Advertisement

Roles of Germline Stem Cells and Somatic Multipotent Stem Cells in Hydra Sexual Reproduction

  • Chiemi Nishimiya-Fujisawa
  • Satoru Kobayashi
Chapter
Part of the Diversity and Commonality in Animals book series (DCA)

Abstract

In Hydra, there are distinct germline stem cells (GSCs). The GSCs are cell-autonomously sex determined in Hydra: there are egg-restricted stem cells (EgSCs) and sperm-restricted stem cells (SpSCs). The sex of the individual polyp is determined by the sex of the GSCs present in the body: polyps that have EgSCs are female and produce eggs; while polyps that have SpSCs are male and produce sperm. Occasionally an EgSC transdetermines into an SpSC. The newly emerged SpSC proliferates vigorously and then differentiates into sperm, while EgSCs are eliminated in the presence of SpSCs. Thus, the animal changes sex from female to male. This process is called masculinization. The third stem cell type in Hydra is referred to as multipotent stem cells (MPSCs). MPSCs are somatic stem cells in normal polyps and differentiate exclusively into somatic cells such as nerve cells and nematocytes (cnidarian stinging cells). However, if GSCs are lost during asexual reproduction by budding or regeneration, new ones are regenerated from MPSCs. Thus, sexual reproduction is guaranteed for every polyp. In the rest of this chapter we further discuss the nature of MPSCs found in other lower metazoans and the absence of MPSCs in cnidarians other than hydrozoans.

Keywords

Germline stem cells Multipotent stem cells Sex determination Masculinization Cell plasticity Hydra Cnidaria 

Notes

Acknowledgements

We thank Dr. T. Fujisawa for critical reading of the manuscript and for support and encouragement. We are grateful to all members of the Kobayashi Project at the TARA Life Science Center for Survival Dynamics, University of Tsukuba, for discussions.

This work was supported in part by a Grant-in-Aid for Scientific Research (KAKENHI) on Innovative Areas, “Mechanisms Regulating Gamete Formation in Animals” (#25114002) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) to Satoru Kobayashi; KAKENHI (A) (#24247011) from the Japan Society for the Promotion of Science (JSPS) to Satoru Kobayashi; and a Grant-in-Aid for Challenging Exploratory Research (#15K14565) from JSPS to Chiemi Nishimiya-Fujisawa.

References

  1. Agata K, Nakajima E, Funayama N et al (2006) Two different evolutionary origins of stem cell systems and their molecular basis. Semin Cell Dev Biol 17:503–509.  https://doi.org/10.1016/j.semcdb.2006.05.004 CrossRefPubMedGoogle Scholar
  2. Alexandrova O, Schade M, Böttger A, David CN (2005) Oogenesis in Hydra: nurse cells transfer cytoplasm directly to the growing oocyte. Dev Biol 281:91–101.  https://doi.org/10.1016/j.ydbio.2005.02.015 CrossRefPubMedGoogle Scholar
  3. Alié A, Hayashi T, Sugimura I et al (2015) The ancestral gene repertoire of animal stem cells. Proc Natl Acad Sci U S A.  https://doi.org/10.1073/pnas.1514789112
  4. Anokhin B, Hemmrich-Stanisak G, Bosch T (2010) Karyotyping and single-gene detection using fluorescence in situ hybridization on chromosomes of Hydra magnipapillata (Cnidaria: Hydrozoa). Comp Cytogenet 4:97–110.  https://doi.org/10.3897/compcytogen.v4i2.41 CrossRefGoogle Scholar
  5. Beckmann A, Özbek S (2012) The nematocyst: a molecular map of the cnidarian stinging organelle. Int J Dev Biol 56:577–582.  https://doi.org/10.1387/ijdb.113472ab CrossRefPubMedGoogle Scholar
