Skip to main content
SpringerLink
Log in

Using Caenorhabditis to Explore the Evolution of the Germ Line

  • Chapter
  • First Online:
Book cover Germ Cell Development in C. elegans

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

Abstract

Germ cells share core attributes and homologous molecular components across animal phyla. Nevertheless, abrupt shifts in reproductive mode often occur that are mediated by the rapid evolution of germ cell properties. Studies of Caenorhabditis nematodes show how the otherwise conserved RNA-binding proteins (RBPs) that regulate germline development and differentiation can undergo surprisingly rapid functional evolution. This occurs even as the narrow biochemical tasks performed by the RBPs remain constant. The biological roles of germline RBPs are thus highly context-dependent, and the inference of archetypal roles from isolated models in different phyla may therefore be premature.

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

Access this chapter

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

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 349(6307):346–348

    PubMed  CAS  Google Scholar 

  • Ariz M, Mainpal R, Subramaniam K (2009) C. elegans RNA-binding proteins PUF-8 and MEX-3 function redundantly to promote germline stem cell mitosis. Dev Biol 326(2):295–304

    PubMed  CAS  Google Scholar 

  • Austin J, Kimble J (1989) Transcript analysis of glp-1 and lin-12, homologous genes required for cell interactions during development of C. elegans. Cell 58(3):565–571. doi:0092-8674(89)90437-6[pii]

    PubMed  CAS  Google Scholar 

  • Baldi C, Cho S, Ellis RE (2009) Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. Science 326(5955):1002–1005. doi:326/5955/1002[pii]10.1126/science.1176013

    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(1):107–119

    PubMed  CAS  Google Scholar 

  • Beadell AV, Liu Q, Johnson DM, Haag ES (2011) Independent recruitments of a translational regulator in the evolution of self-fertile nematodes. Proc Natl Acad Sci USA 108:19672–19677. doi:10.1073/pnas.1108068108

    PubMed  CAS  Google Scholar 

  • Beer J, Technau GM, Campos-Ortega JA (1987) Lineage analysis of transplanted individual cells in embryos of Drosophila melanogaster. Dev Genes Evol 196(4):222–230. doi:10.1007/bf00376346

    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 

  • Boterenbrood EC, Nieuwkoop PD (1973) The formation of the mesoderm in urodelean amphibians. Dev Genes Evol 173(4):319–332. doi:10.1007/bf00575837

    Google Scholar 

  • Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, Hoege C, Gharakhani J, Julicher F, Hyman AA (2009) Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324(5935):1729–1732

    PubMed  CAS  Google Scholar 

  • Brawley C, Matunis E (2004) Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 304(5675):1331–1334. doi:10.1126/science.1097676

    PubMed  CAS  Google Scholar 

  • Carroll SB (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134(1):25–36

    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(14):3119–3129

    PubMed  CAS  Google Scholar 

  • Chen PJ, Cho S et al (2001) Specification of germ cell fates by FOG-3 has been conserved during nematode evolution. Genetics 158(4):1513–1525

    PubMed  CAS  Google Scholar 

  • Cho S, Jin SW, Cohen A, Ellis RE (2004) A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res 14(7):1207–1220

    PubMed  CAS  Google Scholar 

  • Cinquin O, Crittenden SL, Morgan DE, Kimble J (2010) Progression from a stem cell-like state to early differentiation in the C. elegans germ line. Proc Natl Acad Sci USA 107(5):2048–2053. doi:0912704107[pii]10.1073/pnas.0912704107

    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(24):5265–5276

    PubMed  CAS  Google Scholar 

  • Coward SJ (1974) Chromatoid bodies in somatic cells of the planarian: observations on their behavior during mitosis. Anat Rec 180(3):533–545. doi:10.1002/ar.1091800312

    PubMed  CAS  Google Scholar 

  • Cox DN, Chao A, Baker J, Chang L, Qiao D, Lin H (1998) A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev 12(23):3715–3727

    PubMed  CAS  Google Scholar 

  • Crittenden SL, Troemel ER, Evans TC, Kimble J (1994) GLP-1 is localized to the mitotic region of the C. elegans germ line. Development 120(10):2901–2911

    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(6889):660–663. doi:10.1038/nature754

    PubMed  CAS  Google Scholar 

  • Crittenden SL, Leonhard KA, Byrd DT, Kimble J (2006) Cellular analyses of the mitotic region in the Caenorhabditis elegans adult germ line. Mol Biol Cell 17(7):3051–3061. doi:E06-03-0170[pii]10.1091/mbc.E06-03-0170

