An atlas of spider development at single-cell resolution provides new insights into arthropod embryogenesis

Leite, Daniel J.; Schönauer, Anna; Blakeley, Grace; Harper, Amber; Garcia-Castro, Helena; Baudouin-Gonzalez, Luis; Wang, Ruixun; Sarkis, Naïra; Nikola, Alexander Günther; Koka, Venkata Sai Poojitha; Kenny, Nathan J.; Turetzek, Natascha; Pechmann, Matthias; Solana, Jordi; McGregor, Alistair P.

Abstract

Spiders are a diverse order of chelicerates that diverged from other arthropods over 500 million years ago. Research on spider embryogenesis, particularly studies using the common house spider Parasteatoda tepidariorum, has made important contributions to understanding the evolution of animal development, including axis formation, segmentation, and patterning. However, we lack knowledge about the cells that build spider embryos, their gene expression profiles and fate. Single-cell transcriptomic analyses have been revolutionary in describing these complex landscapes of cellular genetics in a range of animals. Therefore, we carried out single-cell RNA sequencing of P. tepidariorum embryos at stages 7, 8 and 9, which encompass the establishment and patterning of the body plan, and initial differentiation of many tissues and organs. We identified 20 cell clusters, from 18.5 k cells, which were marked by many developmental toolkit genes, as well as a plethora of genes not previously investigated. We found differences in the cell cycle transcriptional signatures, suggestive of different proliferation dynamics, which related to distinctions between endodermal and some mesodermal clusters, compared with ectodermal clusters. We identified many Hox genes as markers of cell clusters, and Hox gene ohnologs were often present in different clusters. This provided additional evidence of sub- and/or neo-functionalisation of these important developmental genes after the whole genome duplication in an arachnopulmonate ancestor (spiders, scorpions, and related orders). We also examined the spatial expression of marker genes for each cluster to generate a comprehensive cell atlas of these embryonic stages. This revealed new insights into the cellular basis and genetic regulation of head patterning, hematopoiesis, limb development, gut development, and posterior segmentation. This atlas will serve as a platform for future analysis of spider cell specification and fate, and studying the evolution of these processes among animals at cellular resolution.

Citation

Leite, D. J., Schönauer, A., Blakeley, G., Harper, A., Garcia-Castro, H., Baudouin-Gonzalez, L., Wang, R., Sarkis, N., Nikola, A. G., Koka, V. S. P., Kenny, N. J., Turetzek, N., Pechmann, M., Solana, J., & McGregor, A. P. (in press). An atlas of spider development at single-cell resolution provides new insights into arthropod embryogenesis. EvoDevo, 15(1), Article 5. https://doi.org/10.1186/s13227-024-00224-4

• Journal Article Type: Article
• Acceptance Date: Apr 15, 2024
• Online Publication Date: May 10, 2024
• Deposit Date: May 13, 2024
• Publicly Available Date: May 13, 2024
• Journal: EvoDevo
• Electronic ISSN: 2041-9139
• Publisher: BioMed Central
• Peer Reviewed: Peer Reviewed
• Volume: 15
• Issue: 1
• Article Number: 5
• DOI: https://doi.org/10.1186/s13227-024-00224-4
• Keywords: Development, Segmentation, Single-cell RNA sequencing, Extra-embryonic, Head patterning, Hox genes, Spider, Parasteatoda tepidariorum, Cell atlas
• Public URL: https://durham-repository.worktribe.com/output/2437579