  6. Bode H, Berking S, David CN et al (1973) Quantitative analysis of cell types during growth and morphogenesis in Hydra. W Roux’ Arch f Entwicklungsmechanik 171:269–285.  https://doi.org/10.1007/BF00577725 CrossRefGoogle Scholar
  7. Bode HR, Flick KM, Smith GS (1976) Regulation of interstitial cell differentiation in Hydra attenuata. I Homeostatic control of interstitial cell population size. J Cell Sci 20:29–46PubMedGoogle Scholar
  8. Bode HR, Heimfeld S, Chow MA, Huang LW (1987) Gland cells arise by differentiation from interstitial cells in Hydra attenuata. Dev Biol 122:577–585.  https://doi.org/10.1016/0012-1606(87)90321-6 CrossRefPubMedGoogle Scholar
  9. Bosch TC, David CN (1986) Male and female stem cells and sex reversal in Hydra polyps. Proc Natl Acad Sci U S A 83:9478–9482CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bosch TCG, David CN (1987) Stem cells of Hydra magnipapillata can differentiate into somatic cells and germ line cells. Dev Biol 121:182–191.  https://doi.org/10.1016/0012-1606(87)90151-5 CrossRefGoogle Scholar
  11. Brien P (1962) Contribution a l’etude de la biologie sexuelle. Induction gametique et sexuelle chez les Hydres d’eau deuce par des greffes en parabiose. Bull Acad Roy Belg CL Sci 46:825–847Google Scholar
  12. Brien P (1963) Contribution a l’etude de la biologie sexuelle chez les Hydres d’eau douce. Induction gametique et sexuelle par la methode des greffes en parabiose. Bull Bio France/Belg 97:213–283Google Scholar
  13. Burgoyne PS (1987) The role of the mammalian Y chromosome in spermatogenesis. Development 101(Suppl):133–141PubMedGoogle Scholar
  14. Campbell RD (1985) Sex determination in hydra: roles of germ cells (interstitial cells) and somatic cells. J Exp Zool 234(3):451–458CrossRefGoogle Scholar
  15. Campbell RD (1997) Finding the forces that cause budding morphogenesis in hydra. In: 7th international workshop on hydroid development. Tutzing, Germany, September 22–25Google Scholar
  16. Campbell RD, David CN (1974) Cell cycle kinetics and development of Hydra attenuata. II. Interstitial cells. J Cell Sci 16:349–358PubMedGoogle Scholar
  17. Chapman JA, Kirkness EF, Simakov O et al (2010) The dynamic genome of Hydra. Nature 464:592–596.  https://doi.org/10.1038/nature08830 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Collins AG, Schuchert P, Marques AC et al (2006) Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst Biol 55:97–115.  https://doi.org/10.1080/10635150500433615 CrossRefPubMedGoogle Scholar
  19. David C (1973) A quantitative method for maceration of Hydra tissue. Wilhelm Roux’ Arch 171:259–268CrossRefGoogle Scholar
  20. David CN (2012) Interstitial stem cells in Hydra: multipotency and decision-making. Int J Dev Biol 56:489–497.  https://doi.org/10.1387/ijdb.113476cd CrossRefPubMedGoogle Scholar
  21. David CN, Gierer A (1974) Cell cycle kinetics and development of Hydra attenuata. III. Nerve and nematocyte differentiation. J Cell Sci 16:359–375PubMedGoogle Scholar
  22. David CN, Murphy S (1977) Characterization of interstitial stem cells in Hydra by cloning. Dev Biol 58:372–383CrossRefPubMedGoogle Scholar
  23. David CN, Fujisawa T, Bosch TCG (1991) Interstitial stem cell proliferation in Hydra: evidence for strain-specific regulatory signals. Dev Biol 148:501–507.  https://doi.org/10.1016/0012-1606(91)90268-8 CrossRefPubMedGoogle Scholar
  24. Diehl FA, Burnett AL (1964) The role of interstitial cells in the maintenance of Hydra. I. Specific destruction of interstitial cells in normal, asexual, non-budding animals. J Exp Zool 155:253–259CrossRefPubMedGoogle Scholar
