PIE-1 SUMOylation promotes germline fates and piRNA-dependent silencing in C. elegans.

Heesun Kim,Craig C Mello,Shan Lu,Meng-Qiu Dong,Wendy Tan,Darryl Conte,Yue-He Ding,Mei-Qing Zuo

doi:10.7554/elife.63300

Abstract

Germlines shape and balance heredity, integrating and regulating information from both parental and foreign sources. Insights into how germlines handle information have come from the study of factors that specify or maintain the germline fate. In early Caenorhabditis elegans embryos, the CCCH zinc finger protein PIE-1 localizes to the germline where it prevents somatic differentiation programs. Here, we show that PIE-1 also functions in the meiotic ovary where it becomes SUMOylated and engages the small ubiquitin-like modifier (SUMO)-conjugating machinery. Using whole-SUMO-proteome mass spectrometry, we identify HDAC SUMOylation as a target of PIE-1. Our analyses of genetic interactions between pie-1 and SUMO pathway mutants suggest that PIE-1 engages the SUMO machinery both to preserve the germline fate in the embryo and to promote Argonaute-mediated surveillance in the adult germline.

Highlights

During every life cycle, the eukaryotic germline orchestrates a remarkable set of informational tasks that shape heredity and create variation necessary for the evolution of new species
In a parallel study exploring the role of small ubiquitin-like modifier (SUMO) and nucleosome remodeling and deacetylase (NuRD) complex co-factors in piRNA-mediated silencing in the germline, we found that mutations in smo-1 and ubc-9 activate germline expression of a piRNA pathway reporter (Kim et al, 2021), but null alleles of gei-17 do not (Figure 6B)
We have shown that PIE-1 is expressed in the adult germline where it does not directly inhibit transcription, but rather functions along with components of the SUMO pathway to promote the hypoacetylation of germline chromatin and with the SUMO E3 homolog GEI-17 to promote Piwi Argonuate-dependent gene silencing

Summary

Introduction

The eukaryotic germline orchestrates a remarkable set of informational tasks that shape heredity and create variation necessary for the evolution of new species. Inactivation of maternal mep-1 and let-418 causes a striking developmental arrest of L1-stage larvae, whose somatic cells adopt germline-specific transcriptional programs, and assemble germline-specific peri-nuclear nuage-like structures called P granules (Unhavaithaya et al, 2002). These soma-to-germline transformations depend on the trithoraxrelated protein MES-4 and components of a polycomb repressive complex (PRC2) (MES-2 and MES3) (Unhavaithaya et al, 2002), whose functions are thought to promote fertility by maintaining germline chromatin (Strome and Updike, 2015). Our findings are consistent with a model in which PIE-1 engages SUMO to preserve the embryonic germline fate, and to promote the assembly of a MEP-1/Mi-2/HDA-1 chromatin remodeling complex required for inherited Argonaute-mediated gene silencing in the adult hermaphrodite germline

Results

SUMO LIGASE

GEI-17

E Up-regulated

Discussion

Materials and methods