    PubMed  CAS  Google Scholar 

  • Cutter AD, Felix MA, Barriere A, Charlesworth D (2006) Patterns of nucleotide polymorphism distinguish temperate and tropical wild isolates of Caenorhabditis briggsae. Genetics 173(4):2021–2031

    PubMed  CAS  Google Scholar 

  • de Bono M, Hodgkin J (1996) Evolution of sex determination in Caenorhabditis: unusually high divergence of tra-1 and its functional consequences. Genetics 144:587–595

    PubMed  Google Scholar 

  • de Rooij DG (2009) The spermatogonial stem cell niche. Microsc Res Tech 72(8):580–585. doi:10.1002/jemt.20699

    PubMed  Google Scholar 

  • Dolgin ES, Felix MA, Cutter AD (2008) Hakuna Nematoda: genetic and phenotypic diversity in African isolates of Caenorhabditis elegans and C. briggsae. Heredity 100(3):304–315

    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 

  • Extavour CG (2007) Evolution of the bilaterian germ line: lineage origin and modulation of specification mechanisms. Integr Comp Biol 47(5):770–785

    PubMed  Google Scholar 

  • Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130(24):5869–5884

    PubMed  CAS  Google Scholar 

  • Francis R, Maine E, Schedl T (1995) 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(2):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(21):6337–6347

    PubMed  CAS  Google Scholar 

  • Gallo CM, Wang JT, Motegi F, Seydoux G (2010) Cytoplasmic partitioning of P granule components is not required to specify the germline in C. elegans. Science 330(6011):1685–1689

    PubMed  CAS  Google Scholar 

  • Gonczy P, DiNardo S (1996) The germ line regulates somatic cyst cell proliferation and fate during Drosophila spermatogenesis. Development 122(8):2437–2447

    PubMed  CAS  Google Scholar 

  • Goodenough U, Lin H, Lee JH (2007) Sex determination in Chlamydomonas. Semin Cell Dev Biol 18(3):350–361

    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(2):329–339

    PubMed  CAS  Google Scholar 

  • Goriely A, McVean GA et al (2005) Gain-of-function amino acid substitutions drive positive selection of FGFR2 mutations in human spermatogonia. Proc Natl Acad Sci USA 102(17):6051–6056

    PubMed  CAS  Google Scholar 

  • Graustein A, Gaspar JM, Walters JR, Palopoli MF (2002) Levels of DNA polymorphism vary with mating system in the nematode genus Caenorhabditis. Genetics 161(1):99–107

    PubMed  CAS  Google Scholar 

  • Guo T, Peters AH, Newmark PA (2006) A Bruno-like gene is required for stem cell maintenance in planarians. Dev Cell 11(2):159–169. doi:S1534-5807(06)00260-7[pii]10.1016/j.devcel.2006.06.004

    PubMed  CAS  Google Scholar 

  • Guo Y, Lang S, Ellis RE (2009) Independent recruitment of F box genes to regulate hermaphrodite development during nematode evolution. Curr Biol 19(21):1853–1860

    PubMed  CAS  Google Scholar 

  • Haag ES (2007) Why two sexes? Sex determination in multicellular organisms and protistan mating types. Semin Cell Dev Biol 18(3):348–349

    PubMed  Google Scholar 

  • Haag ES, Kimble J (2000) Regulatory elements required for development of Caenorhabditis elegans hermaphrodites are conserved in the tra-2 homologue of C. remanei, a male/female sister species. Genetics 155(1):105–116

    PubMed  CAS  Google Scholar 

  • Haag ES, Wang S, Kimble J (2002) Rapid coevolution of the nematode sex-determining genes fem-3 and tra-2. Curr Biol 12(23):2035–2041

    PubMed  CAS  Google Scholar 

  • Handberg-Thorsager M, Salo E (2007) The planarian nanos-like gene Smednos is expressed in germline and eye precursor cells during development and regeneration. Dev Genes Evol 217(5):403–411. doi:10.1007/s00427-007-0146-3

    PubMed  CAS  Google Scholar 

  • Hansen D, Pilgrim D (1998) Molecular evolution of a sex determination protein. FEM-2 (pp 2c) in Caenorhabditis. Genetics 149:1353–1362

    PubMed  CAS  Google Scholar 

  • Hansen D, Wilson-Berry L, Dang T, Schedl T (2004) 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 

  • Hanyu-Nakamura K, Sonobe-Nojima H, Tanigawa A, Lasko P, Nakamura A (2008) Drosophila Pgc protein inhibits P-TEFb recruitment to chromatin in primordial germ cells. Nature 451(7179):730–733. doi:nature06498[pii]10.1038/nature06498

