SPE-44 Implements Sperm Cell Fate

The sperm/oocyte decision in the hermaphrodite germline of Caenorhabditis elegans provides a powerful model for the characterization of stem cell fate specification and differentiation. The germline sex determination program that governs gamete fate has been well studied, but direct mediators of cell-type-specific transcription are largely unknown. We report the identification of spe-44 as a critical regulator of sperm gene expression. Deletion of spe-44 causes sperm-specific defects in cytokinesis, cell cycle progression, and organelle assembly resulting in sterility. Expression of spe-44 correlates precisely with spermatogenesis and is regulated by the germline sex determination pathway. spe-44 is required for the appropriate expression of several hundred sperm-enriched genes. The SPE-44 protein is restricted to the sperm-producing germline, where it localizes to the autosomes (which contain sperm genes) but is excluded from the transcriptionally silent X chromosome (which does not). The orthologous gene in other Caenorhabditis species is similarly expressed in a sex-biased manner, and the protein likewise exhibits autosome-specific localization in developing sperm, strongly suggestive of an evolutionarily conserved role in sperm gene expression. Our analysis represents the first identification of a transcriptional regulator whose primary function is the control of gamete-type-specific transcription in this system.

• Publication year

  2012

• Venue

  PLoS Genetics

• Publication date

  2012-04-01

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1371/journal.pgen.1002678PMID 22570621PMCID 3343087
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• [Caenorhabditis elegans].

  2020cited by this paper
• Phosphorylation state of a Tob/BTG protein, FOG-3, regulates initiation and maintenance of the Caenorhabditis elegans sperm fate program

  2011cited by this paper
• Direct Conversion of C. elegans Germ Cells into Specific Neuron Types

  2011cited by this paper
• Spermatogenesis‐defective (spe) mutants of the nematode Caenorhabditis elegans provide clues to solve the puzzle of male germline functions during reproduction

  2010cited by this paper
• The mammalian anti‐proliferative BTG/Tob protein family

  2010cited by this paper
• Aire's partners in the molecular control of immunological tolerance.

  2010cited by this paper
• Spermatogenesis-Specific Features of the Meiotic Program in Caenorhabditis elegans

  2009cited by this paper
• TRA-1/GLI controls the expression of the Hox gene lin-39 during C. elegans vulval development.

  2009cited by this paper
• Dephosphorylation of major sperm protein (MSP) fiber protein 3 by protein phosphatase 2A during cell body retraction in the MSP-based amoeboid motility of Ascaris sperm.

  2009cited by this paper
• Regulation of sperm gene expression by the GATA factor ELT-1.

  2009influential reference
• Chemical reprogramming of Caenorhabditis elegans germ cell fate

  2009cited by this paper
• The SAND domain protein ULTRAPETALA1 acts as a trithorax group factor to regulate cell fate in plants.

  2009cited by this paper
• A sensitized genetic background reveals evolution near the terminus of the Caenorhabditis germline sex determination pathway

  2009cited by this paper
• Towards a mutation in every gene in Caenorhabditis elegans.

  2008influential reference
• dmd-3, a doublesex-related gene regulated by tra-1, governs sex-specific morphogenesis in C. elegans

  2008cited by this paper
• Clustal W and Clustal X version 2.0

  2007cited by this paper
• Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans.

  2007cited by this paper
• Control of sex-specific apoptosis in C. elegans by the BarH homeodomain protein CEH-30 and the transcriptional repressor UNC-37/Groucho.

  2007cited by this paper
• The C. elegans protein CEH-30 protects male-specific neurons from apoptosis independently of the Bcl-2 homolog CED-9.

  2007cited by this paper
• A CUL-2 ubiquitin ligase containing three FEM proteins degrades TRA-1 to regulate C. elegans sex determination.

  2007cited by this paper
• Somatic sex determination.

  2006cited by this paper
• RNA in situ hybridization of dissected gonads.

  2006cited by this paper
• The Caenorhabditis elegans GATA factor elt-1 is essential for differentiation and maintenance of hypodermal seam cells and for normal locomotion

  2005cited by this paper
• Structure of sperm-specific protein SSP-19 from Caenorhabditis elegans.

