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. Cell, 184 (25). pp. 6138-6156. ISSN 0092-8674. doi:10.1016/j.cell.2021.11.014. https://resolver.caltech.edu/CaltechAUTHORS:20210517-122046843
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Abstract
How the functions of multicellular organs emerge from the underlying evolution of cell types is poorly understood. We deconstructed evolution of an organ novelty: a rove beetle gland that secretes a defensive cocktail. We show how gland function arose via assembly of two cell types that manufacture distinct compounds. One cell type, comprising a chemical reservoir within the abdomen, produces alkane and ester compounds. We demonstrate that this cell type is a hybrid of cuticle cells and ancient pheromone and adipocyte-like cells, executing its function via a mosaic of enzymes from each parental cell type. The second cell type synthesizes benzoquinones using a chimera of conserved cellular energy and cuticle formation pathways. We show that evolution of each cell type was shaped by coevolution between the two cell types, yielding a potent secretion that confers adaptive value. Our findings illustrate how cooperation between cell types arises, generating new, organ-level behaviors.
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| Additional Information: | © 2021 Elsevier Inc. Received 23 June 2021, Revised 29 September 2021, Accepted 10 November 2021, Available online 9 December 2021. We thank Y. Kishi, T. Naragon, J. Wagner, M. Spero, C. VanDrisse, the Bioinformatics Resource Center, and the Single Cell Profiling and Engineering Center (SPEC) in the Beckman Institute at Caltech for assistance with this work. We are grateful to M. Bronner, M. Dickinson and four anonymous reviewers for constructive feedback. A.B. is a Simons Fellow of the Life Sciences Research Foundation (LSRF). This work was supported by a Rita Allen Foundation Scholars Award, an Alfred P. Sloan Research Fellowship, a Shurl and Kay Curci Foundation grant, a Klingenstein-Simons Fellowship Award, and a National Science Foundation CAREER award (NSF 2047472 to J.P.). Author contributions: Conceptualization, J.P. and A.B.; Methodology, J.P. and A.B.; Investigation, A.B., J.M.B., R.W.L., S.A.K., M.Y., and J.P.; Formal Analysis, A.B.; Data Curation, A.B.; Writing – Original Draft, J.P. and A.B.; Writing – Review & Editing, J.P., A.B., and S.A.K.; Supervision, J.P.; Project Administration, J.P.; Funding Acquisition, A.B. and J.P. The authors declare no competing interests. Data and code 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’ (BioProject: PRJNA707010) and ‘Genome and transcriptome sequencing of rove beetles (Staphylinidae)’ (BioProject: PRJNA764224). All other data were uploaded to CaltechData: https://data.caltech.edu/records/1915 (processed scRNaseq 10x data), https://data.caltech.edu/records/1900 (processed SMARTseq data), https://data.caltech.edu/records/1905 (raw rheology video data), https://data.caltech.edu/records/1914 (transcriptome data of Dalotia), https://data.caltech.edu/records/1919 (genomes and transcriptomes of other rove beetles), https://data.caltech.edu/records/1917 (RNAi experiments, survival assays, in vitro enzyme data), and https://data.caltech.edu/records/1916 (alignment and tree fasta files). 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/toxicity data analyses can be found on CaltechData (https://data.caltech.edu/records/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). | |||||||||||||||||||||||||||||||||
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| Subject Keywords: | cell type evolution; biosynthetic pathway evolution; enzyme evolution; organ function; evolution of cooperation; single cell RNAseq; rove beetles; Dalotia coriaria | |||||||||||||||||||||||||||||||||
| Issue or Number: | 25 | |||||||||||||||||||||||||||||||||
| DOI: | 10.1016/j.cell.2021.11.014 | |||||||||||||||||||||||||||||||||
| Record Number: | CaltechAUTHORS:20210517-122046843 | |||||||||||||||||||||||||||||||||
| Persistent URL: | https://resolver.caltech.edu/CaltechAUTHORS:20210517-122046843 | |||||||||||||||||||||||||||||||||
| Official Citation: | Adrian Brückner, Jean M. Badroos, Robert W. Learsch, Mina Yousefelahiyeh, Sheila A. Kitchen, Joseph Parker, Evolutionary assembly of cooperating cell types in an animal chemical defense system, Cell, Volume 184, Issue 25, 2021, Pages 6138-6156.e28, ISSN 0092-8674, https://doi.org/10.1016/j.cell.2021.11.014. (https://www.sciencedirect.com/science/article/pii/S0092867421013295) | |||||||||||||||||||||||||||||||||
| 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: | 05 Jan 2022 22:49 |
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