    PubMed  CAS  Google Scholar 

  • Hashimoto Y, Maegawa S, Nagai T, Yamaha E, Suzuki H, Yasuda K, Inoue K (2004) Localized maternal factors are required for zebrafish germ cell formation. Dev Biol 268(1):152–161. doi:10.1016/j.ydbio.2003.12.013 S0012160603007942[pii]

    PubMed  CAS  Google Scholar 

  • Heasman J, Quarmby J, Wylie CC (1984) The mitochondrial cloud of Xenopus oocytes: the source of germinal granule material. Dev Biol 105(2):458–469. doi:0012-1606(84)90303-8[pii]

    PubMed  CAS  Google Scholar 

  • Heffer A, Shultz JW, Pick L (2010) Surprising flexibility in a conserved Hox transcription factor over 550 million years of evolution. Proc Natl Acad Sci USA 107(42):18040–18045

    PubMed  CAS  Google Scholar 

  • Henderson ST, Gao D, Lambie EJ, Kimble J (1994) lag-2 may encode a signaling ligand for the GLP-1 and LIN-12 receptors of C. elegans. Development 120(10):2913–2924

    PubMed  CAS  Google Scholar 

  • Hill RC, Haag ES (2009) A sensitized genetic background reveals evolution near the terminus of the Caenorhabditis germline sex determination pathway. Evol Dev 4:333–341

    Google Scholar 

  • Hill RC, de Carvalho CE, Salogiannis J, Schlager B, Pilgrim D, Haag ES (2006) Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes. Dev Cell 10(4):531–538

    PubMed  CAS  Google Scholar 

  • Hillier LW, Miller RD, Baird SE, Chinwalla A, Fulton LA, Koboldt DC, Waterston RH (2007) Comparison of C. elegans and C. briggsae genome sequences reveals extensive conservation of chromosome organization and synteny. PLoS Biol 5(7):e167

    PubMed  Google Scholar 

  • Hird SN, Paulsen JE, Strome S (1996) Segregation of germ granules in living Caenorhabditis elegans embryos: cell-type-specific mechanisms for cytoplasmic localisation. Development 122(4):1303–1312

    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(1):15–52

    PubMed  CAS  Google Scholar 

  • Hori I, Kishida Y (2003) Quantitative changes in nuclear pores and chromatoid bodies induced by neuropeptides during cell differentiation in the planarian Dugesia japonica. J Submicrosc Cytol Pathol 35(4):439–444

    PubMed  CAS  Google Scholar 

  • Huettner AF (1923) The origin of the germ cells in Drosophila melanogaster. J Morphol 37(2):385–423. doi:10.1002/jmor.1050370204

    Google Scholar 

  • Humphrey RR (1925) The primordial germ cells of Hemidactylium and other amphibia. J Morphol 41(1):1–43. doi:10.1002/jmor.1050410103

    Google Scholar 

  • Humphrey RR (1927) Extirpation of the primordial germ cells of Amblystoma: its effect upon the development of the gonad. J Exp Zool 49(2):363–399. doi:10.1002/jez.1400490207

    Google Scholar 

  • Ikenishi K, Nieuwkoop PD (1978) Location and ultrastructure of primordial germ cells (PGCs) in Ambystoma mexicanum. Dev Growth Differ 20(1):1–9. doi:10.1111/j.1440-169X.1978.00001.x

    Google Scholar 

  • Illmensee K, Mahowald AP (1974) Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proc Natl Acad Sci USA 71(4):1016–1020

    PubMed  CAS  Google Scholar 

  • Jan E, Yoon JW, Walterhouse D, Iannaccone P, Goodwin EB (1997) Conservation of the C. elegans tra-2 3’UTR translational control. EMBO J 16(20):6301–6313

    PubMed  CAS  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(1):258–269. doi:10.1093/emboj/18.1.258

    PubMed  CAS  Google Scholar 

  • Johnson AD, Bachvarova RF, Drum M, Masi T (2001) Expression of axolotl DAZL RNA, a marker of germ plasm: widespread maternal RNA and onset of expression in germ cells approaching the gonad. Dev Biol 234(2):402–415. doi:10.1006/dbio.2001.0264 S0012-1606(01)90264-7[pii]

    PubMed  CAS  Google Scholar 

  • Johnson AD, Crother B, White ME, Patient R, Bachvarova RF, Drum M, Masi T (2003) Regulative germ cell specification in axolotl embryos: a primitive trait conserved in the mammalian lineage. Philos Trans R Soc Lond B Biol Sci 358(1436):1371–1379. doi:10.1098/rstb.2003.1331

    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(1):165–183. doi:S0012-1606(96)90293-6[pii]10.1006/dbio.1996.0293