  2004cited by this paper
• Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss

  2004cited by this paper
• fog-2 and the Evolution of Self-Fertile Hermaphroditism in Caenorhabditis

  2004cited by this paper
• A phylogeny of caenorhabditis reveals frequent loss of introns during nematode evolution.

  2004cited by this paper
• C dil, a Human Gl and S Phase Protein Phosphatase That Associates with Cdk2

  2003cited by this paper
• Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans

  2003influential reference
• Crystal structure and nuclear magnetic resonance analyses of the SAND domain from glucocorticoid modulatory element binding protein-1 reveals deoxyribonucleic acid and zinc binding regions.

  2003cited by this paper
• Mitotic Phosphorylation of Histone H3: Spatio-Temporal Regulation by Mammalian Aurora Kinases

  2002cited by this paper
• X-chromosome silencing in the germline of C. elegans.

  2002cited by this paper
• A Sperm Cytoskeletal Protein That Signals Oocyte Meiotic Maturation and Ovulation

  2001cited by this paper
• The SAND domain structure defines a novel DNA-binding fold in transcriptional regulation

  2001cited by this paper
• Properties of the glucocorticoid modulatory element binding proteins GMEB-1 and -2: potential new modifiers of glucocorticoid receptor transactivation and members of the family of KDWK proteins.

  2000cited by this paper
• A global profile of germline gene expression in C. elegans.

  2000influential reference
• A novel member of the tob family of proteins controls sexual fate in Caenorhabditis elegans germ cells.

  2000cited by this paper
• Mab-3 is a direct tra-1 target gene regulating diverse aspects of C. elegans male sexual development and behavior.

  2000cited by this paper
• CPEB proteins control two key steps in spermatogenesis in C. elegans.

  2000cited by this paper
• TRA-1A regulates transcription of fog-3, which controls germ cell fate in C. elegans.

  2000cited by this paper
• Cloning and characterization of hGMEB1, a novel glucocorticoid modulatory element binding protein

  1999cited by this paper
• The TRA-1A sex determination protein of C. elegans regulates sexually dimorphic cell deaths by repressing the egl-1 cell death activator gene.

  1999cited by this paper
• Interaction of SP100 with HP1 proteins: a link between the promyelocytic leukemia-associated nuclear bodies and the chromatin compartment.

  1998cited by this paper
• The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation.

  1998cited by this paper
• Chromatin components as part of a putative transcriptional repressing complex.

  1998cited by this paper
• Cloning and Characterization of a Novel Binding Factor (GMEB-2) of the Glucocorticoid Modulatory Element*

  1998cited by this paper
• The APECED polyglandular autoimmune syndrome protein, AIRE-1, contains the SAND domain and is probably a transcription factor.

  1998cited by this paper
• ELT-1, a GATA-like transcription factor, is required for epidermal cell fates in Caenorhabditis elegans embryos.

  1997cited by this paper
• Distinct requirements for somatic and germline expression of a generally expressed Caernorhabditis elegans gene.

  1997cited by this paper
• DEAF‐1, a novel protein that binds an essential region in a Deformed response element.

  1996cited by this paper
• The fog-3 gene and regulation of cell fate in the germ line of Caenorhabditis elegans.

  1995cited by this paper
• The Factor Binding to the Glucocorticoid Modulatory Element of the Tyrosine Aminotransferase Gene Is a Novel and Ubiquitous Heteromeric Complex (*)

  1995cited by this paper
• The C. elegans sex-determining gene fem-2 encodes a putative protein phosphatase.

  1995cited by this paper
• Genetic and molecular characterization of the Caenorhabditis elegans spermatogenesis-defective gene spe-17.

  1993cited by this paper
• Molecular cloning and duplication of the nematode sex-determining gene tra-1.

  1993cited by this paper
• Isolation of ORC6, a component of the yeast origin recognition complex by a one-hybrid system.

  1993cited by this paper
• Zinc fingers in sex determination: only one of the two C. elegans Tra-1 proteins binds DNA in vitro.

