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Soma-to-germline RNA communication

Abstract

More than a century ago, August Weissman defined a distinction between the germline (responsible for propagating heritable information from generation to generation) and the perishable soma. A central motivation for this distinction was to argue against the inheritance of acquired characters, as the germline was partly defined by its protection from external conditions. However, recent decades have seen an explosion of studies documenting the intergenerational and transgenerational effects of environmental conditions, forcing a re-evaluation of how external signals are sensed by, or communicated to, the germline epigenome. Here, motivated by the centrality of small RNAs in paradigms of epigenetic inheritance, we review across species the myriad examples of intercellular RNA trafficking from nurse cells or somatic tissues to developing gametes.

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Fig. 1: Germline niche cells.
Fig. 2: Dead-end germline products.
Fig. 3: Vesicle trafficking from dedicated reproductive support tissues.
Fig. 4: Systemic RNA spread.
Fig. 5: Environmental control of the mammalian sperm epigenome.

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Acknowledgements

The authors thank V. Rinaldi and C. Galan for critical reading of the manuscript, and K. Slotkin and J. McCarrey for helpful discussions. This work was supported by Templeton Foundation Grant 61350 to O.J.R. and a Pew Biomedical Scholars Award to C.C.C.

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Glossary

Selfish genetic elements

DNA sequences that can move within a genome and generate multiple copies, often to the detriment of the host, most famously, transposons.

Balbiani body

A subcellular structure in oocytes comprising mitochondria, endoplasmic reticulum and Golgi membranes, and germ plasm RNAs and proteins.

Endo-replicate

To copy parts of the genome without mitosis, leading either to whole genome polyploidy or to selective amplification of specific genomic loci.

Argonautes

Effector proteins that bind to small RNAs such as short interfering RNAs, microRNAs and PIWI-interacting RNAs, and use these small RNAs to target homologous RNAs such as transposon RNAs.

Syncytium

A structure, often formed by cell fusion or nuclear division without cell division, in which multiple nuclei share the same cytoplasm.

Oolemma

The oocyte membrane.

RNA-directed DNA methylation (RdDM) pathway

A pathway in plants in which small RNAs direct cytosine methylation at genomic target sites.

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Conine, C.C., Rando, O.J. Soma-to-germline RNA communication. Nat Rev Genet (2021). https://doi.org/10.1038/s41576-021-00412-1

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