Skip to main content
SpringerLink
Log in
Book cover

Germ Cell Development in C. elegans pp 41–69Cite as

Sex Determination in the Caenorhabditis elegans Germline

  • Chapter
  • First Online:

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 757))

Abstract

How is sex determined? In the animal kingdom, there are diverse sets of mechanisms for determining organismal sex, with the predominant ones being chromosomally based, either a dominant-acting sex chromosome or the ratio of the number of X chromosome to autosomes, which lead to oocyte-producing females and sperm-producing males. The resulting germline sexual phenotype is often the logical consequence of somatic sex determination. In this respect however, the Caenorhabditis elegans hermaphrodite is different from mammals and Drosophila. In fact in the C. elegans hermaphrodite germline, male gametes are transiently produced in a female body during larval development. To override chromosomal signals, sex determination of germ cells strongly depends on post-transcriptional regulation. A pivotal role for male gamete production (spermatogenesis) is played by the fem-3 mRNA, which is controlled through FBF and other RNA-binding proteins or splicing factors. Thanks to its powerful genetics, transparent body, small size, and the ability to make sperm and oocytes within one individual, C. elegans represents an excellent system to investigate cellular differentiation and post-transcriptional control.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Ahringer J, Kimble J (1991) Control of the sperm-oocyte switch in Caenorhabditis elegans hermaphrodites by the fem-3 3’ untranslated region. Nature 49:346–348

    Google Scholar 

  • Ahringer J, Rosenquist TA, Lawson DN, Kimble J (1992) The Caenorhabditis elegans sex determining gene fem-3 is regulated post-transcriptionally. EMBO J 11:2303–2310

    PubMed  CAS  Google Scholar 

  • Austin J, Kimble J (1987) glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51:589–599

    PubMed  CAS  Google Scholar 

  • Bachorik JL, Kimble J (2005) Redundant control of the Caenorhabditis elegans sperm/oocyte switch by PUF-8 and FBF-1, two distinct PUF RNA-binding proteins. Proc Natl Acad Sci USA 102:10893–10897

    PubMed  CAS  Google Scholar 

  • Baker BS, Wolfner MF (1988) A molecular analysis of doublesex, a bifunctional gene that controls both male and female sexual differentiation in Drosophila melanogaster. Genes Dev 2:477–489

    PubMed  CAS  Google Scholar 

  • Barton MK, Kimble J (1990) fog-1, a regulatory gene required for specification of spermatogenesis in the germ line of Caenorhabditis elegans. Genetics 125:29–39

    PubMed  CAS  Google Scholar 

  • Barton MK, Schedl TB, Kimble J (1987) Gain-of-function mutations of fem-3, a sex-determination gene in Caenorhabditis elegans. Genetics 115:107–119

    PubMed  CAS  Google Scholar 

  • Belfiore M, Mathies LD, Pugnale P, Moulder G, Barstead R, Kimble J, Puoti A (2002) The MEP-1 zinc-finger protein acts with MOG DEAH box proteins to control gene expression via the fem-3 3 ‘ untranslated region in Caenorhabditis elegans. RNA 8:725–739

    PubMed  CAS  Google Scholar 

  • Belfiore M, Pugnale P, Saudan Z, Puoti A (2004) Roles of the C. elegans cyclophilin-like protein MOG-6 in MEP-1 binding and germline fates. Development 131:2935–2945

    PubMed  CAS  Google Scholar 

  • Bell LR, Horabin JI, Schedl P, Cline TW (1991) Positive Autoregulation of Sex-Lethal by Alternative Splicing Maintains the Female Determined State in Drosophila. Cell 65:229–239

    PubMed  CAS  Google Scholar 

  • Berry LW, Westlund B, Schedl T (1997) Germ-line tumor formation caused by activation of glp-1 a Caenorhabditis elegans member of the Notch family of receptors. Development 124(4):925–936

    PubMed  CAS  Google Scholar 

  • Bridges CB (1916) Non-disjunction as proof of the chromosome theory of heredity (concluded). Genetics 1:107–163

    PubMed  CAS  Google Scholar 

  • Carmi I, Kopczynski JB, Meyer BJ (1998) The nuclear hormone receptor SEX-1 is an X-chromosome signal that determines nematode sex. Nature 396:168–173

    PubMed  CAS  Google Scholar 

  • Casper AL, Van Doren M (2009) The establishment of sexual identity in the Drosophila germline. Development 136:3821–3830

    PubMed  CAS  Google Scholar 

  • Chagnovich D, Lehmann R (2001) Poly(A)-independent regulation of maternal hunchback translation in the Drosophila embryo. Proc Natl Acad Sci USA 98:11359–11364

    PubMed  CAS  Google Scholar 

  • Chen P, Ellis RE (2000) TRA-1A regulates transcription of fog-3, which controls germ cell fate in C. elegans. Development 127:3119–3129

    PubMed  CAS  Google Scholar 

  • Chin-Sang ID, Spence AM (1996) Caenorhabditis elegans sex-determining protein FEM-2 is a protein phosphatase that promotes male development and interacts directly with FEM-3. Genes Dev 10:2314–2325

