Introduction to Germ Cell Development in Caenorhabditis elegans

Chapter
Part of the Advances in Experimental Medicine and Biology book series (volume 757)

Abstract

A central feature of the continuum of life in sexually reproducing metazoans is the cycle of the germline from one generation to the next. This volume describes the cycle of the germline for Caenorhabditis elegans through chapters that are focused on distinct aspects or processes in germ cell development. Topics include sequential and dependent processes such as specification of germ cells as distinct from somatic cells, sex determination, stem cell proliferative fate versus meiotic development decision, recombination/progression through meiotic prophase, contemporaneous processes such as gametogenesis, meiotic development and apoptosis, and continuing the cycle into the next generation through fertilization and the oocyte-to-embryo transition. Throughout germ cell development, translational control and epigenetic mechanisms play prominent roles. These different aspects of germ cell development are seamlessly integrated under optimal conditions and are modified in the different reproductive strategies that are employed by C. elegans under harsh environmental conditions. In this chapter, we set the stage by providing a brief background on the C. elegans system and germ cell development, indicating processes in the cycle of the germline that are covered in each chapter.

Keywords

C. elegans Germ cell Gametogenesis Meiosis Reproduction Somatic gonad Apoptosis Meiotic recombination Sex determination Fertilization Germline stem cell 

Notes

Acknowledgments

We thank Dave Hansen for comments, and Karen Fiorino for the artwork. Nanette Pazdernik is supported by NIH T32 HD 49305. Research in the Schedl laboratory is supported by R01 GM085150.

