Cadherin preserves cohesion across involuting tissues during C. elegans neurulation

Abstract

The internalization of the central nervous system, termed neurulation in vertebrates, is a critical step in embryogenesis. Open questions remain regarding how force propels coordinated tissue movement during the process, and little is known as to how internalization happens in invertebrates. We show that in C. elegans morphogenesis, apical constriction in the retracting pharynx drives involution of the adjacent neuroectoderm. HMR-1/cadherin mediates this process via inter-tissue attachment, as well as cohesion within the neuroectoderm. Our results demonstrate that HMR-1 is capable of mediating embryo-wide reorganization driven by a centrally located force generator, and indicate a non-canonical use of cadherin on the basal side of an epithelium that may apply to vertebrate neurulation. Additionally, we highlight shared morphology and gene expression in tissues driving involution, which suggests that neuroectoderm involution in C. elegans is potentially homologous with vertebrate neurulation and thus may help elucidate the evolutionary origin of the brain.

Cross-modality Synthesis of EM Time Series and Live Fluorescence Imaging

“…All scale bars 1 μm. (a) FM cross section of a comma stage embryo with a ubiquitous histone marker (red) and a broadly expressed cell membrane label (green) 31 . Anterior view.…”

“…While the scale of the ensemble models is fairly constant over the developmental stages, the consistent adjacency graph that guides alignment is dynamic (Fig. S4a), only 146 adjacencies, about a third of consistent adjacencies, are observed at all three periods due to both inconsistent landmarks and embryo-wide cell movements during organ morphogenesis and body elongation 31 . The result is a single-cell level alignment between the FM and EM series, with a predicted identity for each cell in the EM series (Fig.…”

“…Since cells are typically identified in EM based on specialized adult morphologies it is challenging to identify cells in the embryo during their emergence. Instead, significant work using live FM has examined C. elegans embryogenesis, providing insight into neurulation 30,31 , organogenesis 32,33 , neuropil formation 29,[34][35][36][37] , synaptic specificity 38 , as well as lineage differentiation and brain asymmetry [39][40][41] . Lineage tracing in FM establishes definitive identities for cells via ancestry even when they lack distinctive positions or morphologies 35,42 and light sheet microscopy allows imaging to extend into embryonic motion 43 .…”

Cross-modality synthesis of EM time series and live fluorescence imaging

“…However, since neurons are typically identified in EM based on specialized adult morphologies it is challenging to identify them in the embryo during their emergence. It is primarily work using live FM that has examined the C. elegans nervous system during embryogenesis, providing insight into neurulation ( Shah et al, 2017b ; Barnes et al, 2020 ), organogenesis ( Low et al, 2019 ; Fan et al, 2019 ), neuropil formation ( Moyle et al, 2021 ; Rapti et al, 2017 ; Kennerdell et al, 2009 ; Shah et al, 2017a ; Sengupta et al, 2021 ), synaptic specificity ( Berghoff, 2021 ), as well as lineage differentiation and brain asymmetry ( Chuang et al, 2007 ; Cochella and Hobert, 2012 ; Masoudi et al, 2021 ). Lineage tracing in FM establishes definitive identities for cells via ancestry even when they lack distinctive positions or morphologies ( Shah et al, 2017a ; Bao et al, 2006 ) and light sheet microscopy allows imaging to extend into embryonic motion ( Wu et al, 2013 ).…”

Stereotyped Behavioral Maturation and Rhythmic Quiescence in C. elegans Embryos

“…Embryos are small (~50x30x30 µm 3 ) and transparent, enabling in vivo imaging of cell migration, neurite growth, synaptogenesis, neuronal activity, and behavior during the mere ~14 hours from fertilization to hatching (Shah et al, 2017;Barnes et al, 2020;Heiman & Shaham, 2009;Fan et al, 2019;Christensen et al, 2015;McDonald et al, 2020;Sengupta et al, 2020;Ardiel et al, 2017;Hall & Hedgecock, 1991;Atakan et al, 2020;Bayer et al, 2021). C. elegans boasts a sophisticated molecular genetic toolkit, a complete neuronal wiring diagram, and a comprehensive atlas of single cell gene expression across embryogenesis (White et al, 1986;Cook et al, 2019;Witvliet et al, 2021;Packer et al, 2019).…”