    PubMed  CAS  Google Scholar 

  • Kawase E, Wong MD, Ding BC, Xie T (2004) Gbb/Bmp signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development 131(6):1365–1375. doi:10.1242/dev.01025 dev.01025[pii]

    PubMed  CAS  Google Scholar 

  • Kelleher DF, de Carvalho CE, Doty AV, Layton M, Cheng AT, Mathies LD, Pilgrim D, Haag ES (2008) Comparative genetics of sex determination: masculinizing mutations in Caenorhabditis briggsae. Genetics 178(3):1415–1429

    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(8):3936–3941. doi:1000495107[pii]10.1073/pnas.1000495107

    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. doi:10.1146/annurev.cellbio.23.090506.123326

    PubMed  CAS  Google Scholar 

  • Kimble J, Simpson P (1997) The LIN-12/Notch signaling pathway and its regulation. Annu Rev Cell Dev Biol 13:333–361. doi:10.1146/annurev.cellbio.13.1.333

    PubMed  CAS  Google Scholar 

  • Kimble JE, White JG (1981) On the control of germ cell development in Caenorhabditis elegans. Dev Biol 81(2):208–219. doi:0012-1606(81)90284-0[pii]

    PubMed  CAS  Google Scholar 

  • King FJ, Lin H (1999) Somatic signaling mediated by fs(1)Yb is essential for germline stem cell maintenance during Drosophila oogenesis. Development 126(9):1833–1844

    PubMed  CAS  Google Scholar 

  • Kiontke K, Sudhaus W (2006) Ecology of Caenorhabditis species. WormBook:1–14. doi:10.1895/wormbook.1.37.1

    Google Scholar 

  • Kiontke K, Gavin NP, Raynes Y, Roehrig C, Piano F, Fitch DHA (2004) Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci USA 101(24):9003–9008

    PubMed  CAS  Google Scholar 

  • Kiontke K, Félix M-A, Ailion M, Rockman M, Braendle C, Penigault J-B, Fitch DHA (2011) A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits. BMC Evol Biol 11:339. doi:10.1186/1471-2148-11-339

    PubMed  CAS  Google Scholar 

  • Kirilly D, Xie T (2007) The Drosophila ovary: an active stem cell community. Cell Res 17(1):15–25. doi:7310123[pii]10.1038/sj.cr.7310123

    PubMed  CAS  Google Scholar 

  • Koboldt DC, Staisch J, Thillainathan B, Haines K, Baird SE, Chamberlin HM, Haag ES, Miller RD, Gupta BP (2010) A toolkit for rapid gene mapping in the nematode Caenorhabditis briggsae. BMC Genomics 11:236. doi:1471-2164-11-236[pii]10.1186/1471-2164-11-236

    PubMed  Google Scholar 

  • Komiya T, Itoh K, Ikenishi K, Furusawa M (1994) Isolation and characterization of a novel gene of the DEAD box protein family which is specifically expressed in germ cells of Xenopus laevis. Dev Biol 162(2):354–363. doi:10.1006/dbio.1994.1093 S0012-1606(84)71093-1[pii]

    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(18):1009–1018

    PubMed  CAS  Google Scholar 

  • Kurimoto K, Yabuta Y, Ohinata Y, Shigeta M, Yamanaka K, Saitou M (2008) Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice. Genes Dev 22(12):1617–1635. doi:22/12/1617[pii]10.1101/gad.1649908

    PubMed  CAS  Google Scholar 

  • Kuwabara PE (1996) Interspecies comparison reveals evolution of control regions in the nematode sex-determining gene tra-2. Genetics 144(2):597–607

    PubMed  CAS  Google Scholar 

  • Lamont LB, Crittenden SL, Bernstein D, Wickens M, Kimble J (2004) FBF-1 and FBF-2 regulate the size of the mitotic region in the C. elegans germline. Dev Cell 7(5):697–707. doi:S1534580704003338[pii]10.1016/j.devcel.2004.09.013

    PubMed  CAS  Google Scholar 

  • Lawson KA, Dunn NR, Roelen BA, Zeinstra LM, Davis AM, Wright CV, Korving JP, Hogan BL (1999) Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 13(4):424–436

    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(18):2408–2420. doi:10.1101/gad.915901

    PubMed  CAS  Google Scholar 

  • Lee MH, Schedl T (2010) C. elegans star proteins, GLD-1 and ASD-2, regulate specific RNA targets to control development. Advances in Experimental Medicine and Biology 693:106–122

    PubMed  CAS  Google Scholar 

  • Lee SC, Ni M, Li W, Shertz C, Heitman J (2010) The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev 74(2):298–340. doi:74/2/298[pii]10.1128/MMBR.00005-10