    PubMed  CAS  Google Scholar 

  • Chu DS, Dawes HE, Lieb JD, Chan RC, Kuo AF, Meyer BJ (2002) A molecular link between gene-specific and chromosome-wide transcriptional repression. Genes Dev 16:796–805

    PubMed  CAS  Google Scholar 

  • Ciosk R, DePalma M, Priess JR (2004) ATX-2, the C. elegans ortholog of ataxin 2, functions in translational regulation in the germline. Development 131:4831–4841

    PubMed  CAS  Google Scholar 

  • Clifford R, Lee MH, Nayak S, Ohmachi M, Giorgini F, Schedl T (2000) FOG-2, a novel F-box containing protein, associates with the GLD-1 RNA binding protein and directs male sex determination in the C. elegans hermaphrodite germline. Development 127:5265–5276

    PubMed  CAS  Google Scholar 

  • Cline TW (1978) Two closely linked mutations in Drosophila melanogaster that are lethal to opposite sexes and interact with daughterless. Genetics 90:683–698

    PubMed  CAS  Google Scholar 

  • Cline TW (1984) Autoregulatory functioning of a Drosophila gene-product that establishes and maintains the sexually determined state. Genetics 107:231–277

    PubMed  CAS  Google Scholar 

  • Coschigano KT, Wensink PC (1993) Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila. Genes Dev 7:42–54

    PubMed  CAS  Google Scholar 

  • Crittenden SL, Bernstein DS, Bachorik JL, Thompson BE, Gallegos M, Petcherski AG, Moulder G, Barstead R, Wickens M, Kimble J (2002) A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417:660–663

    PubMed  CAS  Google Scholar 

  • Crittenden SL, Eckmann CR, Wang L, Bernstein DS, Wickens M, Kimble J (2003) Regulation of the mitosis/meiosis decision in the Caenorhabditis elegans germline. Philos Trans R Soc Lond B Biol Sci 358:1359–1362

    PubMed  CAS  Google Scholar 

  • Dawes HE, Berlin DS, Lapidus DM, Nusbaum C, Davis TL, Meyer BJ (1999) Dosage compensation proteins targeted to X chromosomes by a determinant of hermaphrodite fate. Science 284:1800–1804

    PubMed  CAS  Google Scholar 

  • DeLong L, Plenefisch JD, Klein RD, Meyer BJ (1993) Feedback control of sex determination by dosage compensation revealed through Caenorhabditis elegans sdc-3 mutations. Genetics 133:875–896

    PubMed  CAS  Google Scholar 

  • Doniach T (1986) Activity of the sex-determining gene tra-2 is modulated to allow spermatogenesis in the C. elegans hermaphrodite. Genetics 114:53–76

    PubMed  CAS  Google Scholar 

  • Doniach T, Hodgkin J (1984) A sex-determining gene, fem-1, required for both male and hermaphrodite development in Caenorhabditis elegans. Dev Biol 106:223–235

    PubMed  CAS  Google Scholar 

  • Donovan PJ, Stott D, Cairns LA, Heasman J, Wylie CC (1986) Migratory and postmigratory mouse primordial germ cells behave differently in culture. Cell 44:831–838

    PubMed  CAS  Google Scholar 

  • Eckmann CR, Kraemer B, Wickens M, Kimble J (2002) GLD-3, a bicaudal-C homolog that inhibits FBF to control germline sex determination in C. elegans. Dev Cell 3:697–710

    PubMed  CAS  Google Scholar 

  • Eckmann CR, Crittenden SL, Suh N, Kimble J (2004) GLD-3 and control of the mitosis/meiosis decision in the germline of Caenorhabditis elegans. Genetics 168:147–160

    PubMed  CAS  Google Scholar 

  • Ellis RE (2008) Sex determination in the Caenorhabditis elegans germ line. Curr Top Dev Biol 83:41–64

    PubMed  CAS  Google Scholar 

  • Ellis R (2010) The sperm/oocyte decision, a C. elegans perspective. In: Verlhac M-H, Villeneuve A (eds) Oogenesis: the universal process. Wiley, New York

    Google Scholar 

  • Ellis RE, Kimble J (1994) Control of germ cell differentiation in Caenorhabditis elegans. Ciba Found Symp 182:179–188

    PubMed  CAS  Google Scholar 

  • Ellis RE, Kimble J (1995) The fog-3 gene and regulation of cell fate in the germ line of Caenorhabditis elegans. Genetics 139:561–577

    PubMed  CAS  Google Scholar 

  • Ellis R, Schedl T (2007) Sex determination in the germ line. WormBook: 1–13

    Google Scholar 

  • Ewen KA, Koopman P (2010) Mouse germ cell development: from specification to sex determination. Mol Cell Endocrinol 323:76–93

    PubMed  CAS  Google Scholar 

  • Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811

    PubMed  CAS  Google Scholar 

  • Ford CE, Jones KW, Polani PE, De Almeida JC, Briggs JH (1959) A sex-chromosome anomaly in a case of gonadal dysgenesis (Turner’s syndrome). Lancet 1:711–713