  25. Dübel S (1989) Cell differentiation in the head of Hydra. Differentiation 41:99–109.  https://doi.org/10.1111/j.1432-0436.1989.tb00737.x CrossRefGoogle Scholar
  26. Dübel S, Schaller HC (1990) Terminal differentiation of ectodermal epithelial stem cells of Hydra can occur in G2 without requiring mitosis or S phase. J Cell Biol 110:939–945.  https://doi.org/10.1083/jcb.110.4.939 CrossRefPubMedGoogle Scholar
  27. Extavour CG, Pang K, Matus DQ, Martindale MQ (2005) vasa and nanos expression patterns in a sea anemone and the evolution of bilaterian germ cell specification mechanisms. Evol Dev 7:201–215.  https://doi.org/10.1111/j.1525-142X.2005.05023.x CrossRefPubMedGoogle Scholar
  28. Finnerty JR, Pang K, Burton P et al (2004) Origins of bilateral symmetry: Hox and Dpp expression in a sea anemone. Science 304:1335–1337.  https://doi.org/10.1126/science.1091946 CrossRefPubMedGoogle Scholar
  29. Foox J, Siddall ME (2015) The road to Cnidaria: history of phylogeny of the Myxozoa. J Parasitol 101:269–274.  https://doi.org/10.1645/14-671.1 CrossRefPubMedGoogle Scholar
  30. Funayama N, Nakatsukasa M, Mohri K et al (2010) Piwi expression in archeocytes and choanocytes in demosponges: insights into the stem cell system in demosponges. Evol Dev 12:275–287.  https://doi.org/10.1111/j.1525-142X.2010.00413.x CrossRefPubMedGoogle Scholar
  31. Galliot B, Schmid V (2002) Cnidarians as a model system for understanding evolution and regeneration. Int J Dev Biol 46:39–48PubMedGoogle Scholar
  32. Genikhovich G, Kürn U, Hemmrich G, Bosch TCG (2006) Discovery of genes expressed in Hydra embryogenesis. Dev Biol 289:466–481.  https://doi.org/10.1016/j.ydbio.2005.10.028 CrossRefPubMedGoogle Scholar
  33. Gierer A, Berking S, Bode H et al (1972) Regeneration of Hydra from reaggregated cells. Nat New Biol 239:98–101CrossRefPubMedGoogle Scholar
  34. Goetsch W (1922) Gonochorismus und Hermaphroditismus bei Hydrozoen. Zool Anz 55:30–34Google Scholar
  35. Gold DA, Jacobs DK (2013) Stem cell dynamics in Cnidaria: are there unifying principles? Dev Genes Evol:1–14.  https://doi.org/10.1007/s00427-012-0429-1
  36. Gold DA, Gates RD, Jacobs DK (2014) The early expansion and evolutionary dynamics of POU class genes. Mol Biol Evol 31:3136–3147.  https://doi.org/10.1093/molbev/msu243 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Hager G, David CN (1997) Pattern of differentiated nerve cells in Hydra is determined by precursor migration. Development 124:569–576PubMedGoogle Scholar
  38. Hara K, Nakagawa T, Enomoto H et al (2014) Mouse spermatogenic stem cells continually interconvert between equipotent singly isolated and syncytial states. Cell Stem Cell 14:658–672.  https://doi.org/10.1016/j.stem.2014.01.019 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Hashiyama K, Hayashi Y, Kobayashi S (2011) Drosophila sex lethal gene initiates female development in germline progenitors. Science 333:885–888.  https://doi.org/10.1126/science.1208146 CrossRefPubMedGoogle Scholar
  40. Hemmrich G, Khalturin K, Boehm A-M et al (2012) Molecular signatures of the three stem cell lineages in Hydra and the emergence of stem cell function at the base of multicellularity. Mol Biol Evol.  https://doi.org/10.1093/molbev/mss134
  41. Hobmayer B, Jenewein M, Eder D et al (2012) Stemness in Hydra—a current perspective. Int J Dev Biol.  https://doi.org/10.1387/ijdb.113426bh
  42. Holstein TW, David CN (1990) Cell cycle length, cell size, and proliferation rate in Hydra stem cells. Dev Biol 142:392–400.  https://doi.org/10.1016/0012-1606(90)90360-U CrossRefPubMedGoogle Scholar