    PubMed  CAS  Google Scholar 

  • Leonard J (2010) The evolution of sexes, anisogamy, and sexual systems: natural versus sexual selection. In: Leonard J, Cordoba-Aguilar A (eds) The evolution of primary sexual characters in animals. Oxford University Press, Oxford

    Google Scholar 

  • Lin H (2002) The stem-cell niche theory: lessons from flies. Nat Rev Genet 3(12):931–940. doi:10.1038/nrg952 nrg952[pii]

    PubMed  CAS  Google Scholar 

  • Liu Q, Stumpf C, Wickens M, Haag ES (2012) Context-dependent function of a conserved translational regulatory module. Development 139:ppTBA

    Google Scholar 

  • Lublin AL, Evans TC (2007) The RNA-binding proteins PUF-5, PUF-6, and PUF-7 reveal multiple systems for maternal mRNA regulation during C. elegans oogenesis. Dev Biol 303(2):635–649

    PubMed  CAS  Google Scholar 

  • Mann RS, Lelli KM, Joshi R (2009) Hox specificity unique roles for cofactors and collaborators. Curr Top Dev Biol 88:63–101

    PubMed  CAS  Google Scholar 

  • McCarter J, Bartlett B, Dang T, Schedl T (1997) Soma-germ cell interactions in Caenorhabditis elegans: multiple events of hermaphrodite germline development require the somatic sheath and spermathecal lineages. Dev Biol 181(2):121–143. doi:10.1006/dbio.1996.8429 S0012-1606(96)98429-8[pii]

    PubMed  CAS  Google Scholar 

  • McCourt RM, Delwiche CF, Karol KG (2004) Charophyte algae and land plant origins. Trends Ecol Evol 19(12):661–666

    PubMed  Google Scholar 

  • McGovern M, Voutev R, Maciejowski J, Corsi AK, Hubbard EJ (2009) A “latent niche” mechanism for tumor initiation. Proc Natl Acad Sci USA 106(28):11617–11622. doi:0903768106[pii]10.1073/pnas.0903768106

    PubMed  CAS  Google Scholar 

  • Mello CC, Draper BW, Krause M, Weintraub H, Priess JR (1992) The pie-1 and mex-1 genes and maternal control of blastomere identity in early C. elegans embryos. Cell 70(1):163–176. doi:0092-8674(92)90542-K[pii]

    PubMed  CAS  Google Scholar 

  • Mello CC, Schubert C, Draper B, Zhang W, Lobel R, Priess JR (1996) The PIE-1 protein and germline specification in C. elegans embryos. Nature 382(6593):710–712. doi:10.1038/382710a0

    PubMed  CAS  Google Scholar 

  • Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, Pichel JG, Westphal H, Saarma M, Sariola H (2000) Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287(5457):1489–1493. doi:8297[pii]

    PubMed  CAS  Google Scholar 

  • Merritt C, Seydoux G (2010) The Puf RNA-binding proteins FBF-1 and FBF-2 inhibit the expression of synaptonemal complex proteins in germline stem cells. Development 137(11):1787–1798. doi:dev.050799[pii]10.1242/dev.050799

    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(19):1476–1482

    PubMed  CAS  Google Scholar 

  • Morgan T (1901) Growth and regeneration in Planaria lugubris. Dev Genes Evol 13(1):179–212. doi:10.1007/bf02161982

    Google Scholar 

  • Morgan CT, Lee M-H et al (2010) Chemical reprogramming of Caenorhabditis elegans germ cell fate. Nat Chem Biol 6(2):102–104

    PubMed  CAS  Google Scholar 

  • Nayak S, Goree J, Schedl T (2005) fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis. PLoS Biol 3(1):e6

    PubMed  Google Scholar 

  • Newmark PA, Sanchez Alvarado A (2002) Not your father’s planarian: a classic model enters the era of functional genomics. Nat Rev Genet 3(3):210–219. doi:10.1038/nrg759 nrg759[pii]

    PubMed  CAS  Google Scholar 

  • Olsen LC, Aasland R, Fjose A (1997) A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech Dev 66(1–2):95–105

    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(7):3147–3155. doi:E05-11-1067[pii]10.1091/mbc.E05-11-1067

    PubMed  CAS  Google Scholar 

  • Pepper AS, Killian DJ, Hubbard EJ (2003a) Genetic analysis of Caenorhabditis elegans glp-1 mutants suggests receptor interaction or competition. Genetics 163(1):115–132

    PubMed  CAS  Google Scholar 

  • Pepper AS, Lo TW, Killian DJ, Hall DH, Hubbard EJ (2003b) The establishment of Caenorhabditis elegans germline pattern is controlled by overlapping proximal and distal somatic gonad signals. Dev Biol 259(2):336–350. doi:S0012160603002033[pii]

