Amphioxus neuroglia: Molecular characterization and evidence for early compartmentalization of the developing nerve cord

Abstract

Glial cells play important roles in the development and homeostasis of metazoan nervous systems. However, while their involvement in the development and function in the central nervous system (CNS) of vertebrates is increasingly well understood, much less is known about invertebrate glia and the evolutionary history of glial cells more generally. An investigation into amphioxus glia is therefore timely, as this organism is the best living proxy for the last common ancestor of all chordates, and hence provides a window into the role of glial cell development and function at the transition of invertebrates and vertebrates. We report here our findings on amphioxus glia as characterized by molecular probes correlated with anatomical data at the transmission electron microscopy (TEM) level. The results show that amphioxus glial lineages express genes typical of vertebrate astroglia and radial glia, and that they segregate early in development, forming what appears to be a spatially separate cell proliferation zone positioned laterally, between the dorsal and ventral zones of neural cell proliferation. Our study provides strong evidence for the presence of vertebrate‐type glial cells in amphioxus, while highlighting the role played by segregated progenitor cell pools in CNS development. There are implications also for our understanding of glial cells in a broader evolutionary context, and insights into patterns of precursor cell deployment in the chordate nerve cord.

Functional Conservation and Genetic Divergence of Chordate Glycinergic Neurotransmission: Insights from Amphioxus Glycine Transporters

“…We retrieved additional sequences compared to previous work [30] and report their developmental expression patterns in the amphioxus Branchiostoma lanceolatum. Based on an updated phylogeny of deuterostome glycine transporters, this analysis revealed expression of amphioxus glycine transporters in neurons and glial cells, further strengthening the previously proposed homology of amphioxus and vertebrate glial cell populations [36]. However, we found the paralog-specific expression domains of amphioxus and vertebrate glycine transporter genes to be inversed, hinting at a particularly complex evolutionary history of this gene family.…”

“…Cross-sections of the rhombospinal region of the nerve cord (Fig. 4K-M) showed that GlyT2.1 was expressed by floor plate and ventrolateral ependymal cells [36]. In L1 larvae, GlyT2.1 was faintly expressed in dorsal cells located posteriorly to the frontal eye complex (Fig.…”

“…8A,B). The anterior part of the rhombospinal region, spanning approximately the CNS territory between somites 2 and 4, recently shown to possess a stereotyped dorsoventral organization of neural and glial compartments [36]. Virtually all the ventrolateral cells are neurons and the mediolateral and floor plate cells are glial cells with marked similarities to vertebrate astroglia (Fig.…”

“…The neurochemistry of the amphioxus nervous system is similar to that of vertebrates [34,35]. Of particular interest is the presence of evenly-spaced groups of glycinergic neurons in the rhombospinal regions, at the level of somites 2 to 5, with the first two groups also containing GA-BAergic neurons [34] and astroglia-like cells being abundant in the whole rhombospinal region [36]. Here, we analyzed the genome of three amphioxus species to characterize the glycine transporter repertoire of cephalochordates.…”

JNK Mediates Differentiation, Cell Polarity and Apoptosis During Amphioxus Development by Regulating Actin Cytoskeleton Dynamics and ERK Signalling

“…Recent research in amphioxus has provided considerable knowledge on the mechanisms underlying axial patterning, germline formation, nervous system development, regeneration, genome architecture, and gene regulation (Somorjai et al, 2012a,b;Marlétaz et al, 2018;Lin et al, 2020;Bozzo et al, 2021). Much of this has been facilitated by recent advances in "omics, " including transcriptomics, genomics and single cell, and the advancement of new methodologies including knockdown and microscopy (Escrivà, 2018).…”