Cargando…

A Drosophila glial cell atlas reveals a mismatch between transcriptional and morphological diversity

Morphology is a defining feature of neuronal identity. Like neurons, glia display diverse morphologies, both across and within glial classes, but are also known to be morphologically plastic. Here, we explored the relationship between glial morphology and transcriptional signature using the Drosophi...

Descripción completa

Detalles Bibliográficos
Autores principales: Lago-Baldaia, Inês, Cooper, Maia, Seroka, Austin, Trivedi, Chintan, Powell, Gareth T., Wilson, Stephen W., Ackerman, Sarah D., Fernandes, Vilaiwan M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619882/
https://www.ncbi.nlm.nih.gov/pubmed/37862379
http://dx.doi.org/10.1371/journal.pbio.3002328
_version_ 1785130087874560000
author Lago-Baldaia, Inês
Cooper, Maia
Seroka, Austin
Trivedi, Chintan
Powell, Gareth T.
Wilson, Stephen W.
Ackerman, Sarah D.
Fernandes, Vilaiwan M.
author_facet Lago-Baldaia, Inês
Cooper, Maia
Seroka, Austin
Trivedi, Chintan
Powell, Gareth T.
Wilson, Stephen W.
Ackerman, Sarah D.
Fernandes, Vilaiwan M.
author_sort Lago-Baldaia, Inês
collection PubMed
description Morphology is a defining feature of neuronal identity. Like neurons, glia display diverse morphologies, both across and within glial classes, but are also known to be morphologically plastic. Here, we explored the relationship between glial morphology and transcriptional signature using the Drosophila central nervous system (CNS), where glia are categorised into 5 main classes (outer and inner surface glia, cortex glia, ensheathing glia, and astrocytes), which show within-class morphological diversity. We analysed and validated single-cell RNA sequencing data of Drosophila glia in 2 well-characterised tissues from distinct developmental stages, containing distinct circuit types: the embryonic ventral nerve cord (VNC) (motor) and the adult optic lobes (sensory). Our analysis identified a new morphologically and transcriptionally distinct surface glial population in the VNC. However, many glial morphological categories could not be distinguished transcriptionally, and indeed, embryonic and adult astrocytes were transcriptionally analogous despite differences in developmental stage and circuit type. While we did detect extensive within-class transcriptomic diversity for optic lobe glia, this could be explained entirely by glial residence in the most superficial neuropil (lamina) and an associated enrichment for immune-related gene expression. In summary, we generated a single-cell transcriptomic atlas of glia in Drosophila, and our extensive in vivo validation revealed that glia exhibit more diversity at the morphological level than was detectable at the transcriptional level. This atlas will serve as a resource for the community to probe glial diversity and function.
format Online
Article
Text
id pubmed-10619882
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-106198822023-11-02 A Drosophila glial cell atlas reveals a mismatch between transcriptional and morphological diversity Lago-Baldaia, Inês Cooper, Maia Seroka, Austin Trivedi, Chintan Powell, Gareth T. Wilson, Stephen W. Ackerman, Sarah D. Fernandes, Vilaiwan M. PLoS Biol Methods and Resources Morphology is a defining feature of neuronal identity. Like neurons, glia display diverse morphologies, both across and within glial classes, but are also known to be morphologically plastic. Here, we explored the relationship between glial morphology and transcriptional signature using the Drosophila central nervous system (CNS), where glia are categorised into 5 main classes (outer and inner surface glia, cortex glia, ensheathing glia, and astrocytes), which show within-class morphological diversity. We analysed and validated single-cell RNA sequencing data of Drosophila glia in 2 well-characterised tissues from distinct developmental stages, containing distinct circuit types: the embryonic ventral nerve cord (VNC) (motor) and the adult optic lobes (sensory). Our analysis identified a new morphologically and transcriptionally distinct surface glial population in the VNC. However, many glial morphological categories could not be distinguished transcriptionally, and indeed, embryonic and adult astrocytes were transcriptionally analogous despite differences in developmental stage and circuit type. While we did detect extensive within-class transcriptomic diversity for optic lobe glia, this could be explained entirely by glial residence in the most superficial neuropil (lamina) and an associated enrichment for immune-related gene expression. In summary, we generated a single-cell transcriptomic atlas of glia in Drosophila, and our extensive in vivo validation revealed that glia exhibit more diversity at the morphological level than was detectable at the transcriptional level. This atlas will serve as a resource for the community to probe glial diversity and function. Public Library of Science 2023-10-20 /pmc/articles/PMC10619882/ /pubmed/37862379 http://dx.doi.org/10.1371/journal.pbio.3002328 Text en © 2023 Lago-Baldaia et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Methods and Resources
Lago-Baldaia, Inês
Cooper, Maia
Seroka, Austin
Trivedi, Chintan
Powell, Gareth T.
Wilson, Stephen W.
Ackerman, Sarah D.
Fernandes, Vilaiwan M.
A Drosophila glial cell atlas reveals a mismatch between transcriptional and morphological diversity
title A Drosophila glial cell atlas reveals a mismatch between transcriptional and morphological diversity
title_full A Drosophila glial cell atlas reveals a mismatch between transcriptional and morphological diversity
title_fullStr A Drosophila glial cell atlas reveals a mismatch between transcriptional and morphological diversity
title_full_unstemmed A Drosophila glial cell atlas reveals a mismatch between transcriptional and morphological diversity
title_short A Drosophila glial cell atlas reveals a mismatch between transcriptional and morphological diversity
title_sort drosophila glial cell atlas reveals a mismatch between transcriptional and morphological diversity
topic Methods and Resources
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619882/
https://www.ncbi.nlm.nih.gov/pubmed/37862379
http://dx.doi.org/10.1371/journal.pbio.3002328
work_keys_str_mv AT lagobaldaiaines adrosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT coopermaia adrosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT serokaaustin adrosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT trivedichintan adrosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT powellgaretht adrosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT wilsonstephenw adrosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT ackermansarahd adrosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT fernandesvilaiwanm adrosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT lagobaldaiaines drosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT coopermaia drosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT serokaaustin drosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT trivedichintan drosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT powellgaretht drosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT wilsonstephenw drosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT ackermansarahd drosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity
AT fernandesvilaiwanm drosophilaglialcellatlasrevealsamismatchbetweentranscriptionalandmorphologicaldiversity