Whole-organism cellular gene-expression atlas reveals conserved cell types in the ventral nerve cord of Platynereis dumerilii

The comparative study of cell types is a powerful approach toward deciphering animal evolution. To avoid selection biases, however, comparisons ideally involve all cell types present in a multicellular organism. Here, we use image registration and a newly developed “Profiling by Signal Probability M...

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Published in:	Proceedings of the National Academy of Sciences - PNAS Vol. 114; no. 23; pp. 5878 - 5885
Main Authors:	Vergara, Hernando Martínez, Bertucci, Paola Yanina, Hantz, Peter, Tosches, Maria Antoniett, Achim, Kaia, Vopalensky, Pavel, Arendt, Detlev
Format:	Journal Article
Language:	English
Published:	United States National Academy of Sciences 06-06-2017
Subjects:	Aquatic life Biological Sciences Cells Cerebrospinal fluid COLLOQUIUM PAPERS Comparative studies Differentiation Evolution GATA-1 protein Gene expression Genes Image registration Interneurons Neural tube Neurons Platynereis dumerilii Sackler on Gene Regulatory Networks and Network Models in Development and Evolution Transcription factors Ventral nerve cord Vertebrates evo-devo Kolmer-Agduhr cells ProSPr gene-expression atlas cell-type evolution
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Summary:	The comparative study of cell types is a powerful approach toward deciphering animal evolution. To avoid selection biases, however, comparisons ideally involve all cell types present in a multicellular organism. Here, we use image registration and a newly developed “Profiling by Signal Probability Mapping” algorithm to generate a cellular resolution 3D expression atlas for an entire animal. We investigate three-segmented young worms of the marine annelid Platynereis dumerilii, with a rich diversity of differentiated cells present in relatively low number. Starting from whole-mount expression images for close to 100 neural specification and differentiation genes, our atlas identifies and molecularly characterizes 605 bilateral pairs of neurons at specific locations in the ventral nerve cord. Among these pairs, we identify sets of neurons expressing similar combinations of transcription factors, located at spatially coherent anterior-posterior, dorsal-ventral, and mediallateral coordinates that we interpret as cell types. Comparison with motor and interneuron types in the vertebrate neural tube indicates conserved combinations, for example, of cell types cospecified by Gata1/2/3 and Tal transcription factors. These include V2b interneurons and the central spinal fluid-contacting Kolmer-Agduhr cells in the vertebrates, and several neuron types in the intermediate ventral ganglionic mass in the annelid. We propose that Kolmer-Agduhr cell-like mechanosensory neurons formed part of the mucociliary sole in protostome-deuterostome ancestors and diversified independently into several neuron types in annelid and vertebrate descendants.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by Douglas H. Erwin, Smithsonian National Museum of Natural History, Washington, DC, and accepted by Editorial Board Member Neil H. Shubin February 10, 2017 (received for review August 24, 2016) Author contributions: H.M.V. and D.A. designed research; H.M.V., P.Y.B., and P.H. performed research; H.M.V., P.Y.B., P.H., M.A.T., K.A., and P.V. contributed new reagents/analytic tools; H.M.V. analyzed data; and H.M.V. and D.A. wrote the paper.
ISSN:	0027-8424 1091-6490
DOI:	10.1073/pnas.1610602114