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The Ancient Origin and Function of Germline Cysts

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Syncytia: Origin, Structure, and Functions

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 71))

Abstract

Gamete production in most animal species is initiated within an evolutionarily ancient multicellular germline structure, the germline cyst, whose interconnected premeiotic cells synchronously develop from a single progenitor arising just downstream from a stem cell. Cysts in mice, Drosophila, and many other animals protect developing sperm, while in females, cysts generate nurse cells that guard sister oocytes from transposons (TEs) and help them grow and build a Balbiani body. However, the origin and extreme evolutionary conservation of germline cysts remains a mystery. We suggest that cysts arose in ancestral animals like Hydra and Planaria whose multipotent somatic and germline stem cells (neoblasts) express genes conserved in all animal germ cells and frequently begin differentiation in cysts. A syncytial state is proposed to help multipotent stem cell chromatin transition to an epigenetic state with heterochromatic domains suitable for TE repression and specialized function. Most modern animals now lack neoblasts but have retained stem cells and cysts in their early germlines, which continue to function using this ancient epigenetic strategy.

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Acknowledgments

We thank Dr. Steven DeLuca and Haolong Zhu who carried out the studies in Fig. 1.3a and a′ (DeLuca et al. 2020; Pang et al. 2023). We thank Drs. Qi Yin, Bhawana Bhawana, and Asya Davidian of the Spradling lab for helpful comments on the manuscript.

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Correspondence to Allan C. Spradling .

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© 2024 The Author(s), under exclusive license to Springer Nature Switzerland AG

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Spradling, A.C. (2024). The Ancient Origin and Function of Germline Cysts. In: Kloc, M., Uosef, A. (eds) Syncytia: Origin, Structure, and Functions. Results and Problems in Cell Differentiation, vol 71. Springer, Cham. https://doi.org/10.1007/978-3-031-37936-9_1

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