    PubMed  CAS  Google Scholar 

  • Francis R, Barton MK, Kimble J, Schedl T (1995a) gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics 139:579–606

    PubMed  CAS  Google Scholar 

  • Francis R, Maine E, Schedl T (1995b) Analysis of the multiple roles of gld-1 in germline development: interactions with the sex determination cascade and the glp-1 signaling pathway. Genetics 139:607–630

    PubMed  CAS  Google Scholar 

  • Gallegos M, Ahringer J, Crittenden S, Kimble J (1998) Repression by the 3’ UTR of fem-3, a sex-determining gene, relies on a ubiquitous mog-dependent control in Caenorhabditis elegans. EMBO J 17:6337–6347

    PubMed  CAS  Google Scholar 

  • Gonzalez AN, Lu H, Erickson JW (2008) A shared enhancer controls a temporal switch between promoters during Drosophila primary sex determination. Proc Natl Acad Sci USA 105:18436–18441

    PubMed  CAS  Google Scholar 

  • Goodwin EB, Okkema PG, Evans TC, Kimble J (1993) Translational regulation of tra-2 by its 3’ untranslated region controls sexual identity in C. elegans. Cell 75:329–339

    PubMed  CAS  Google Scholar 

  • Graham PL, Kimble J (1993) The Mog-1 gene is required for the switch from spermatogenesis to oogenesis in Caenorhabditis Elegans. Genetics 133:919–931

    PubMed  CAS  Google Scholar 

  • Graham PL, Schedl T, Kimble J (1993) More Mog genes that influence the switch from spermatogenesis to oogenesis in the hermaphrodite germ-line of Caenorhabditis elegans. Dev Genet 14:471–484

    PubMed  CAS  Google Scholar 

  • Gubbay J, Collignon J, Koopman P, Capel B, Economou A, Munsterberg A, Vivian N, Goodfellow P, Lovell-Badge R (1990) A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 346:245–250

    PubMed  CAS  Google Scholar 

  • Hamaoka BY, Dann CE 3rd, Geisbrecht BV, Leahy DJ (2004) Crystal structure of Caenorhabditis elegans HER-1 and characterization of the interaction between HER-1 and TRA-2A. Proc Natl Acad Sci USA 101:11673–11678

    PubMed  CAS  Google Scholar 

  • Hansen D, Schedl T (2012) Stem cell proliferation versus meiotic fate decision in C. elegans. Advances in Experimental Medicine and Biology 757:71–99. (Chap. 4, this volume) Springer, New York

    Google Scholar 

  • Hansen D, Hubbard EJ, Schedl T (2004a) Multi-pathway control of the proliferation versus meiotic development decision in the Caenorhabditis elegans germline. Dev Biol 268:342–357

    PubMed  CAS  Google Scholar 

  • Hansen D, Wilson-Berry L, Dang T, Schedl T (2004b) Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development 131:93–104

    PubMed  CAS  Google Scholar 

  • Hargitai B, Kutnyanszky V, Blauwkamp TA, Stetak A, Csankovszki G, Takacs-Vellai K, Vellai T (2009) xol-1, the master sex-switch gene in C. elegans, is a transcriptional target of the terminal sex-determining factor TRA-1. Development 136:3881–3887

    PubMed  CAS  Google Scholar 

  • Harley VR, Goodfellow PN (1994) The biochemical role of Sry in sex determination. Mol Reprod Dev 39:184–193

    PubMed  CAS  Google Scholar 

  • Hodgkin J (1980) More sex-determination mutants of Caenorhabditis elegans. Genetics 96:649–664

    PubMed  CAS  Google Scholar 

  • Hodgkin J (1986) Sex determination in the nematode C. elegans: analysis of tra-3 suppressors and characterization of fem genes. Genetics 114:15–52

    PubMed  CAS  Google Scholar 

  • Hodgkin J (1987) A genetic analysis of the sex-determining gene, tra-1, in the nematode Caenorhabditis elegans. Genes Dev 1:731–745

    PubMed  CAS  Google Scholar 

  • Hodgkin JA, Brenner S (1977) Mutations causing transformation of sexual phenotype in the nematode Caenorhabditis elegans. Genetics 86:275–287

    PubMed  CAS  Google Scholar 

  • Hodgkin J, Zellan JD, Albertson DG (1994) Identification of a candidate primary sex determination locus, fox-1, on the X chromosome of Caenorhabditis elegans. Development 120:3681–3689

    PubMed  CAS  Google Scholar 

  • Hoshijima K, Inoue K, Higuchi I, Sakamoto H, Shimura Y (1991) Control of doublesex alternative splicing by transformer and transformer-2 in Drosophila. Science 252:833–836

    PubMed  CAS  Google Scholar 

  • Hsu V, Zobel CL, Lambie EJ, Schedl T, Kornfeld K (2002) Caenorhabditis elegans lin-45 raf is essential for larval viability, fertility and the induction of vulval cell fates. Genetics 160:481–492

