SNPC-1.3 is a sex-specific transcription factor that drives male piRNA expression in C. elegans

Piwi-interacting RNAs (piRNAs) play essential roles in silencing repetitive elements to promote fertility in metazoans. Studies in worms, flies, and mammals reveal that piRNAs are expressed in a sex-specific manner. However, the mechanisms underlying this sex-specific regulation are unknown. Here we...

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Main Authors: Charlotte P Choi, Rebecca J Tay, Margaret R Starostik, Suhua Feng, James J Moresco, Brooke E Montgomery, Emily Xu, Maya A Hammonds, Michael C Schatz, Taiowa A Montgomery, John R Yates III, Steven E Jacobsen, John K Kim
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/60681
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spelling doaj-034abfc8c9fd447491aed156f688b3272021-05-05T22:46:58ZengeLife Sciences Publications LtdeLife2050-084X2021-02-011010.7554/eLife.60681SNPC-1.3 is a sex-specific transcription factor that drives male piRNA expression in C. elegansCharlotte P Choi0https://orcid.org/0000-0002-1857-6599Rebecca J Tay1https://orcid.org/0000-0002-2270-0505Margaret R Starostik2https://orcid.org/0000-0002-5274-2765Suhua Feng3James J Moresco4Brooke E Montgomery5Emily Xu6Maya A Hammonds7Michael C Schatz8Taiowa A Montgomery9https://orcid.org/0000-0001-7857-3253John R Yates III10https://orcid.org/0000-0001-5267-1672Steven E Jacobsen11John K Kim12https://orcid.org/0000-0001-9838-3254Department of Biology, Johns Hopkins University, Baltimore, United StatesDepartment of Biology, Johns Hopkins University, Baltimore, United StatesDepartment of Biology, Johns Hopkins University, Baltimore, United StatesDepartment of Molecular, Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, United States; Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research, University of California, Los Angeles, Los Angeles, United StatesCenter for the Genetics of Host Defense, University of Texas Southwestern Medical Center, Dallas, United StatesDepartment of Biology, Colorado State University, Fort Collins, United StatesDepartment of Biology, Johns Hopkins University, Baltimore, United StatesDepartment of Biology, Johns Hopkins University, Baltimore, United StatesDepartment of Biology, Johns Hopkins University, Baltimore, United States; Department of Computer Science, Johns Hopkins University, Baltimore, United StatesDepartment of Biology, Colorado State University, Fort Collins, United StatesDepartment of Molecular Medicine, The Scripps Research Institute, La Jolla, United StatesDepartment of Molecular, Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, United States; Howard Hughes Medical Institute, University of California, Los Angeles, Los Angeles, United StatesDepartment of Biology, Johns Hopkins University, Baltimore, United StatesPiwi-interacting RNAs (piRNAs) play essential roles in silencing repetitive elements to promote fertility in metazoans. Studies in worms, flies, and mammals reveal that piRNAs are expressed in a sex-specific manner. However, the mechanisms underlying this sex-specific regulation are unknown. Here we identify SNPC-1.3, a male germline-enriched variant of a conserved subunit of the small nuclear RNA-activating protein complex, as a male-specific piRNA transcription factor in Caenorhabditis elegans. SNPC-1.3 colocalizes with the core piRNA transcription factor, SNPC-4, in nuclear foci of the male germline. Binding of SNPC-1.3 at male piRNA loci drives spermatogenic piRNA transcription and requires SNPC-4. Loss of snpc-1.3 leads to depletion of male piRNAs and defects in male-dependent fertility. Furthermore, TRA-1, a master regulator of sex determination, binds to the snpc-1.3 promoter and represses its expression during oogenesis. Loss of TRA-1 targeting causes ectopic expression of snpc-1.3 and male piRNAs during oogenesis. Thus, sexually dimorphic regulation of snpc-1.3 expression coordinates male and female piRNA expression during germline development.https://elifesciences.org/articles/60681piRNAspermatogenesissex determinationgermline developmentTRA-1transcription
collection DOAJ
language English
format Article
sources DOAJ
author Charlotte P Choi
Rebecca J Tay
Margaret R Starostik
Suhua Feng
James J Moresco
Brooke E Montgomery
Emily Xu
Maya A Hammonds
Michael C Schatz
Taiowa A Montgomery
John R Yates III
Steven E Jacobsen
John K Kim
spellingShingle Charlotte P Choi
Rebecca J Tay
Margaret R Starostik
Suhua Feng
James J Moresco
Brooke E Montgomery
Emily Xu
Maya A Hammonds
Michael C Schatz
Taiowa A Montgomery
John R Yates III
Steven E Jacobsen
John K Kim
SNPC-1.3 is a sex-specific transcription factor that drives male piRNA expression in C. elegans
eLife
piRNA
spermatogenesis
sex determination
germline development
TRA-1
transcription
author_facet Charlotte P Choi
Rebecca J Tay
Margaret R Starostik
Suhua Feng
James J Moresco
Brooke E Montgomery
Emily Xu
Maya A Hammonds
Michael C Schatz
Taiowa A Montgomery
John R Yates III
Steven E Jacobsen
John K Kim
author_sort Charlotte P Choi
title SNPC-1.3 is a sex-specific transcription factor that drives male piRNA expression in C. elegans
title_short SNPC-1.3 is a sex-specific transcription factor that drives male piRNA expression in C. elegans
title_full SNPC-1.3 is a sex-specific transcription factor that drives male piRNA expression in C. elegans
title_fullStr SNPC-1.3 is a sex-specific transcription factor that drives male piRNA expression in C. elegans
title_full_unstemmed SNPC-1.3 is a sex-specific transcription factor that drives male piRNA expression in C. elegans
title_sort snpc-1.3 is a sex-specific transcription factor that drives male pirna expression in c. elegans
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-02-01
description Piwi-interacting RNAs (piRNAs) play essential roles in silencing repetitive elements to promote fertility in metazoans. Studies in worms, flies, and mammals reveal that piRNAs are expressed in a sex-specific manner. However, the mechanisms underlying this sex-specific regulation are unknown. Here we identify SNPC-1.3, a male germline-enriched variant of a conserved subunit of the small nuclear RNA-activating protein complex, as a male-specific piRNA transcription factor in Caenorhabditis elegans. SNPC-1.3 colocalizes with the core piRNA transcription factor, SNPC-4, in nuclear foci of the male germline. Binding of SNPC-1.3 at male piRNA loci drives spermatogenic piRNA transcription and requires SNPC-4. Loss of snpc-1.3 leads to depletion of male piRNAs and defects in male-dependent fertility. Furthermore, TRA-1, a master regulator of sex determination, binds to the snpc-1.3 promoter and represses its expression during oogenesis. Loss of TRA-1 targeting causes ectopic expression of snpc-1.3 and male piRNAs during oogenesis. Thus, sexually dimorphic regulation of snpc-1.3 expression coordinates male and female piRNA expression during germline development.
topic piRNA
spermatogenesis
sex determination
germline development
TRA-1
transcription
url https://elifesciences.org/articles/60681
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