  1993cited by this paper
• Molecular analysis of the C. elegans sex-determining gene tra-1: a gene encoding two zinc finger proteins.

  1992cited by this paper
• Mutation of a putative sperm membrane protein in Caenorhabditis elegans prevents sperm differentiation but not its associated meiotic divisions

  1992cited by this paper
• Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences.

  1991cited by this paper
• The product of fem-1, a nematode sex-determining gene, contains a motif found in cell cycle control proteins and receptors for cell-cell interactions.

  1990cited by this paper
• fog-1, a regulatory gene required for specification of spermatogenesis in the germ line of Caenorhabditis elegans.

  1990influential reference
• Methods in Yeast Genetics: A Laboratory Course Manual

  1990cited by this paper
• Mutations that disrupt the morphogenesis and localization of a sperm-specific organelle in Caenorhabditis elegans.

  1989cited by this paper
• A unique cytoskeleton associated with crawling in the amoeboid sperm of the nematode, Ascaris suum

  1989cited by this paper
• Analysis of the role of tra-1 in germline sex determination in the nematode Caenorhabditis elegans.

  1989cited by this paper
• [Genetics of Caenorhabditis elegans].

  1989cited by this paper
• MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts.

  1988cited by this paper
• Molecular cloning and transcript analysis of fem-3, a sex-determination gene in Caenorhabditis elegans.

  1988cited by this paper
• Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans.

  1988cited by this paper
• Methods in Yeast Genetics. A Laboratory Course Manual.

  1988cited by this paper
• A genetic analysis of the sex-determining gene, tra-1, in the nematode Caenorhabditis elegans.

  1987cited by this paper
• Sex determination in the nematode C. elegans: analysis of tra-3 suppressors and characterization of fem genes.

  1986influential reference
• Monoclonal antibodies which distinguish certain classes of neuronal and supporting cells in the nervous tissue of the nematode Caenorhabditis elegans

  1985cited by this paper
• A sex-determining gene, fem-1, required for both male and hermaphrodite development in Caenorhabditis elegans.

  1984influential reference
• Monoclonal antibodies to mitotic cells.

  1983cited by this paper
• Identification of a large multigene family encoding the major sperm protein of Caenorhabditis elegans.

  1983cited by this paper
• Sperm morphogenesis in wild-type and fertilization-defective mutants of Caenorhabditis elegans

  1981cited by this paper
• Caenorhabditis elegans fertilization-defective mutants with abnormal sperm.

  1980cited by this paper
• Methods in yeast genetics

  1979cited by this paper
• Spermatogenesis in males of the free-living nematode, Caenorhabditis elegans.

  1978cited by this paper
• Characterization of temperature-sensitive, fertilization-defective mutants of the nematode caenorhabditis elegans.

  1978cited by this paper
• The genetics of Caenorhabditis elegans.

  1974cited by this paper
• and Behavior

  year unknowncited by this paper
• Report 3 0 UTRs Are the Primary Regulators of Gene Expression in the C . elegans Germline

  year unknowncited by this paper

• Identification and Functional Verification of Variants Associated With Clubfoot and Arthrogrypotic Hand Deformation in a Multigeneration Polish Family.

  2025cites this paper
• The novel HRD motif kinase SPE-60 is required for sperm development and motility in Caenorhabditis elegans

  2025cites this paper
• Genome-Wide Temporal Gene Expression Reveals a Post-Reproductive Shift in the Nematode Caenorhabditis briggsae

  2025cites this paper
• Mediator-29 limits Caenorhabditis elegans fecundity

  2025cites this paper
• RNAi-dependent expression of sperm genes in ADL chemosensory neurons is required for olfactory responses in Caenorhabditis elegans

  2024cites this paper
• Analysis of the C. elegans Germline Stem Cell Pool.