    PubMed  CAS  Google Scholar 

  • Jacobs PA, Strong JA (1959) A case of human intersexuality having a possible XXY sex-determining mechanism. Nature 183:302–303

    PubMed  CAS  Google Scholar 

  • Jager S, Schwartz HT, Horvitz HR, Conradt B (2004) The Caenorhabditis elegans F-box protein SEL-10 promotes female development and may target FEM-1 and FEM-3 for degradation by the proteasome. Proc Natl Acad Sci USA 101:12549–12554

    PubMed  Google Scholar 

  • Jan E, Motzny CK, Graves LE, Goodwin EB (1999) The STAR protein, GLD-1, is a translational regulator of sexual identity in Caenorhabditis elegans. EMBO J 18:258–269

    PubMed  CAS  Google Scholar 

  • Johnson CL, Spence AM (2011) Epigenetic licensing of germline gene expression by maternal RNA in C. elegans. Science 333:1311–1314

    PubMed  CAS  Google Scholar 

  • Jones AR, Francis R, Schedl T (1996) GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. Dev Biol 180:165–183

    PubMed  CAS  Google Scholar 

  • Jungkamp AC, Stoeckius M, Mecenas D, Grun D, Mastrobuoni G, Kempa S, Rajewsky N (2011) In vivo and transcriptome-wide identification of RNA binding protein target sites. Mol Cell 44:828–840

    PubMed  CAS  Google Scholar 

  • Kadyk LC, Kimble J (1998) Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development 125:1803–1813

    PubMed  CAS  Google Scholar 

  • Karashima T, Sugimoto A, Yamamoto M (2000) Caenorhabditis elegans homologue of the human azoospermia factor DAZ is required for oogenesis but not for spermatogenesis. Development 127:1069–1079

    PubMed  CAS  Google Scholar 

  • Kashimada K, Koopman P (2010) Sry: the master switch in mammalian sex determination. Development 137:3921–3930

    PubMed  CAS  Google Scholar 

  • Kasturi P, Zanetti S, Passannante M, Saudan Z, Muller F, Puoti A (2010) The C. elegans sex determination protein MOG-3 functions in meiosis and binds to the CSL co-repressor CIR-1. Dev Biol 344:593–602

    PubMed  CAS  Google Scholar 

  • Kawano T, Kataoka N, Dreyfuss G, Sakamoto H (2004) Ce-Y14 and MAG-1, components of the exon-exon junction complex, are required for embryogenesis and germline sexual switching in Caenorhabditis elegans. Mech Dev 121:27–35

    PubMed  CAS  Google Scholar 

  • Kelly WG, Fire A (1998) Chromatin silencing and the maintenance of a functional germline in Caenorhabditis elegans. Development 125:2451–2456

    PubMed  CAS  Google Scholar 

  • Kent J, Wheatley SC, Andrews JE, Sinclair AH, Koopman P (1996) A male-specific role for SOX9 in vertebrate sex determination. Development 122:2813–2822

    PubMed  CAS  Google Scholar 

  • Kerins JA, Hanazawa M, Dorsett M, Schedl T (2010) PRP-17 and the pre-mRNA splicing pathway are preferentially required for the proliferation versus meiotic development decision and germline sex determination in Caenorhabditis elegans. Dev Dyn 239:1555–1572

    PubMed  CAS  Google Scholar 

  • Kershner AM, Kimble J (2010) Genome-wide analysis of mRNA targets for Caenorhabditis elegans FBF, a conserved stem cell regulator. Proc Natl Acad Sci USA 107:3936–3941

    PubMed  CAS  Google Scholar 

  • Kim KW, Nykamp K, Suh N, Bachorik JL, Wang L, Kimble J (2009) Antagonism between GLD-2 binding partners controls gamete sex. Dev Cell 16:723–733

    PubMed  CAS  Google Scholar 

  • Kim KW, Wilson TL, Kimble J (2010) GLD-2/RNP-8 cytoplasmic poly(A) polymerase is a broad-spectrum regulator of the oogenesis program. Proc Natl Acad Sci USA 107:17445–17450

    PubMed  CAS  Google Scholar 

  • Kimble J, Crittenden SL (2007) Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu Rev Cell Dev Biol 23:405–433

    PubMed  CAS  Google Scholar 

  • Kimble J, Edgar L, Hirsh D (1984) Specification of male development in Caenorhabditis elegans: the fem genes. Dev Biol 105:234–239

    PubMed  CAS  Google Scholar 

  • Koebernick K, Pieler T (2002) Gli-type zinc finger proteins as bipotential transducers of Hedgehog signaling. Differentiation 70:69–76

    PubMed  CAS  Google Scholar 

  • Konishi T, Uodome N, Sugimoto A (2008) The Caenorhabditis elegans DDX-23, a homolog of yeast splicing factor PRP28, is required for the sperm-oocyte switch and differentiation of various cell types. Dev Dyn 237:2367–2377