References

  1. Ahringer J (2006) Reverse genetics. In: Ambros V (ed) WormBook. ed. The C. elegans Research Community.doi:10.1895/wormbook.1.47.1 Google Scholar
  2. Angelo G, Van Gilst MR (2009) Starvation protects germline stem cells and extends reproductive ­longevity in C. elegans. Science 326(5955):954–958. doi:10.1126/science.1178343 PubMedCrossRefGoogle Scholar
  3. 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(4):589–599. doi:0092-8674(87)90128-0PubMedCrossRefGoogle Scholar
  4. Bailly A, Gartner A (2012) Germ cell apoptosis and DNA damage responses. Advances in Experimental Medicine and Biology 757:249–276. (Chap. 9, this volume) Springer, New YorkGoogle Scholar
  5. Barstead RJ, Moerman DG (2006) C. elegans deletion mutant screening. Methods Mol Biol 351:51–58. doi:10.1385/1-59745-151-7:51 PubMedGoogle Scholar
  6. 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):925–936PubMedGoogle Scholar
  7. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77(1):71–94PubMedGoogle Scholar
  8. Brenner S, Stretton AOW, Kaplan S (1965) Genetic code: the ‘nonsense’ triplets for chain termination and their suppression. Nature 206(4988):994–998PubMedCrossRefGoogle Scholar
  9. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC (1994) Green fluorescent protein as a marker for gene expression. Science 263(5148):802–805PubMedCrossRefGoogle Scholar
  10. Chu DS, Shakes DC (2012) Spermatogenesis. Advances in Experimental Medicine and Biology 757:171–203. (Chap. 7, this volume) Springer, New YorkGoogle Scholar
  11. Felix MA, Braendle C (2010) The natural history of Caenorhabditis elegans. Curr Biol 20(22):R965–R969. doi:10.1016/j.cub.2010.09.050 PubMedCrossRefGoogle Scholar
  12. 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(6669):806–811PubMedCrossRefGoogle Scholar
  13. Frokjaer-Jensen C, Davis MW, Hopkins CE, Newman BJ, Thummel JM, Olesen SP, Grunnet M, Jorgensen EM (2008) Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40(11):1375–1383. doi:10.1038/ng.248 PubMedCrossRefGoogle Scholar
  14. Gibert MA, Starck J, Beguet B (1984) Role of the gonad cytoplasmic core during oogenesis of the nematode Caenorhabditis elegans. Biol Cell 50(1):77–85PubMedCrossRefGoogle Scholar
  15. Govindan JA, Cheng H, Harris JE, Greenstein D (2006) Galphao/i and Galphas signaling function in parallel with the MSP/Eph receptor to control meiotic diapause in C. elegans. Curr Biol 16(13):1257–1268. doi:10.1016/j.cub.2006.05.020 PubMedCrossRefGoogle Scholar
  16. Govindan JA, Nadarajan S, Kim S, Starich TA, Greenstein D (2009) Somatic cAMP signaling regulates MSP-dependent oocyte growth and meiotic maturation in C. elegans. Development 136(13):2211–2221. doi:10.1242/dev.034595 PubMedCrossRefGoogle Scholar
  17. Grant B, Hirsh D (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10(12):4311–4326PubMedGoogle Scholar
  18. Green RA, Kao H-L, Audhya A, Arur S, Mayers JR, Fridolfsson HN, Schulman M, Schloissnig S, Niessen S, Laband K, Wang S, Starr DA, Hyman AA, Schedl T, Desai A, Piano F, Gunsalus KC, Oegema K (2011) A high-resolution C. elegans essential gene network based on phenotypic profiling of a complex tissue. Cell 145(3):470–482PubMedCrossRefGoogle Scholar
  19. Haag ES, Liu Q (2012) Using Caenorhabditis to explore the evolution of the germ line. Advances in Experimental Medicine and Biology 757:405–425. (Chap. 14, this volume) Springer, New YorkGoogle Scholar
  20. Hall DH, Winfrey VP, Blaeuer G, Hoffman LH, Furuta T, Rose KL, Hobert O, Greenstein D (1999) Ultrastructural features of the adult hermaphrodite gonad of Caenorhabditis elegans: relations between the germ line and soma. Dev Biol 212(1):101–123PubMedCrossRefGoogle Scholar
  21. 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 YorkGoogle Scholar
  22. Hedgecock EM, Culotti JG, Hall DH, Stern BD (1987) Genetics of cell and axon migrations in Caenorhabditis elegans. Development 100(3):365–382PubMedGoogle Scholar
  23. Hirsh D, Oppenheim D, Klass M (1976) Development of the reproductive system of Caenorhabditis elegans. Dev Biol 49(1):200–219PubMedCrossRefGoogle Scholar
  24. Hobert O (2010) The impact of whole genome sequencing on model system genetics: get ready for the ride. Genetics 184(2):317–319. doi:10.1534/genetics.109.112938 PubMedCrossRefGoogle Scholar
  25. Hodgkin J (1986) Sex determination in the nematode C. elegans: analysis of tra-3 suppressors and characterization of fem genes. Genetics 114:15–52PubMedGoogle Scholar
  26. Hodgkin J, Barnes TM (1991) More is not better: brood size and population growth in a self-­fertilizing nematode. Proc R Soc Lond B Biol Sci 246(1315):19–24. doi:10.1098/rspb.1991.0119 CrossRefGoogle Scholar
  27. Hubbard EJ, Korta DZ, Dalfó D (2012) Physiological control of germline development. Advances in Experimental Medicine and Biology 757:101–131. (Chap. 5, this volume) Springer, New YorkGoogle Scholar
  28. Jakubowski J, Kornfeld K (1999) A local, high-density, single-nucleotide polymorphism map used to clone Caenorhabditis elegans cdf-1. Genetics 153(2):743–752PubMedGoogle Scholar
  29. Jaramillo-Lambert A, Ellefson M, Villeneuve AM, Engebrecht J (2007) Differential timing of S phases, X chromosome replication, and meiotic prophase in the C. elegans germ line. Dev Biol 308(1):206–221. doi:10.1016/j.ydbio.2007.05.019 PubMedCrossRefGoogle Scholar
  30. Kelly WG, Fire A (1998) Chromatin silencing and the maintenance of a functional germline in Caenorhabditis elegans. Development 125(13):2451–2456PubMedGoogle Scholar
  31. Kelly WG, Schaner CE, Dernburg AF, Lee MH, Kim SK, Villeneuve AM, Reinke V (2002) X-chromosome silencing in the germline of C. elegans. Development 129(2):479–492PubMedGoogle Scholar
  32. Killian DJ, Hubbard EJ (2005) Caenorhabditis elegans germline patterning requires coordinated development of the somatic gonadal sheath and the germ line. Dev Biol 279(2):322–335. doi:10.1016/j.ydbio.2004.12.021 PubMedCrossRefGoogle Scholar