  43. Honegger TG, Zürrer D, Tardent P (1989) Oogenesis in Hydra carnea: a new model based on light and electron microscopic analyses of oocyte and nurse cell differentiation. Tissue Cell 21:381–393.  https://doi.org/10.1016/0040-8166(89)90052-9 CrossRefPubMedGoogle Scholar
  44. Hyman LH (1928) Miscellaneous observations on hydra, with special reference to reproduction. Biol Bull 54:65–108–1CrossRefGoogle Scholar
  45. Ikami K, Tokue M, Sugimoto R, et al. (2015) Hierarchical differentiation competence in response to retinoic acid ensures stem cell maintenance during mouse spermatogenesis. Development 142:1582–1592. dev. 118695.  https://doi.org/10.1242/dev.118695 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Iwamori T, Iwamori N, Ma L et al (2010) TEX14 interacts with CEP55 to block cell abscission. Mol Cell Biol 30:2280–2292.  https://doi.org/10.1128/MCB.01392-09 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Jiménez-Guri E, Philippe H, Okamura B, Holland PWH (2007) Buddenbrockia is a Cnidarian worm. Science 317:116–118.  https://doi.org/10.1126/science.1142024 CrossRefPubMedGoogle Scholar
  48. Juliano C, Wessel G (2010) Versatile germline genes. Science 329:640–641.  https://doi.org/10.1126/science.1194037 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Juliano CE, Voronina E, Stack C et al (2006) Germ line determinants are not localized early in sea urchin development, but do accumulate in the small micromere lineage. Dev Biol 300:406–415.  https://doi.org/10.1016/j.ydbio.2006.07.035 CrossRefPubMedGoogle Scholar
  50. Juliano CE, Swartz SZ, Wessel GM (2010a) A conserved germline multipotency program. Development 137:4113–4126.  https://doi.org/10.1242/dev.047969 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Juliano CE, Yajima M, Wessel GM (2010b) Nanos functions to maintain the fate of the small micromere lineage in the sea urchin embryo. Dev Biol 337:220–232.  https://doi.org/10.1016/j.ydbio.2009.10.030 CrossRefPubMedGoogle Scholar
  52. Juliano CE, Reich A, Liu N et al (2014) PIWI proteins and PIWI-interacting RNAs function in Hydra somatic stem cells. PNAS 111:337–342.  https://doi.org/10.1073/pnas.1320965111 CrossRefPubMedGoogle Scholar
  53. Kayal E, Bentlage B, Collins AG et al (2012) Evolution of linear mitochondrial genomes in medusozoan cnidarians. Genome Biol Evol 4:1–12.  https://doi.org/10.1093/gbe/evr123 CrossRefPubMedGoogle Scholar
  54. Kayal E, Roure B, Philippe H et al (2013) Cnidarian phylogenetic relationships as revealed by mitogenomics. BMC Evol Biol 13:5.  https://doi.org/10.1186/1471-2148-13-5 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Kloc M, Bilinski S, Dougherty MT et al (2004) Formation, architecture and polarity of female germline cyst in Xenopus. Dev Biol 266:43–61.  https://doi.org/10.1016/j.ydbio.2003.10.002 CrossRefPubMedGoogle Scholar
  56. Künzel T, Heiermann R, Frank U et al (2010) Migration and differentiation potential of stem cells in the cnidarian Hydractinia analysed in eGFP-transgenic animals and chimeras. Dev Biol 348:120–129.  https://doi.org/10.1016/j.ydbio.2010.08.017 CrossRefPubMedGoogle Scholar
  57. Kuznetsov S, Lyanguzowa M, Bosch TC (2001) Role of epithelial cells and programmed cell death in Hydra spermatogenesis. Zoology (Jena) 104:25–31.  https://doi.org/10.1078/0944-2006-00005 CrossRefGoogle Scholar
  58. Leclère L, Jager M, Barreau C et al (2012) Maternally localized germ plasm mRNAs and germ cell/stem cell formation in the cnidarian Clytia. Dev Biol.  https://doi.org/10.1016/j.ydbio.2012.01.018