    PubMed  CAS  Google Scholar 

  • Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovellbadge R (1991) Male development of chromosomally female mice transgenic for Sry. Nature 351:117–121

    PubMed  CAS  Google Scholar 

  • Kraemer B, Crittenden S, Gallegos M, Moulder G, Barstead R, Kimble J, Wickens M (1999) NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans. Curr Biol 9:1009–1018

    PubMed  CAS  Google Scholar 

  • Kuwabara PE (1996) A novel regulatory mutation in the C. elegans sex determination gene tra-2 defines a candidate ligand/receptor interaction site. Development 122:2089–2098

    PubMed  CAS  Google Scholar 

  • Lamont LB, Kimble J (2007) Developmental expression of FOG-1/CPEB protein and its control in the Caenorhabditis elegans hermaphrodite germ line. Dev Dyn 236:871–879

    PubMed  CAS  Google Scholar 

  • Lee MH, Schedl T (2001) Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development. Genes Dev 15:2408–2420

    PubMed  CAS  Google Scholar 

  • Lee MH, Schedl T (2004) Translation repression by GLD-1 protects its mRNA targets from nonsense-mediated mRNA decay in C. elegans. Genes Dev 18:1047–1059

    PubMed  CAS  Google Scholar 

  • Lee MH, Schedl T (2006) RNA-binding proteins. WormBook: 1–13

    Google Scholar 

  • Lee MH, Ohmachi M, Arur S, Nayak S, Francis R, Church D, Lambie E, Schedl T (2007) Multiple functions and dynamic activation of MPK-1 extracellular signal-regulated kinase signaling in Caenorhabditis elegans germline development. Genetics 177:2039–2062

    PubMed  CAS  Google Scholar 

  • Lieb JD, de Solorzano CO, Rodriguez EG, Jones A, Angelo M, Lockett S, Meyer BJ (2000) The Caenorhabditis elegans dosage compensation machinery is recruited to X chromosome DNA attached to an autosome. Genetics 156:1603–1621

    PubMed  CAS  Google Scholar 

  • Luitjens C, Gallegos M, Kraemer B, Kimble J, Wickens M (2000) CPEB proteins control two key steps in spermatogenesis in C. elegans. Genes Dev 14:2596–2609

    PubMed  CAS  Google Scholar 

  • Lum DH, Kuwabara PE, Zarkower D, Spence AM (2000) Direct protein-protein interaction between the intracellular domain of TRA-2 and the transcription factor TRA-1A modulates feminizing activity in C. elegans. Genes Dev 14:3153–3165

    PubMed  CAS  Google Scholar 

  • Madl JE, Herman RK (1979) Polyploids and sex determination in Caenorhabditis elegans. Genetics 93:393–402

    PubMed  CAS  Google Scholar 

  • Maine EM, Hansen D, Springer D, Vought VE (2004) Caenorhabditis elegans atx-2 promotes germline proliferation and the oocyte fate. Genetics 168:817–830

    PubMed  CAS  Google Scholar 

  • Mantina P, MacDonald L, Kulaga A, Zhao L, Hansen D (2009) A mutation in teg-4 which encodes a protein homologous to the SAP130 pre-mRNA splicing factor, disrupts the balance between proliferation and differentiation in the C. elegans germ line. Mech Dev 126:417–429

    PubMed  CAS  Google Scholar 

  • Marin VA, Evans TC (2003) Translational repression of a C. elegans Notch mRNA by the STAR/KH domain protein GLD-1. Development 130:2623–2632

    PubMed  CAS  Google Scholar 

  • Mason DA, Rabinowitz JS, Portman DS (2008) dmd-3 a doublesex-related gene regulated by tra-1, governs sex-specific morphogenesis in C. elegans. Development 135:2373–2382

    PubMed  CAS  Google Scholar 

  • Mattaj IW, Habets WJ, van Venrooij WJ (1986) Monospecific antibodies reveal details of U2 snRNP structure and interaction between U1 and U2 snRNPs. EMBO J 5:997–1002

    PubMed  CAS  Google Scholar 

  • McLaren A (1984) Meiosis and differentiation of mouse germ cells. Symp Soc Exp Biol 38:7–23

    PubMed  CAS  Google Scholar 

  • Mendez R, Richter JD (2001) Translational control by CPEB: a means to the end. Nat Rev Mol Cell Biol 2:521–529

    PubMed  CAS  Google Scholar 

  • Merritt C, Rasoloson D, Ko D, Seydoux G (2008) 3’UTRs are the primary regulators of gene expression in the C. elegans germline. Curr Biol 18:1476–1482

    PubMed  CAS  Google Scholar 

  • Meyer BJ (2005) X-Chromosome dosage compensation. WormBook: 1–14

    Google Scholar 

  • Meyer BJ, Casson LP (1986) Caenorhabditis elegans compensates for the difference in X chromosome dosage between the sexes by regulating transcript levels. Cell 47:871–881

    PubMed  CAS  Google Scholar 

  • Miller LM, Plenefisch JD, Casson LP, Meyer BJ (1988) xol-1: a gene that controls the male modes of both sex determination and X chromosome dosage compensation in C. elegans. Cell 55:167–183

