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Evolutionary assembly of cooperating cell types in an animal chemical defense system

Brückner, Adrian and Badroos, Jean M. and Learsch, Robert W. and Yousefelahiyeh, Mina and Kitchen, Sheila A. and Parker, Joseph (2021) Evolutionary assembly of cooperating cell types in an animal chemical defense system. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20210517-122046843

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Abstract

A long-standing challenge in biology is explaining how the functions of multicellular organs emerge from the underlying evolution of cell types. We deconstructed evolution of an organ novelty: a rove beetle gland that secretes a defensive cocktail. We show that gland function was pieced together via assembly of two cell types that manufacture distinct compounds. One cell type forms a chemical reservoir in the beetle’s abdomen and produces alkane and ester compounds. We demonstrate that this cell type is a hybrid of cuticle cells and ancient pheromone and adipocyte-like cells, and executes its function via a mosaic of enzymes sourced from each parental cell type. The second cell type synthesizes noxious benzoquinones using a chimeric pathway derived from conserved cellular energy and cuticle formation pathways. We present evidence that evolution of each cell type was shaped by coevolution between the two cell types: the benzoquinones produced by the second cell type dissolve in solvents produced by the first, yielding a potent secretion that confers adaptive value onto the gland as a whole. Our findings illustrate how cooperation between cell types can arise, generating new, organ-level behaviors.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2021.05.13.444042DOIDiscussion Paper
https://doi.org/10.22002/D1.1915DOIProcessed scRNAseq 10x data
https://doi.org/10.22002/D1.1900DOIProcessed SMARTseq data
https://doi.org/10.22002/D1.1905DOIRaw rheology video data
https://doi.org/10.22002/D1.1914DOITranscriptome data
https://doi.org/10.22002/D1.1917DOIRNAi experiments, survival assays, in vitro enzyme data
https://doi.org/10.22002/D1.1916DOIAlignment and tree fasta files
https://doi.org/10.22002/D1.1918DOICode
ORCID:
AuthorORCID
Brückner, Adrian0000-0002-9184-8562
Badroos, Jean M.0000-0002-0867-3686
Learsch, Robert W.0000-0001-6329-5879
Yousefelahiyeh, Mina0000-0003-0365-3018
Kitchen, Sheila A.0000-0003-4402-8139
Parker, Joseph0000-0001-9598-2454
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. This version posted May 15, 2021. Data and code availability: Data availability: Raw sequence reads related to this manuscript have been deposited on NCBI under the BioProject ‘RNAseq (10x and SMARTseq) of the tergal gland of Dalotia coriaria’ (Accession: PRJNA707010; ID: 707010). All other data was uploaded to CaltechData: https://doi.org/10.22002/D1.1915 (processed scRNAseq 10x data), https://doi.org/10.22002/D1.1900 (processed SMARTseq data), https://doi.org/10.22002/D1.1905 (raw rheology video data), https://doi.org/10.22002/D1.1914 (transcriptome data), https://doi.org/10.22002/D1.1917 (RNAi experiments, survival assays, in vitro enzyme data), and https://doi.org/10.22002/D1.1916 (alignment and tree fasta files). Data analysis and visualization software: Analysis and visualization of transcriptomic data were performed using Python 3.0 (Van Rossum, 2000) and R v.3.6.0 (Team and others, 2013) assisted by JupyterLab (Kluyver et al., 2016). The following R packages were used: AnnotationForge (Carlson and Pages, 2019), AnnotationHub (Morgan et al., 2019), biomart (Durinck et al., 2009) boot (Canty and Ripley, 2017), BUSpaRse (Moses and Pachter, 2021) car (Fox et al., 2012), clusterProfiler (Yu et al., 2012), cowplot (Wilke, 2017), data.table (Dowle et al., 2019), dbplyr (Wickham and Ruiz, 2019), DropletUtils (Lun et al., 2019) effects (Fox, 2003), ggplot2 (Wickham, 2011), lattice (Sarkar, 2008), lme4 (Bates et al., 2007), MASS (Ripley et al., 2013) Matrix (Bates and Maechler, 2010), nlme (Pinheiro et al., 2007), randomForest (Liaw and Wiener, 2002), Seurat v3 (Stuart et al., 2019) sleuth (Pimentel et al., 2017), tidyverse (Wickham et al., 2019), vcd (Meyer et al., 2020). Code availability: Detailed code for scRNAseq analyses with Seurat and cNMF; video analyses of rheology data; custom R scripts for SMARTseq analyses via sleuth, GOterm assignments and survival data analysis can be found on CaltechData (https://doi.org/10.22002/D1.1918). All other statistical comparisons using ANOVAs, Kruskal-Wallis tests, U-tests and simple ordinations were done in Past 3.04 (Hammer et al., 2001).
Record Number:CaltechAUTHORS:20210517-122046843
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210517-122046843
Official Citation:Evolutionary assembly of cooperating cell types in an animal chemical defense system. Adrian Brückner, Jean M. Badroos, Robert W. Learsch, Mina Yousefelahiyeh, Sheila A. Kitchen, Joseph Parker. bioRxiv 2021.05.13.444042; doi: https://doi.org/10.1101/2021.05.13.444042
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:109150
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:17 May 2021 20:04
Last Modified:17 May 2021 20:04

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