Abstract
How genes are regulated to produce the correct assortment of proteins for every cell type is a fundamental question in biology. For many genes, regulation begins at the DNA level with the use of promoter sequences to control transcription. Regulation can also occur after transcription using sequences in the 3' untranslated region (UTR) of the mRNA to affect mRNA stability and/or translation [1]. The C. elegans gonad is an excellent tissue to study gene regulation during development: In the adult, germ cells are arranged in order of differentiation, with undifferentiated progenitors at one end of the gonad, cells in meiotic prophase in the middle, and gametes at the other end [2]. Using a transgenic assay, we have compared the contribution of promoters and 3' UTRs to gene regulation during germline development. We find that for most genes tested, 3' UTRs are sufficient for regulation. With the exception of promoters activated during spermatogenesis, promoters are permissive for expression in all germ cell types (from progenitors to oocytes and sperm). In progenitors, 3' UTRs inhibit the production of meiotic and oocyte proteins by posttranscriptional mechanisms involving PUF- and KH-domain RNA-binding proteins. Our findings indicate that many genes rely primarily on 3' UTRs, not promoters, for regulation during germline development.
MeSH Terms
3' Untranslated Regions/metabolism
Animals
Caenorhabditis elegans
Gene Expression Regulation, Developmental
Germ Cells/metabolism
Male
Promoter Regions, Genetic
RNA Processing, Post-Transcriptional
RNA, Messenger/metabolism
RNA-Binding Proteins/metabolism
Spermatogenesis
Spermatozoa/metabolism
Chemicals
3' Untranslated Regions
RNA, Messenger
RNA-Binding Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Merritt Christopher
Department of Molecular Biology and Genetics, Howard Hughes Medical Institute, Center for Cell Dynamics, Johns Hopkins School of Medicine, Baltimore, Maryland 21205, USA.
Rasoloson Dominique
Ko Darae
Seydoux Geraldine
References (31)
31 references, click to expand
-
Translational repression restricts expression of the C. elegans Nanos homolog NOS-2 to the embryonic germline.
Dev Biol. 2006 Apr 1;292(1):244-52
PMID: 16499902
-
Translational regulators maintain totipotency in the Caenorhabditis elegans germline.
Science. 2006 Feb 10;311(5762):851-3
PMID: 16469927
-
Promotion of oogenesis and embryogenesis in the C. elegans gonad by EFL-1/DPL-1 (E2F) does not require LIN-35 (pRB).
Development. 2006 Aug;133(16):3147-57
PMID: 16854972
-
The GLD-2 poly(A) polymerase activates gld-1 mRNA in the Caenorhabditis elegans germ line.
Proc Natl Acad Sci U S A. 2006 Oct 10;103(41):15108-12
PMID: 17012378
-
Pathway to totipotency: lessons from germ cells.
Cell. 2006 Dec 1;127(5):891-904
PMID: 17129777
-
Developmental expression of FOG-1/CPEB protein and its control in the Caenorhabditis elegans hermaphrodite germ line.
Dev Dyn. 2007 Mar;236(3):871-9
PMID: 17279572
-
High-throughput in vivo analysis of gene expression in Caenorhabditis elegans.
PLoS Biol. 2007 Sep;5(9):e237
PMID: 17850180
-
Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans.
Annu Rev Cell Dev Biol. 2007;23:405-33
PMID: 17506698
-
A universal framework for regulatory element discovery across all genomes and data types.
Mol Cell. 2007 Oct 26;28(2):337-50
PMID: 17964271
-
Germline proliferation and its control.
WormBook. 2005;:1-14
PMID: 18050413
-
Introduction to the germ line.
WormBook. 2005;:1-4
PMID: 18050415
-
Germline genomics.
WormBook. 2006;:1-10
PMID: 18050476
-
RNA-binding proteins.
WormBook. 2006;:1-13
PMID: 18050487
-
Sex determination in the germ line.
WormBook. 2007;:1-13
PMID: 18050498
-
Revealing posttranscriptional regulatory elements through network-level conservation.
PLoS Comput Biol. 2005 Dec;1(7):e69
PMID: 16355253
-
elt-1, a gene encoding a Caenorhabditis elegans GATA transcription factor, is highly expressed in the germ lines with msp genes as the potential targets.
Mol Cells. 1999 Oct 31;9(5):535-41
PMID: 10597043
-
Intercistronic region required for polycistronic pre-mRNA processing in Caenorhabditis elegans.
Mol Cell Biol. 2001 Feb;21(4):1111-20
PMID: 11158298
-
Creation of low-copy integrated transgenic lines in Caenorhabditis elegans.
Genetics. 2001 Mar;157(3):1217-26
PMID: 11238406
-
Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development.
Genes Dev. 2001 Sep 15;15(18):2408-20
PMID: 11562350
-
A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans.
Nature. 2002 Jun 6;417(6889):660-3
PMID: 12050669
-
Translational repression of a C. elegans Notch mRNA by the STAR/KH domain protein GLD-1.
Development. 2003 Jun;130(12):2623-32
PMID: 12736207
-
The STAR/Maxi-KH domain protein GLD-1 mediates a developmental switch in the translational control of C. elegans PAL-1.
Development. 2004 Jul;131(14):3263-72
PMID: 15201219
-
ATX-2, the C. elegans ortholog of ataxin 2, functions in translational regulation in the germline.
Development. 2004 Oct;131(19):4831-41
PMID: 15342467
-
GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development.
Dev Biol. 1996 Nov 25;180(1):165-83
PMID: 8948583
-
Translational repression of C. elegans p53 by GLD-1 regulates DNA damage-induced apoptosis.
Cell. 2005 Feb 11;120(3):357-68
PMID: 15707894
-
Binding specificity and mRNA targets of a C. elegans PUF protein, FBF-1.
RNA. 2005 Apr;11(4):447-58
PMID: 15769874
-
Systematic discovery of regulatory motifs in human promoters and 3' UTRs by comparison of several mammals.
Nature. 2005 Mar 17;434(7031):338-45
PMID: 15735639
-
Gene regulatory networks for development.
Proc Natl Acad Sci U S A. 2005 Apr 5;102(14):4936-42
PMID: 15788537
-
Histone dynamics in living cells revealed by photobleaching.
DNA Repair (Amst). 2005 Jul 28;4(8):939-50
PMID: 15905138
-
Profiling condition-specific, genome-wide regulation of mRNA stability in yeast.
Proc Natl Acad Sci U S A. 2005 Dec 6;102(49):17675-80
PMID: 16317069
-
LIP-1 phosphatase controls the extent of germline proliferation in Caenorhabditis elegans.
EMBO J. 2006 Jan 11;25(1):88-96
PMID: 16319922