    PubMed  CAS  Google Scholar 

  • Morgan DE, Crittenden SL, Kimble J (2010) The C. elegans adult male germline: stem cells and sexual dimorphism. Dev Biol 346:204–214

    PubMed  CAS  Google Scholar 

  • Murata Y, Wharton RP (1995) Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80:747–756

    PubMed  CAS  Google Scholar 

  • Nagengast AA, Salz HK (2001) The Drosophila U2 snRNP protein U2A’ has an essential function that is SNF/U2B” independent. Nucleic Acids Res 29:3841–3847

    PubMed  CAS  Google Scholar 

  • Nigon V (1952) Experimental modifications of the sex ratio in a pseudogamous nematode. C R Hebd Seances Acad Sci 234:2568–2570

    PubMed  CAS  Google Scholar 

  • Nousch M, Eckmann CR (2012) Translational control in the C. elegans germ line. Advances in Experimental Medicine and Biology 757:205–247. (Chap. 8, this volume) Springer, New York

    Google Scholar 

  • Nusbaum C, Meyer BJ (1989) The Caenorhabditis elegans gene sdc-2 controls sex determination and dosage compensation in XX animals. Genetics 122:579–593

    PubMed  CAS  Google Scholar 

  • Nykamp K, Lee MH, Kimble J (2008) C. elegans La-related protein, LARP-1, localizes to germline P bodies and attenuates Ras-MAPK signaling during oogenesis. RNA 14:1378–1389

    PubMed  CAS  Google Scholar 

  • Ogura K, Kishimoto N, Mitani S, Gengyo-Ando K, Kohara Y (2003) Translational control of maternal glp-1 mRNA by POS-1 and its interacting protein SPN-4 in Caenorhabditis elegans. Development 130:2495–2503

    PubMed  CAS  Google Scholar 

  • Oliver B, Perrimon N, Mahowald AP (1988) Genetic-evidence that the Sans-Fille locus is involved in Drosophila sex determination. Genetics 120:159–171

    PubMed  CAS  Google Scholar 

  • Ostrer H (2000) Sexual differentiation. Semin Reprod Med 18:41–49

    PubMed  CAS  Google Scholar 

  • Otori M, Karashima T, Yamamoto M (2006) The Caenorhabditis elegans homologue of deleted in azoospermia is involved in the sperm/oocyte switch. Mol Biol Cell 17:3147–3155

    PubMed  CAS  Google Scholar 

  • Perry MD, Li W, Trent C, Robertson B, Fire A, Hageman JM, Wood WB (1993) Molecular characterization of the her-1 gene suggests a direct role in cell signaling during Caenorhabditis elegans sex determination. Genes Dev 7:216–228

    PubMed  CAS  Google Scholar 

  • Perry MD, Trent C, Robertson B, Chamblin C, Wood WB (1994) Sequenced alleles of the Caenorhabditis elegans sex-determining gene her-1 include a novel class of conditional promoter mutations. Genetics 138:317–327

    PubMed  CAS  Google Scholar 

  • Powell JR, Jow MM, Meyer BJ (2005) The T-box transcription factor SEA-1 is an autosomal element of the X:A signal that determines C. elegans sex. Dev Cell 9:339–349

    PubMed  CAS  Google Scholar 

  • Puoti A, Kimble J (1999) The Caenorhabditis elegans sex determination gene mog-1 encodes a member of the DEAH-box protein family. Mol Cell Biol 19:2189–2197

    PubMed  CAS  Google Scholar 

  • Puoti A, Kimble J (2000) The hermaphrodite sperm/oocyte switch requires the Caenorhabditis elegans homologs of PRP2 and PRP22. Proc Natl Acad Sci USA 97:3276–327681

    PubMed  CAS  Google Scholar 

  • Puoti A, Pugnale P, Belfiore M, Schlappi AC, Saudan Z (2001) RNA and sex determination in Caenorhabditis elegans. Post-transcriptional regulation of the sex-determining tra-2 and fem-3 mRNAs in the Caenorhabditis elegans hermaphrodite. EMBO Rep 2:899–904

    PubMed  CAS  Google Scholar 

  • Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, Hodgkin J, Zarkower D (1998) Evidence for evolutionary conservation of sex-determining genes. Nature 391:691–695

    PubMed  CAS  Google Scholar 

  • Rhind NR, Miller LM, Kopczynski JB, Meyer BJ (1995) xol-1 acts as an early switch in the C. elegans male/hermaphrodite decision. Cell 80:71–82

    PubMed  CAS  Google Scholar 

  • Rosenquist TA, Kimble J (1988) Molecular cloning and transcript analysis of fem-3, a sex-determination gene in Caenorhabditis elegans. Genes Dev 2:606–616

    PubMed  CAS  Google Scholar 

  • Rybarska A, Harterink M, Jedamzik B, Kupinski AP, Schmid M, Eckmann CR (2009) GLS-1, a novel P granule component, modulates a network of conserved RNA regulators to influence germ cell fate decisions. PLoS Genet 5:e1000494