  2023cites this paper
• Mechanical force of uterine occupation enables large vesicle extrusion from proteostressed maternal neurons

  2023cites this paper
• C. elegans germ granules sculpt both germline and somatic RNAome

  2023cites this paper
• The Genetics of Fitness Reorganization during the Transition to Multicellularity: The Volvocine regA-like Family as a Model

  2023cites this paper
• NHR-23 and SPE-44 regulate distinct sets of genes during Caenorhabditis elegans spermatogenesis

  2022cites this paper
• Sex Determination in Nematode Germ Cells

  2022cites this paper
• The intrinsically disordered protein SPE-18 promotes localized assembly of MSP in Caenorhabditis elegans spermatocytes

  2021cites this paper
• Subcellular patterns of SPE-6 localization reveal unexpected complexities in Caenorhabditis elegans sperm activation and sperm function

  2021cites this paper
• Functional recovery of the germ line following splicing collapse

  2021cites this paper
• Network analysis in aged C. elegans reveals candidate regulatory genes of ageing

  2021cites this paper
• The intrinsically disordered protein SPE-18 promotes localized assembly of the major sperm protein in C. elegans spermatocytes

  2020influential citation
• Sperm fate is promoted by the mir-44 microRNA family in the Caenorhabditis elegans hermaphrodite germline.

  2020cites this paper
• The conserved molting/circadian rhythm regulator NHR-23/NR1F1 serves as an essential co-regulator of C. elegans spermatogenesis

  2020cites this paper
• Self-sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodes

  2019cites this paper
• Independent evolution of complex development in animals and plants: deep homology and lateral gene transfer

  2019cites this paper
• A study of a novel self-fertility mechanism in the hermaphroditic nematode Rhabditis sp. SB347

  2019influential citation
• Auxin-Mediated Sterility Induction System for Longevity and Mating Studies in Caenorhabditis elegans

  2018influential citation
• Spatial transcriptomics of C. elegans males and hermaphrodites identifies novel fertility genes

  2018influential citation
• Characterizing the role of spe-6 in C. elegans spermatogenesis

  2018cites this paper
• Spatial Transcriptomics of C. elegans Males and Hermaphrodites Identifies Sex-Specific Differences in Gene Expression Patterns.

  2018cites this paper
• A study of a novel self-fertility mechanism in the hermaphroditic nematode Rhabditis sp. SB347

  2017influential citation
• Analysis of the C. elegans Germline Stem Cell Pool.

  2017cites this paper
• Germ cell cysts and simultaneous sperm and oocyte production in a hermaphroditic nematode.

  2017influential citation
• Discovery and Characterization of Novel Sperm Development Patterns in the Nematode Rhabditis Sp. Sb347

  2017cites this paper
• Mapping Challenging Mutations by Whole-Genome Sequencing

  2016influential citation
• A New Player in the Spermiogenesis Pathway of Caenorhabditis elegans

  2015cites this paper
• Genetic and Cytological Analysis of SPE-6, a C. elegans Tau Tubulin Kinase

  2015cites this paper
• CSR-1 and P granules suppress sperm-specific transcription in the C. elegans germline

  2015cites this paper
• Genomic Analyses of Sperm Fate Regulator Targets Reveal a Common Set of Oogenic mRNAs in Caenorhabditis elegans

  2015cites this paper
• The regulation of spermatogenesis and sperm function in nematodes.

  2014cites this paper
• A New Dataset of Spermatogenic vs. Oogenic Transcriptomes in the Nematode Caenorhabditis elegans

  2014influential citation
• The development of sexual dimorphism: studies of the Caenorhabditis elegans male

  2014cites this paper
• Characterisation of Caenorhabditis elegans sperm transcriptome and proteome

  2014cites this paper
• Competence for Chemical Reprogramming of Sexual Fate Correlates with an Intersexual Molecular Signature in Caenorhabditis elegans

  2014cites this paper
• The Specification and Global Reprogramming of Histone Epigenetic Marks during Gamete Formation and Early Embryo Development in C. elegans

  2014cites this paper
• Spermatogenesis.

  2013cites this paper
• Premature Sperm Activation and Defective Spermatogenesis Caused by Loss of spe-46 Function in Caenorhabditis elegans

  2013cites this paper
• Germ Cell Development in C. elegans

  2013cites this paper
• Introducing: New types of Gazette content

  2012cites this paper