  33. Kim S, Spike CA, Greenstein D (2012) Control of oocyte growth and meiotic maturation in C. elegans. Advances in Experimental Medicine and Biology 757:277–320. (Chap. 10, this volume) Springer, New YorkGoogle Scholar
  34. Kimble J, Hirsh D (1979) The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev Biol 70(2):396–417PubMedCrossRefGoogle Scholar
  35. 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 PubMedCrossRefGoogle Scholar
  36. 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(4):2039–2062. doi:10.1534/genetics.107.081356 PubMedCrossRefGoogle Scholar
  37. Lui DY, Colaiácovo MP (2012) Meiotic development in C. elegans. Advances in Experimental Medicine and Biology 757:133–170. (Chap. 6, this volume) Springer, New YorkGoogle Scholar
  38. Maddox AS, Habermann B, Desai A, Oegema K (2005) Distinct roles for two C. elegans anillins in the gonad and early embryo. Development 132(12):2837–2848. doi:10.1242/dev.01828 PubMedCrossRefGoogle Scholar
  39. Marcello MR, Singaravelu G, Singson A (2012) Fertilization. Advances in Experimental Medicine and Biology 757:321–350. (Chap. 11, this volume) Springer, New YorkGoogle Scholar
  40. Maupas (1900) Modes et formes de reproduction des nematodes. Translation by Marie-Anne Felix. Archives de Zoologie Experimentale et Generale 8:463–624Google Scholar
  41. 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 PubMedCrossRefGoogle Scholar
  42. McCarter J, Bartlett B, Dang T, Schedl T (1999) On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205(1):111–128. doi:10.1006/dbio.1998.9109 PubMedCrossRefGoogle Scholar
  43. Merritt C, Seydoux G (2010) Transgenic solutions for the germline. WormBook:1–21. doi:10.1895/wormbook.1.148.1 Google Scholar
  44. 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. doi:10.1016/j.cub.2008.08.013 PubMedCrossRefGoogle Scholar
  45. Miller MA, Nguyen VQ, Lee MH, Kosinski M, Schedl T, Caprioli RM, Greenstein D (2001) A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291(5511):2144–2147. doi:10.1126/science.1057586291/5511/2144 PubMedCrossRefGoogle Scholar
  46. Miller MA, Ruest PJ, Kosinski M, Hanks SK, Greenstein D (2003) An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans. Genes Dev 17(2):187–200. doi:10.1101/gad.1028303 PubMedCrossRefGoogle Scholar
  47. Morrison SJ, Spradling AC (2008) Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132(4):598–611. doi:10.1016/j.cell.2008.01.038 PubMedCrossRefGoogle Scholar
  48. Nadarajan S, Govindan JA, McGovern M, Hubbard EJ, Greenstein D (2009) MSP and GLP-1/Notch signaling coordinately regulate actomyosin-dependent cytoplasmic streaming and oocyte growth in C. elegans. Development 136(13):2223–2234. doi:10.1242/dev.034603 PubMedCrossRefGoogle Scholar
  49. 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 YorkGoogle Scholar
  50. Reinke V, Gil IS, Ward S, Kazmer K (2004) Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131(2):311–323. doi:10.1242/dev.00914 PubMedCrossRefGoogle Scholar
  51. Robertson S, Lin R (2012) The oocyte-to-embryo transition. Advances in Experimental Medicine and Biology 757:351–372. (Chap. 12, this volume) Springer, New YorkGoogle Scholar
  52. Sarin S, Prabhu S, O’Meara MM, Pe’er I, Hobert O (2008) Caenorhabditis elegans mutant allele identification by whole-genome sequencing. Nat Methods 5(10):865–867. doi:10.1038/nmeth.1249 PubMedCrossRefGoogle Scholar
  53. Schisa JA, Pitt JN, Priess JR (2001) Analysis of RNA associated with P granules in germ cells of C. elegans adults. Development 128(8):1287–1298PubMedGoogle Scholar
  54. Seidel HS, Kimble J (2011) The oogenic germline starvation response in C. elegans. PLoS One 6(12):e28074. doi:10.1371/journal.pone.0028074 Google Scholar
  55. Sijen T, Fleenor J, Simmer F, Thijssen KL, Parrish S et al (2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107:465–476PubMedCrossRefGoogle Scholar
  56. Sulston JE, Horvitz HR (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56(1):110–156PubMedCrossRefGoogle Scholar
  57. Van Wynsberghe PM, Maine EM (2012) Epigenetic control of germline development. Advances in Experimental Medicine and Biology 757:373–403. (Chap. 13, this volume) Springer, New YorkGoogle Scholar
  58. Wang JT, Seydoux S (2012) Germ cell specification. Advances in Experimental Medicine and Biology 757:17–39. (Chap. 2, this volume) Springer, New YorkGoogle Scholar
  59. Ward S, Carrel JS (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73(2):304–321PubMedCrossRefGoogle Scholar
  60. Ward S, Argon Y, Nelson GA (1981) Sperm morphogenesis in wild-type and fertilization-defective mutants of Caenorhabditis elegans. J Cell Biol 91(1):26–44PubMedCrossRefGoogle Scholar
  61. Wicks SR, Yeh RT, Gish WR, Waterston RH, Plasterk RH (2001) Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat Genet 28(2):160–164. doi:10.1038/88878 PubMedCrossRefGoogle Scholar
  62. Wolke U, Jezuit EA, Priess JR (2007) Actin-dependent cytoplasmic streaming in C. elegans oogenesis. Development 134(12):2227–2236. doi:10.1242/dev.004952 PubMedCrossRefGoogle Scholar
  63. Wood AJ, Lo TW, Zeitler B, Pickle CS, Ralston EJ, Lee AH, Amora R, Miller JC, Leung E, Meng X, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Meyer BJ (2011) Targeted genome editing across species using ZFNs and TALENs. Science 333(6040):307. doi:10.1126/science.1207773PubMedCrossRefGoogle Scholar
  64. Yochem J, Herman RK (2003) Investigating C. elegans development through mosaic analysis. Development 130(20):4761–4768. doi:10.1242/dev.00701Google Scholar
  65. 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 YorkGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of GeneticsWashington University School of MedicineSt. LouisUSA

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