  59. Lim AK, Kai T (2007) Unique germ-line organelle, nuage, functions to repress selfish genetic elements in Drosophila melanogaster. PNAS 104:6714–6719.  https://doi.org/10.1073/pnas.0701920104 CrossRefPubMedGoogle Scholar
  60. Lim RSM, Anand A, Nishimiya-Fujisawa C et al (2014) Analysis of Hydra PIWI proteins and piRNAs uncover early evolutionary origins of the piRNA pathway. Dev Biol 386:237–251.  https://doi.org/10.1016/j.ydbio.2013.12.007 CrossRefPubMedGoogle Scholar
  61. Lin H, Spradling AC (1993) Germline stem cell division and egg chamber development in transplanted Drosophila germaria. Dev Biol 159:140–152.  https://doi.org/10.1006/dbio.1993.1228 CrossRefPubMedGoogle Scholar
  62. Littlefield CL (1984) The interstitial cells control the sexual phenotype of heterosexual chimeras of Hydra. Dev Biol 102:426–432CrossRefPubMedGoogle Scholar
  63. Littlefield CL (1985) Germ cells in Hydra oligactis males. I. Isolation of a subpopulation of interstitial cells that is developmentally restricted to sperm production. Dev Biol, 112:185–193. doi: 4054434Google Scholar
  64. Littlefield CL (1986) Germ cells control sex determination in Hydra. Prog Clin Biol Res 217A:175–178. doi: 3749129PubMedGoogle Scholar
  65. Littlefield CL (1991) Cell lineages in Hydra: isolation and characterization of an interstitial stem cell restricted to egg production in Hydra oligactis. Dev Biol 143:378–388. doi: 1991559CrossRefGoogle Scholar
  66. Littlefield L (1994) Cell–cell interactions and the control of sex determination in Hydra. Semin Dev Biol 5:13–20.  https://doi.org/10.1006/sedb.1994.1003 CrossRefGoogle Scholar
  67. Littlefield CL, Dunne JF, Bode HR (1985) Spermatogenesis in Hydra oligactis. I. Morphological description and characterization using a monoclonal antibody specific for cells of the spermatogenic pathway. Dev Biol 110:308–320. doi: 4018401CrossRefPubMedGoogle Scholar
  68. Mahowald AP (1962) Fine structure of pole cells and polar granules in Drosophila melanogaster. J Exp Zool 151:201–215.  https://doi.org/10.1002/jez.1401510302 CrossRefGoogle Scholar
  69. Mahowald AP (1972) Ultrastructural observations on oogenesis in Drosophila. J Morphol 137:29–48.  https://doi.org/10.1002/jmor.1051370103 CrossRefPubMedGoogle Scholar
  70. Mahowald AP, Hennen S (1971) Ultrastructure of the “germ plasm” in eggs and embryos of Rana pipiens. Dev Biol 24:37–53.  https://doi.org/10.1016/0012-1606(71)90045-5 CrossRefPubMedGoogle Scholar
  71. Marlow H, Roettinger E, Boekhout M, Martindale MQ (2012) Functional roles of Notch signaling in the cnidarian Nematostella vectensis. Dev Biol 362:295–308.  https://doi.org/10.1016/j.ydbio.2011.11.012 CrossRefPubMedGoogle Scholar
  72. Martin VJ, Littlefield CL, Archer WE, Bode HR (1997) Embryogenesis in Hydra. Biol Bull 192:345–363CrossRefPubMedGoogle Scholar
  73. Martínez DE, Bridge D (2012) Hydra, the everlasting embryo, confronts aging. Int J Dev Biol.  https://doi.org/10.1387/ijdb.113461dm
  74. McLaren A (1981) The fate of germ cells in the testis of fetal sex-reversed mice. J Reprod Fertil 61:461–467CrossRefPubMedGoogle Scholar
  75. Millane RC, Kanska J, Duffy DJ et al (2011) Induced stem cell neoplasia in a cnidarian by ectopic expression of a POU domain transcription factor. Development 138:2429–2439.  https://doi.org/10.1242/dev.064931 CrossRefPubMedGoogle Scholar
  76. Miller MA, Technau U, Smith KM, Steele RE (2000) Oocyte development in Hydra involves selection from competent precursor cells. Dev Biol 224:326–338.  https://doi.org/10.1006/dbio.2000.9790 CrossRefPubMedGoogle Scholar