    PubMed  Google Scholar 

  • Ryder SP, Frater LA, Abramovitz DL, Goodwin EB, Williamson JR (2004) RNA target specificity of the STAR/GSG domain post-transcriptional regulatory protein GLD-1. Nat Struct Mol Biol 11:20–28

    PubMed  CAS  Google Scholar 

  • Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, Hall JC, Taylor BJ, Wasserman SA (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87:1079–1089

    PubMed  CAS  Google Scholar 

  • Salz HK, Erickson JW (2010) Sex determination in Drosophila: the view from the top. Fly 4:60–70

    PubMed  CAS  Google Scholar 

  • Schedl T (1997) Developmental genetics of the germ line. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR (eds) C. elegans Il. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Schedl T, Kimble J (1988) fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 119:43–61

    PubMed  CAS  Google Scholar 

  • Schedl T, Graham PL, Barton MK, Kimble J (1989) Analysis of the role of tra-1 in germline sex determination in the nematode Caenorhabditis elegans. Genetics 123:755–769

    PubMed  CAS  Google Scholar 

  • Scherly D, Boelens W, Dathan NA, van Venrooij WJ, Mattaj IW (1990) Major determinants of the specificity of interaction between small nuclear ribonucleoproteins U1A and U2B’’ and their cognate RNAs. Nature 345:502–506

    PubMed  CAS  Google Scholar 

  • Schvarzstein M, Spence AM (2006) The C. elegans sex-determining GLI protein TRA-1A is regulated by sex-specific proteolysis. Dev Cell 11:733–740

    PubMed  CAS  Google Scholar 

  • Shimada M, Kanematsu K, Tanaka K, Yokosawa H, Kawahara H (2006) Proteasomal ubiquitin receptor RPN-10 controls sex determination in Caenorhabditis elegans. Mol Biol Cell 17:5356–5371

    PubMed  CAS  Google Scholar 

  • Sillekens PT, Beijer RP, Habets WJ, van Verooij WJ (1989) Molecular cloning of the cDNA for the human U2 snRNA-specific A’ protein. Nucleic Acids Res 17:1893–1906

    PubMed  CAS  Google Scholar 

  • Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf AM, Lovell-Badge R, Goodfellow PN (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346:240–244

    PubMed  CAS  Google Scholar 

  • Skipper M, Milne CA, Hodgkin J (1999) Genetic and molecular analysis of fox-1, a numerator element involved in Caenorhabditis elegans primary sex determination. Genetics 151:617–631

    PubMed  CAS  Google Scholar 

  • Slanchev K, Stebler J, de la Cueva-Mendez G, Raz E (2005) Development without germ cells: the role of the germ line in zebrafish sex differentiation. Proc Natl Acad Sci USA 102:4074–4079

    PubMed  CAS  Google Scholar 

  • Sokol SB, Kuwabara PE (2000) Proteolysis in Caenorhabditis elegans sex determination: cleavage of TRA-2A by TRA-3. Genes Dev 14:901–906

    PubMed  CAS  Google Scholar 

  • Sonoda J, Wharton RP (1999) Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev 13:2704–2712

    PubMed  CAS  Google Scholar 

  • Starostina NG, Lim JM, Schvarzstein M, Wells L, Spence AM, Kipreos ET (2007) A CUL-2 ubiquitin ligase containing three FEM proteins degrades TRA-1 to regulate C. elegans sex determination. Dev Cell 13:127–139

    PubMed  CAS  Google Scholar 

  • Steinmann-Zwicky M (1988) Sex determination in Drosophila - the X-chromosomal gene Liz is required for Sxl activity. EMBO J 7:3889–3898

    PubMed  CAS  Google Scholar 

  • Suh N, Crittenden SL, Goldstrohm A, Hook B, Thompson B, Wickens M, Kimble J (2009) FBF and its dual control of gld-1 expression in the Caenorhabditis elegans germline. Genetics 181:1249–1260

    PubMed  CAS  Google Scholar 

  • Tabara H, Sarkissian M, Kelly WG, Fleenor J, Grishok A, Timmons L, Fire A, Mello CC (1999) The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99:123–132

    PubMed  CAS  Google Scholar 

  • Tamashiro DA, Alarcon VB, Marikawa Y (2008) Ectopic expression of mouse Sry interferes with Wnt/beta-catenin signaling in mouse embryonal carcinoma cell lines. Biochim Biophys Acta 1780:1395–1402

    PubMed  CAS  Google Scholar 

  • Thompson BE, Bernstein DS, Bachorik JL, Petcherski AG, Wickens M, Kimble J (2005) Dose-dependent control of proliferation and sperm specification by FOG-1/CPEB. Development 132:3471–3481

    PubMed  CAS  Google Scholar 

  • Trent C, Purnell B, Gavinski S, Hageman J, Chamblin C, Wood WB (1991) Sex-specific transcriptional regulation of the C. elegans sex-determining gene her-1. Mech Dev 34:43–55