    PubMed  CAS  Google Scholar 

  • Praitis V, Casey E, Collar D, Austin J (2001) Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157(3):1217–1226

    PubMed  CAS  Google Scholar 

  • Ramesh MA, Malik SB, Logsdon JM Jr (2005) A phylogenomic inventory of meiotic genes; ­evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr Biol 15(2):185–191

    PubMed  CAS  Google Scholar 

  • Raz E (2003) Primordial germ-cell development: the zebrafish perspective. Nat Rev Genet 4(9):690–700. doi:10.1038/nrg1154

    PubMed  CAS  Google Scholar 

  • Reddien PW, Sanchez Alvarado A (2004) Fundamentals of planarian regeneration. Annu Rev Cell Dev Biol 20:725–757. doi:10.1146/annurev.cellbio.20.010403.095114

    PubMed  CAS  Google Scholar 

  • Ross JA, Koboldt DC, Staisch JE, Chamberlin HM, Gupta BP, Miller RD, Baird SE, Haag ES (2011) Caenorhabditis briggsae recombinant inbred line genotypes reveal inter-strain incompatibility and the evolution of recombination. PLoS Genet 7(7):e1002174

    PubMed  CAS  Google Scholar 

  • Salo E, Baguna J (1984) Regeneration and pattern formation in planarians. I. The pattern of mitosis in anterior and posterior regeneration in Dugesia (G) tigrina, and a new proposal for blastema formation. J Embryol Exp Morphol 83:63–80

    PubMed  CAS  Google Scholar 

  • Salvetti A, Rossi L, Lena A, Batistoni R, Deri P, Rainaldi G, Locci MT, Evangelista M, Gremigni V (2005) DjPum, a homologue of Drosophila Pumilio, is essential to planarian stem cell maintenance. Development 132(8):1863–1874. doi:dev.01785[pii]10.1242/dev.01785

    PubMed  CAS  Google Scholar 

  • Sanchez Alvarado A (2006) Planarian regeneration: its end is its beginning. Cell 124(2):241–245. doi:S0092-8674(06)00060-2[pii]10.1016/j.cell.2006.01.012

    PubMed  CAS  Google Scholar 

  • Sato K, Sugita T, Kobayashi K, Fujita K, Fujii T, Matsumoto Y, Mikami T, Nishizuka N, Nishizuka S, Shojima K, Suda M, Takahashi G, Himeno H, Muto A, Ishida S (2001) Localization of mitochondrial ribosomal RNA on the chromatoid bodies of marine planarian polyclad embryos. Dev Growth Differ 43(2):107–114. doi:dgd558[pii]

    PubMed  CAS  Google Scholar 

  • Sato K, Shibata N, Orii H, Amikura R, Sakurai T, Agata K, Kobayashi S, Watanabe K (2006) Identification and origin of the germline stem cells as revealed by the expression of nanos-related gene in planarians. Dev Growth Differ 48(9):615–628. doi:DGD897[pii]10.1111/j.1440-169X.2006.00897.x

    PubMed  CAS  Google Scholar 

  • Schedl T (1997) Developmental genetics of the germ line. doi:NBK20133 [bookaccession]

    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(1):43–61

    PubMed  CAS  Google Scholar 

  • Schmid M, Kuchler B, Eckmann CR (2009) Two conserved regulatory cytoplasmic poly(A) polymerases, GLD-4 and GLD-2, regulate meiotic progression in C. elegans. Genes Dev 23(7):824–836. doi:23/7/824[pii]10.1101/gad.494009

    PubMed  CAS  Google Scholar 

  • Segal SP, Graves LE, Verheyden J, Goodwin EB (2001) RNA-Regulated TRA-1 nuclear export controls sexual fate. Dev Cell 1(4):539–551. doi:S1534-5807(01)00068-5[pii]

    PubMed  CAS  Google Scholar 

  • Seydoux G, Mello CC, Pettitt J, Wood WB, Priess JR, Fire A (1996) Repression of gene expression in the embryonic germ lineage of C. elegans. Nature 382(6593):713–716. doi:10.1038/382713a0

    PubMed  CAS  Google Scholar 

  • Shibata N, Umesono Y, Orii H, Sakurai T, Watanabe K, Agata K (1999) Expression of vasa(vas)-related genes in germline cells and totipotent somatic stem cells of planarians. Dev Biol 206(1):73–87. doi:S0012-1606(98)99130-8[pii]10.1006/dbio.1998.9130

