tunicates to support this scenario. Methods and results Here, we show that the axial columnar cells, a unique cell type in the adhesive larval papillae of the tunicate Ciona, are enriched for orthologs of vertebrate smooth/non-muscle-specific effectors of contractility, in addition to developing from progenitors that express conserved cardiomyocyte regulatory factors. We show that these cells contract during the retraction of the Ciona papillae during larval settlement and metamorphosis. Conclusions We propose that the axial columnar cells of Ciona are a myoepithelial cell type required for transducing external stimuli into mechanical forces that aid in the attachment of the motile larva to its final substrate. Furthermore, they share developmental and functional features with vertebrate myoepithelial cells, vascular smooth muscle cells, and cardiomyocytes. We discuss these findings in the context of the proposed models of vertebrate smooth muscle and cardiomyocyte evolution.

A microfluidic device for controlled exposure of transgenic Ciona intestinalis larvae to chemical stimuli demonstrates they can respond to carbon dioxide

“…Our data do not distinguish between mechanosensation and chemosensation as palp reporter 22 activity responded to both stimulus and control treatments, however genomic and molecular evolution data suggest ACCs may be a site for chemosensation and homologous to CO2sensitive vertebrate necklace olfactory neurons. ACCs also express GnRH [14] and we note olfactory placode derived CO 2 -sensing neurons that express GnRH have been identified in zebrafish [57]. This contrasts with the recent suggestion that ACCs may be a non-neural myoepithelial cell type homologous to vertebrate smooth muscle, myoepithelial, and cardiomyocyte cells [14].…”

A muscle-related contractile tissue specified by myocardin-related transcription factor activity in Porifera

“…By each of these metrics, the endopinacoderm falls within the range of variation exhibited by myocytes in other animals. For example, the ascidian Ciona robusta and the annelid Platynereis dumerilii both have striated myocytes that express stMyHC, are regulated by the troponin C/tropomyosin complex, and are developmentally specified by a fast-muscle CoRC as well as smooth muscles that express nmMyHC and are patterned by a slow-muscle CoRC (7,33). The flatworm Schistosoma mansoni, has smooth muscles that express stMyHC, are regulated by MLCK phosphorylation of the RLC, and patterned by a fast-muscle CoRC that includes MyoD (34,35).…”

From neuron to muscle to movement: a complete biomechanical model ofHydracontractile behaviors

“…Hydra’s main muscle cell type is the epitheliomuscular cell (Leclère and Röttinger, 2017) , which has a similar structure to smooth muscle (Balachander et al, 2015) with no striation (Johnson et al, 2020) . The ectodermal epitheliomuscular cells of Hydra display longitudinally oriented processes called myonemes which effect body contraction (Leclère and Röttinger, 2017) .…”

“…We will referto these two calcium signaling pathways as the “slow” and “fast” pathways respectively, based on their typical time scales. Both IP 3 -related calcium release Johnson et al, 2020) and electrical excitability (Holman and Anderson, 1991) are observed in epitheliomuscular cells.…”