  77. Mochizuki K, Sano H, Kobayashi S et al (2000) Expression and evolutionary conservation of nanos-related genes in Hydra. Dev Genes Evol 210:591–602. doi: 11151296CrossRefGoogle Scholar
  78. Mochizuki K, Nishimiya-Fujisawa C, Fujisawa T (2001) Universal occurrence of the vasa-related genes among metazoans and their germline expression in Hydra. Dev Genes Evol 211:299–308.  https://doi.org/10.1007/s004270100156 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Morrison SJ, Spradling AC (2008) Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132:598–611.  https://doi.org/10.1016/j.cell.2008.01.038 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Müller WA, Teo R, Frank U (2004) Totipotent migratory stem cells in a hydroid. Dev Biol 275:215–224.  https://doi.org/10.1016/j.ydbio.2004.08.006 CrossRefPubMedGoogle Scholar
  81. Munck A, David CN (1985) Cell proliferation and differentiation kinetics during spermatogenesis in Hydra carnea. Wilhelm Rouxs Arch Dev Biol 194:247–256.  https://doi.org/10.1007/BF01152170 CrossRefGoogle Scholar
  82. Nakamura S, Kobayashi K, Nishimura T et al (2010) Identification of germline stem cells in the ovary of the teleost medaka. Science 328:1561–1563.  https://doi.org/10.1126/science.1185473 CrossRefPubMedGoogle Scholar
  83. Nakanishi N, Renfer E, Technau U, Rentzsch F (2012) Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms. Development 139:347–357.  https://doi.org/10.1242/dev.071902 CrossRefPubMedGoogle Scholar
  84. Nishimiya-Fujisawa C, Kobayashi S (2012) Germline stem cells and sex determination in Hydra. Int J Dev Biol 56:499–508.  https://doi.org/10.1387/ijdb.123509cf CrossRefPubMedPubMedCentralGoogle Scholar
  85. Nishimiya-Fujisawa C, Sugiyama T (1993) Genetic analysis of developmental mechanisms in Hydra. XX. Cloning of interstitial stem cells restricted to the sperm differentiation pathway in Hydra magnipapillata. Dev Biol 157:1–9.  https://doi.org/10.1006/dbio.1993.1106 CrossRefPubMedGoogle Scholar
  86. Nishimiya-Fujisawa C, Sugiyama T (1995) Genetic analysis of developmental mechanisms in Hydra. XXII. Two types of female germ stem cells are present in a male strain of Hydra magnipapillata. Dev Biol 172:324–336.  https://doi.org/10.1006/dbio.1995.0026 CrossRefPubMedGoogle Scholar
  87. Nishimura T, Sato T, Yamamoto Y et al (2015) foxl3 is a germ cell–intrinsic factor involved in sperm–egg fate decision in medaka. Science 349:328–331.  https://doi.org/10.1126/science.aaa2657 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Noda K (1970) The fate of aggregates formed by two species of Hydra (Hydra magnipapillata and Pelmatohydra robusta). J Fac Sci Hokkaido Univ Ser Vi Zool 17:432–439Google Scholar
  89. Noda K (1971) Reconstitution of dissociated cells of Hydra. Zool Mag 80:99–101Google Scholar
  90. Noda K, Kanai C (1977) An ultrastructural observation on Pelmatohydra robusta at sexual and asexual stages, with a special reference to “germinal plasm”. J Ultrastruct Res 61:284–294.  https://doi.org/10.1016/S0022-5320(77)80053-1 CrossRefPubMedGoogle Scholar
  91. Noda K, Kanai C (1980) An ultrastructural observation on the embryogenesis of Pelmatohydra robusta, with special reference to “germinal dense bodies”. In: Tardent P, Tardent R (eds) Developmental and cellular biology of coelenterates. Elsevier, North-HollandGoogle Scholar
  92. Önal P, Grun D, Adamidi C et al (2012) Gene expression of pluripotency determinants is conserved between mammalian and planarian stem cells. EMBO J 31:2755–2769.  https://doi.org/10.1038/emboj.2012.110 CrossRefPubMedPubMedCentralGoogle Scholar