    PubMed  CAS  Google Scholar 

  • Shibata N, Rouhana L, Agata K (2010) Cellular and molecular dissection of pluripotent adult somatic stem cells in planarians. Dev Growth Differ 52(1):27–41. doi:DGD1155[pii]10.1111/j.1440-169X.2009.01155.x

    PubMed  CAS  Google Scholar 

  • Song X, Xie T (2002) DE-cadherin-mediated cell adhesion is essential for maintaining somatic stem cells in the Drosophila ovary. Proc Natl Acad Sci USA 99(23):14813–14818. doi:10.1073/pnas.232389399 232389399[pii]

    PubMed  CAS  Google Scholar 

  • Song X, Wong MD, Kawase E, Xi R, Ding BC, McCarthy JJ, Xie T (2004) Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development 131(6):1353–1364. doi:10.1242/dev.01026 dev.01026[pii]

    PubMed  CAS  Google Scholar 

  • Steenkamp ET, Wright J, Baldauf SL (2006) The protistan origins of animals and fungi. Mol Biol Evol 23(1):93–106. doi:msj011[pii]10.1093/molbev/msj011

    PubMed  CAS  Google Scholar 

  • Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR, Chen N, Chinwalla A, Clarke L, Clee C, Coghlan A (2003) The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 1(2):E45

    PubMed  Google Scholar 

  • Stothard P, Pilgrim D (2006) Conspecific and interspecific interactions between the FEM-2 and the FEM-3 sex-determining proteins despite rapid sequence divergence. J Mol Evol 62(3):281–291

    PubMed  CAS  Google Scholar 

  • Stothard P, Hansen D, Pilgrim D (2002) Evolution of the PP2C family in Caenorhabditis: rapid divergence of the sex-determining protein FEM-2. J Mol Evol 54(2):267–282

    PubMed  CAS  Google Scholar 

  • Strome S, Wood WB (1983) Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell 35(1):15–25

    PubMed  CAS  Google Scholar 

  • Subramaniam K, Seydoux G (2003) Dedifferentiation of primary spermatocytes into germ cell tumors in C. elegans lacking the pumilio-like protein PUF-8. Curr Biol 13(2):134–139

    PubMed  CAS  Google Scholar 

  • Suh N, Jedamzik B, Eckmann CR, Wickens M, Kimble J (2006) The GLD-2 poly(A) polymerase activates gld-1 mRNA in the Caenorhabditis elegans germ line. Proc Natl Acad Sci USA 103(41):15108–15112. doi:0607050103[pii]10.1073/pnas.0607050103

    PubMed  CAS  Google Scholar 

  • Sulston JE, Horvitz HR (1977) Post-embryonic cell lineages of the nematode Caenorhabditis elegans. Dev Biol 56(1):110–156. doi:0012-1606(77)90158-0[pii]

    PubMed  CAS  Google Scholar 

  • Tam PP, Zhou SX (1996) The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev Biol 178(1):124–132. doi:S0012-1606(96)90203-1[pii]10.1006/dbio.1996.0203

    PubMed  CAS  Google Scholar 

  • Tanurdzic M, Banks JA (2004) Sex-determining mechanisms in land plants. Plant Cell 16(Suppl):S61–S71. doi:10.1105/tpc.016667

    PubMed  CAS  Google Scholar 

  • Tax FE, Yeargers JJ, Thomas JH (1994) Sequence of C. elegans lag-2 reveals a cell-signalling domain shared with Delta and Serrate of Drosophila. Nature 368(6467):150–154. doi:10.1038/368150a0

    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(15):3471–3481

    PubMed  CAS  Google Scholar 

  • Timinszky G, Bortfeld M, Ladurner AG (2008) Repression of RNA polymerase II transcription by a Drosophila oligopeptide. PLoS One 3(6):e2506. doi:10.1371/journal.pone.0002506

    PubMed  Google Scholar 

  • Venkatarama T, Lai F, Luo X, Zhou Y, Newman K, King ML (2010) Repression of zygotic gene expression in the Xenopus germline. Development 137(4):651–660. doi:137/4/651[pii]10.1242/dev.038554

    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(6):1363–1372. doi:10.1093/emboj/20.6.1363

    PubMed  CAS  Google Scholar 

  • Wang JT, Seydoux S (2012) Germ cell specification. Advances in Experimental Medicine and Biology 757:17–39. (Chap. 2, this volume) Springer, New York

    Google Scholar 

  • Wang Y, Zayas RM, Guo T, Newmark PA (2007) nanos function is essential for development and regeneration of planarian germ cells. Proc Natl Acad Sci USA 104(14):5901–5906. doi:0609708104[pii]10.1073/pnas.0609708104