    PubMed  CAS  Google Scholar 

  • Unhavaithaya Y, Shin TH, Miliaras N, Lee J, Oyama T, Mello CC (2002) MEP-1 and a homolog of the NURD complex component Mi-2 act together to maintain germline-soma distinctions in C. elegans. Cell 111:991–1002

    PubMed  CAS  Google Scholar 

  • Vaiman D, Pailhoux E (2000) Mammalian sex reversal and intersexuality: deciphering the sex-determination cascade. Trends Genet 16:488–494

    PubMed  CAS  Google Scholar 

  • Villeneuve AM, Meyer BJ (1987) sdc-1: a link between sex determination and dosage compensation in C. elegans. Cell 48:25–37

    PubMed  CAS  Google Scholar 

  • Wang S, Kimble J (2001) The TRA-1 transcription factor binds TRA-2 to regulate sexual fates in Caenorhabditis elegans. EMBO J 20:1363–1372

    PubMed  CAS  Google Scholar 

  • Wang L, Eckmann CR, Kadyk LC, Wickens M, Kimble J (2002) A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans. Nature 419:312–316

    PubMed  CAS  Google Scholar 

  • Ward S, Roberts TM, Strome S, Pavalko FM, Hogan E (1986) Monoclonal antibodies that recognize a polypeptide antigenic determinant shared by multiple Caenorhabditis elegans sperm-specific proteins. J Cell Biol 102:1778–1786

    PubMed  CAS  Google Scholar 

  • Wawersik M, Milutinovich A, Casper AL, Matunis E, Williams B, Van Doren M (2005) Somatic control of germline sexual development is mediated by the JAK/STAT pathway. Nature 436:563–567

    PubMed  CAS  Google Scholar 

  • Wharton RP, Sonoda J, Lee T, Patterson M, Murata Y (1998) The Pumilio RNA-binding domain is also a translational regulator. Mol Cell 1:863–872

    PubMed  CAS  Google Scholar 

  • Wolff JR, Zarkower D (2008) Somatic sexual differentiation in Caenorhabditis elegans. Curr Top Dev Biol 83:1–39

    PubMed  CAS  Google Scholar 

  • Wreden C, Verrotti AC, Schisa JA, Lieberfarb ME, Strickland S (1997) Nanos and pumilio establish embryonic polarity in Drosophila by promoting posterior deadenylation of hunchback mRNA. Development 124:3015–3023

    PubMed  CAS  Google Scholar 

  • Yonker SA, Meyer BJ (2003) Recruitment of C. elegans dosage compensation proteins for gene-specific versus chromosome-wide repression. Development 130:6519–6532

    PubMed  CAS  Google Scholar 

  • Zamore PD, Williamson JR, Lehmann R (1997) The Pumilio protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins. RNA 3:1421–1433

    PubMed  CAS  Google Scholar 

  • Zanetti S, Meola M, Bochud A, Puoti A (2011) Role of the C. elegans U2 snRNP protein MOG-2 in sex determination, meiosis, and splice site selection. Dev Biol 354:232–241

    PubMed  CAS  Google Scholar 

  • Zanetti S, Grinschgl S, Meola M, Belfiore M, Rey S, Bianchi P, Puoti A (2012) The sperm-oocyte switch in the C. elegans hermaphrodite is controlled through abundance of the fem-3 mRNA. RNA 18:1385–1394

    Google Scholar 

  • Zanin E, Pacquelet A, Scheckel C, Ciosk R, Gotta M (2010) LARP-1 promotes oogenesis by repressing fem-3 in the C. elegans germline. J Cell Sci 123:2717–2724

    PubMed  CAS  Google Scholar 

  • Zarkower D (2006) Somatic sex determination. WormBook: 1–12

    Google Scholar 

  • Zarkower D, Hodgkin J (1992) Molecular analysis of the C. elegans sex-determining gene tra-1: a gene encoding two zinc finger proteins. Cell 70:237–249

    PubMed  CAS  Google Scholar 

  • Zhang B, Gallegos M, Puoti A, Durkin E, Fields S, Kimble J, Wickens MP (1997) A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 390:477–484

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Tim Schedl and Nivedita Awasthi for comments on the manuscript. This work was partially supported by the Novartis Foundation for Medical and Biological Research, grant 10B34.

Author information

Authors and Affiliations

  1. Department of Biology, University of Fribourg, Chemin du Musée 10, 1700, Fribourg, Switzerland

    Simone Zanetti & Alessandro Puoti

Authors
  1. Simone Zanetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alessandro Puoti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alessandro Puoti .

Editor information

Editors and Affiliations

  1. , Department of Genetics, Washington University School of Medicine, 4566 Scott Avenue, St. Louis, 63130, Missouri, USA

    Tim Schedl

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Zanetti, S., Puoti, A. (2013). Sex Determination in the Caenorhabditis elegans Germline. In: Schedl, T. (eds) Germ Cell Development in C. elegans. Advances in Experimental Medicine and Biology, vol 757. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4015-4_3

Download citation

Publish with us

Policies and ethics

Search

Navigation