Close

From spiral cleavage to bilateral symmetry: The developmental cell lineage of the annelid brain

Pavel Vopalensky, Maria Antonietta Tosches, Kaia Achim, Mette Handberg-Thorsager, Detlev Arendt

Preprint posted on 19 February 2018 https://www.biorxiv.org/content/early/2018/02/19/268177

Article now published in BMC Biology at http://dx.doi.org/10.1186/s12915-019-0705-x

An embryological solution to a geometrical problem: the developmental cell lineage of an annelid worm sheds light on the spiralian transition from rotational to bilateral symmetry.

Selected by Erik Clark

Background

Spiralia (aka Lophotrochozoa) is a large clade of marine invertebrates, including important phyla such as annelid worms and molluscs. Due to stereotypic “spiral cleavage” patterns, spiralian embryos exhibit rotational symmetry, but adult spiralians tend to be bilaterally symmetric. This spiral-to-bilateral transition has puzzled embryologists since at least the 1890s, when E. B. Wilson published his pioneering study of the polychaete worm Nereis. Do spirally arranged cells reconfigure their positions by migration, do small numbers of highly-proliferative “bilateral founder” cells take over the embryo, or do cells with non-equivalent lineage histories acquire equivalent identities?

 

Key findings

This study demonstrates that for the annelid brain, the answer is a combination of possibilities two and three. Vopalensky and colleagues carried out time-lapse microscopy of fluorescently labelled, apically-mounted Platynereis dumerilii embryos. (Platynereis, a polychaete worm in the same family as Nereis, is now the premier spiralian model organism.) They were able to track cell divisions until early larval stages, and create a consensus developmental cell lineage of the Platynereis “episphere” (future head). By cross-referencing this lineage tree with gene expression atlases and morphological markers, they could map various cell types onto the tree, and then compare the ancestries of each pair of bilateral clones.

It turns out that the developmental strategy employed by a particular brain region depends on its position within the embryo. In lateral regions, where rotational and mirror-image symmetries align, the pairs of bilateral founder cells tend to represent corresponding lineages from opposing embryonic quadrants. However, in more medial regions, where this is not the case, bilateral founders tend to stem from different lineages within opposing quadrants, or even from separate lineages within the same quadrant. The overall pattern of clonal origins therefore represents an adaptation to the geometrical constraints inherent to spiral cleavage.

 

 

Some examples of bilateral clones (top), and their corresponding lineage trees (bottom). In lateral regions (E), bilateral founders tend to stem from similar lineages, while in medial regions (F,G), the lineages of the founders are often different.

 

Why I chose this preprint

Until recently, spiralians have been relatively neglected by developmental biologists, with much more attention given to their ecdysozoan and deuterostome cousins. However, modern techniques are currently facilitating rapid and exciting advances by Platynereis labs, and these little marine worms are leapfrogging many other model organisms to rank with the likes of C. elegans and Ciona intestinalis as some the best characterised animals on the planet. This preprint, which also serves as an accessible introduction to spiralian development, is a nice example of this trend.

I also thought that this preprint was a fitting one to highlight this month, given the sad passing of John Sulston, who determined the cell lineage of C. elegans. Fluorescent markers and cell tracking algorithms will have made reconstructing the Platynereis cell lineage a less painstaking task than it was for C. elegans, but the usefulness of the resulting knowledge remains the same as ever.

 

Related research

Henry JQ (2014) Spiralian model systems. Int J Dev Biol 58: 389-401.

Bezares-Calderon LA, Berger J, Jasek S, Veraszto C, Mendes S, Guehmann M, Almeda R, Shahidi R, Jekely G (2018) Neural circuitry of a polycystin-mediated hydrodynamic startle response for predator avoidance. bioRxiv doi.org/10.1101/255570

Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64-119.

Tags: annelids, lineage tracing, live-imaging, platynereis, spiralia

Posted on: 16 March 2018

Read preprint (No Ratings Yet)

Have your say

Your email address will not be published. Required fields are marked *

This site uses Akismet to reduce spam. Learn how your comment data is processed.

Sign up to customise the site to your preferences and to receive alerts

Register here

preLists in the developmental biology category:

‘In preprints’ from Development 2022-2023

A list of the preprints featured in Development's 'In preprints' articles between 2022-2023

 



List by Alex Eve, Katherine Brown

preLights peer support – preprints of interest

This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.

 



List by preLights peer support

The Society for Developmental Biology 82nd Annual Meeting

This preList is made up of the preprints discussed during the Society for Developmental Biology 82nd Annual Meeting that took place in Chicago in July 2023.

 



List by Joyce Yu, Katherine Brown

CSHL 87th Symposium: Stem Cells

Preprints mentioned by speakers at the #CSHLsymp23

 



List by Alex Eve

Journal of Cell Science meeting ‘Imaging Cell Dynamics’

This preList highlights the preprints discussed at the JCS meeting 'Imaging Cell Dynamics'. The meeting was held from 14 - 17 May 2023 in Lisbon, Portugal and was organised by Erika Holzbaur, Jennifer Lippincott-Schwartz, Rob Parton and Michael Way.

 



List by Helen Zenner

9th International Symposium on the Biology of Vertebrate Sex Determination

This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.

 



List by Martin Estermann

Alumni picks – preLights 5th Birthday

This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.

 



List by Sergio Menchero et al.

CellBio 2022 – An ASCB/EMBO Meeting

This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.

 



List by Nadja Hümpfer et al.

2nd Conference of the Visegrád Group Society for Developmental Biology

Preprints from the 2nd Conference of the Visegrád Group Society for Developmental Biology (2-5 September, 2021, Szeged, Hungary)

 



List by Nándor Lipták

Fibroblasts

The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!

 



List by Osvaldo Contreras

EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)

A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.

 



List by Alex Eve

EMBL Conference: From functional genomics to systems biology

Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020

 



List by Jesus Victorino

Single Cell Biology 2020

A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.

 



List by Alex Eve

Society for Developmental Biology 79th Annual Meeting

Preprints at SDB 2020

 



List by Irepan Salvador-Martinez, Martin Estermann

FENS 2020

A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020

 



List by Ana Dorrego-Rivas

Planar Cell Polarity – PCP

This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.

 



List by Ana Dorrego-Rivas

Cell Polarity

Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.

 



List by Yamini Ravichandran

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

 



List by Maiko Kitaoka et al.

3D Gastruloids

A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Updated until July 2021.

 



List by Paul Gerald L. Sanchez and Stefano Vianello

ASCB EMBO Annual Meeting 2019

A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)

 



List by Madhuja Samaddar et al.

EDBC Alicante 2019

Preprints presented at the European Developmental Biology Congress (EDBC) in Alicante, October 23-26 2019.

 



List by Sergio Menchero et al.

EMBL Seeing is Believing – Imaging the Molecular Processes of Life

Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019

 



List by Dey Lab

SDB 78th Annual Meeting 2019

A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.

 



List by Alex Eve

Lung Disease and Regeneration

This preprint list compiles highlights from the field of lung biology.

 



List by Rob Hynds

Young Embryologist Network Conference 2019

Preprints presented at the Young Embryologist Network 2019 conference, 13 May, The Francis Crick Institute, London

 



List by Alex Eve

Pattern formation during development

The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.

 



List by Alexa Sadier

BSCB/BSDB Annual Meeting 2019

Preprints presented at the BSCB/BSDB Annual Meeting 2019

 



List by Dey Lab

Zebrafish immunology

A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.

 



List by Shikha Nayar
Close