    PubMed  CAS  Google Scholar 

  • Whitington PM, Dixon KE (1975) Quantitative studies of germ plasm and germ cells during early embryogenesis of Xenopus laevis. J Embryol Exp Morphol 33(1):57–74

    PubMed  CAS  Google Scholar 

  • Wickens M, Bernstein DS, Kimble J, Parker R (2002) A PUF family portrait: 3’UTR regulation as a way of life. Trends Genet 18(3):150–157

    PubMed  CAS  Google Scholar 

  • Williamson A, Lehmann R (1996) Germ cell development in Drosophila. Annu Rev Cell Dev Biol 12:365–391. doi:10.1146/annurev.cellbio.12.1.365

    PubMed  CAS  Google Scholar 

  • Wood WB, Laufer JS, Strome S (1982) Developmental determinants in embryos of Caenorhabditis elegans. J Nematol 14(2):267–273

    PubMed  CAS  Google Scholar 

  • Woodruff GC, Eke O, Baird SE, Felix MA, Haag ES (2010) Insights into species divergence and the evolution of hermaphroditism from fertile interspecies hybrids of Caenorhabditis nematodes. Genetics 186(3):997–1012. doi:genetics.110.120550[pii]10.1534/genetics.110.120550

    PubMed  Google Scholar 

  • Wright JE, Gaidatzis D, Senften M, Farley BM, Westhof E, Ryder SP, Ciosk R (2010) A quantitative RNA code for mRNA target selection by the germline fate determinant GLD-1. EMBO J 30(3):533–545. doi:emboj2010334[pii]10.1038/emboj.2010.334

    PubMed  Google Scholar 

  • Wu H-R, Chen Y-T, Su Y-J, Holland L, Yu J-K (2011) Asymmetric localization of germline markers Vasa and Nanos during early development in the amphioxus Branchiostoma floridae. Dev Biol 353(147–59)

    Google Scholar 

  • Xie T, Li L (2007) Stem cells and their niche: an inseparable relationship. Development 134(11):2001–2006. doi:134/11/2001[pii]10.1242/dev.002022

    PubMed  CAS  Google Scholar 

  • Xie T, Spradling AC (2000) A niche maintaining germ line stem cells in the Drosophila ovary. Science 290(5490):328–330. doi:8892[pii]

    PubMed  CAS  Google Scholar 

  • Ying Y, Zhao GQ (2001) Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev Biol 232(2):484–492. doi:10.1006/dbio.2001.0173 S0012-1606(01)90173-3[pii]

    PubMed  CAS  Google Scholar 

  • Ying Y, Qi X, Zhao GQ (2001) Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc Natl Acad Sci USA 98(14):7858–7862. doi:10.1073/pnas.151242798

    PubMed  CAS  Google Scholar 

  • Yochem J, Greenwald I (1989) glp-1 and lin-12, genes implicated in distinct cell-cell interactions in C. elegans, encode similar transmembrane proteins. Cell 58(3):553–563. doi:0092-8674(89)90436-4[pii]

    PubMed  CAS  Google Scholar 

  • Yoon C, Kawakami K, Hopkins N (1997) Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124(16):3157–3165

    PubMed  CAS  Google Scholar 

  • Zanetti S, Puoti A (2012) Sex determination in the C. elegans germline. Advances in Experimental Medicine and Biology 757:41–69. (Chap. 3, this volume) Springer, New York

    Google Scholar 

  • Zarkower D (2006) Somatic sex determination. WormBook:1–12 (http://www.wormbook.org)

  • 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(6659):477–484. doi:10.1038/37297

    PubMed  CAS  Google Scholar 

  • Zhao Z, Flibotte S, Murray JI, Blick D, Boyle TJ, Gupta B, Moerman DG, Waterston RH (2010) New tools for investigating the comparative biology of Caenorhabditis briggsae and C. elegans. Genetics 184(3):853–863. doi:genetics.109.110270[pii]

    PubMed  CAS  Google Scholar 

  • Zhou Y, King ML (1996) Localization of Xcat-2 RNA, a putative germ plasm component, to the mitochondrial cloud in Xenopus stage I oocytes. Development 122:2947–2953

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the community of Caenorhabditis researchers for fostering a collegial and collaborative research culture, and the National Institutes of Health and National Science Foundation for research funding.

Author information

Authors and Affiliations

  1. Department of Biology, University of Maryland, Building 144, College Park, MD, 20742, USA

    Eric S. Haag & Qinwen Liu

Authors
  1. Eric S. Haag
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qinwen Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eric S. Haag .

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

Haag, E.S., Liu, Q. (2013). Using Caenorhabditis to Explore the Evolution of the Germ Line. 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_14

Download citation

Publish with us

Policies and ethics

Search

Navigation