ZSP‐1 is a Z granule surface protein required for Z granule fluidity and germline immortality in Caenorhabditis elegans

• Published in: The EMBO journal Vol. 40; no. 3; pp. e105612 - n/a
• Main Authors: Wan, Gang, Bajaj, Lakshya, Fields, Brandon, Dodson, Anne E, Pagano, Daniel, Fei, Yuhan, Kennedy, Scott
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.02.2021; Springer Nature B.V; John Wiley and Sons Inc
• Subjects: Animals; Blastomeres; Caenorhabditis elegans; Caenorhabditis elegans - genetics; Caenorhabditis elegans - growth & development; Caenorhabditis elegans - metabolism; Caenorhabditis elegans Proteins - chemistry; Caenorhabditis elegans Proteins - genetics; Caenorhabditis elegans Proteins - metabolism; Compartments; Complexity; EMBO36; Fluidity; Gene expression; Gene Expression Regulation, Developmental; Gene regulation; Genetic screening; Germ cells; Germ Cells - growth & development; Germ Cells - metabolism; germ granules; germline immortality; Granular materials; Homeostasis; Liquidity; Membrane Proteins - chemistry; Membrane Proteins - genetics; Membrane Proteins - metabolism; molecular condensates; Morphology; Nematodes; Polyampholytes; Protein Domains; Proteins; Ribonucleic acid; RNA; RNA Interference; RNA, Small Interfering - genetics; siRNA; small RNA; molecular condensates; small RNA; gene regulation; germline immortality; germ granules
• ISSN: 0261-4189; 1460-2075; 1460-2075
• DOI: 10.15252/embj.2020105612

Germ granules are biomolecular condensates that form in germ cells of all/most animals, where they regulate mRNA expression to promote germ cell function and totipotency. In the adult Caenorhabditis elegans germ cell, these granules are composed of at least four distinct sub‐compartments, one of which is the Z granule. To better understand the role of the Z granule in germ cell biology, we conducted a genetic screen for genes specifically required for Z granule assembly or morphology. Here, we show that zsp‐1, which encodes a low‐complexity/polyampholyte‐domain protein, is required for Z granule homeostasis. ZSP‐1 localizes to the outer surface of Z granules. In the absence of ZSP‐1, Z granules swell to an abnormal size, fail to segregate with germline blastomeres during development, and lose their liquid‐like character. Finally, ZSP‐1 promotes piRNA‐ and siRNA‐directed gene regulation and germline immortality. Our data suggest that Z granules coordinate small RNA‐based gene regulation to promote germ cell function and that ZSP‐1 helps/is need to maintain Z granule morphology and liquidity. SYNOPSIS In Caenorhabditis elegans , the Z granule is one of at least four proposed sub‐compartments of the germline perinuclear nuage, which regulates mRNA expression for germ cell function and totipotency. Here, ZSP‐1 is identified as a regulator of Z granules homeostasis. The low‐complexity/polyampholyte‐domain protein ZSP‐1 localizes to the surface of Z granules. Z granule homeostasis requires ZSP‐1, which regulates their morphology and viscosity. ZSP‐1 promotes germline small RNA pathways and germline immortality. Graphical Abstract The Caenorhabditis elegans Z granule surface protein ZSP‐1 maintains Z‐granule morphology and liquidity to regulate small‐RNA‐based gene regulation and promote germline immortality.