  93. Palakodeti D, Smielewska M, Lu Y-C et al (2008) The PIWI proteins SMEDWI-2 and SMEDWI-3 are required for stem cell function and piRNA expression in planarians. RNA 14:1174–1186.  https://doi.org/10.1261/rna.1085008 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Park E, Hwang D-S, Lee J-S et al (2012) Estimation of divergence times in cnidarian evolution based on mitochondrial protein-coding genes and the fossil record. Mol Phylogenet Evol 62:329–345.  https://doi.org/10.1016/j.ympev.2011.10.008 CrossRefPubMedGoogle Scholar
  95. Pepling ME, Spradling AC (1998) Female mouse germ cells form synchronously dividing cysts. Development 125:3323–3328PubMedGoogle Scholar
  96. Putnam NH, Srivastava M, Hellsten U et al (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86–94.  https://doi.org/10.1126/science.1139158 CrossRefPubMedGoogle Scholar
  97. Rabinowitz JS, Chan XY, Kingsley EP et al (2008) Nanos is required in somatic blast cell lineages in the posterior of a mollusk embryo. Curr Biol 18:331–336.  https://doi.org/10.1016/j.cub.2008.01.055 CrossRefPubMedGoogle Scholar
  98. Ransick A, Cameron RA, Davidson EH (1996) Postembryonic segregation of the germ line in sea urchins in relation to indirect development. Proc Natl Acad Sci U S A 93:6759–6763CrossRefPubMedPubMedCentralGoogle Scholar
  99. Rebscher N (2014) Establishing the germline in spiralian embyos. Int J Dev Biol 58:403–411.  https://doi.org/10.1387/ijdb.140125nr CrossRefPubMedGoogle Scholar
  100. Rebscher N, Volk C, Teo R, Plickert G (2008) The germ plasm component vasa allows tracing of the interstitial stem cells in the cnidarian Hydractinia echinata. Dev Dyn 237:1736–1745.  https://doi.org/10.1002/dvdy.21562 CrossRefPubMedGoogle Scholar
  101. Rebscher N, Lidke AK, Ackermann CF (2012) Hidden in the crowd: primordial germ cells and somatic stem cells in the mesodermal posterior growth zone of the polychaete Platynereis dumerillii are two distinct cell populations. EvoDevo 3:9.  https://doi.org/10.1186/2041-9139-3-9 CrossRefPubMedPubMedCentralGoogle Scholar
  102. Richards GS, Rentzsch F (2014) Transgenic analysis of a SoxB gene reveals neural progenitor cells in the cnidarian Nematostella vectensis. Development 141:4681–4689.  https://doi.org/10.1242/dev.112029 CrossRefPubMedGoogle Scholar
  103. Sato K, Shibata N, Orii H et al (2006) Identification and origin of the germline stem cells as revealed by the expression of nanos-related gene in planarians. Develop Growth Differ 48:615–628.  https://doi.org/10.1111/j.1440-169X.2006.00897.x CrossRefGoogle Scholar
  104. Schmid V (1992) Transdifferentiation in medusae. In: Friedlander KWJ, M (ed) International review of cytology. Academic Press, pp 213–261. https://www.sciencedirect.com/science/article/pii/S007476960862077X?via%3Dihub Google Scholar
  105. Schmid V, Alder H (1984) Isolated, mononucleated, striated muscle can undergo pluripotent transdifferentiation and form a complex regenerate. Cell 38:801–809.  https://doi.org/10.1016/0092-8674(84)90275-7 CrossRefPubMedGoogle Scholar
  106. Schmid V, Wydler M, Alder H (1982) Transdifferentiation and regeneration in vitro. Dev Biol 92:476–488.  https://doi.org/10.1016/0012-1606(82)90193-2 CrossRefPubMedGoogle Scholar
  107. Schmidt T, David CN (1986) Gland cells in Hydra: cell cycle kinetics and development. J Cell Sci 85:197–215PubMedGoogle Scholar
  108. Seipel K, Schmid V (2006) Mesodermal anatomies in cnidarian polyps and medusae. Int J Dev Biol 50:589–599.  https://doi.org/10.1387/ijdb.062150ks CrossRefPubMedGoogle Scholar
  109. Seipel K, Yanze N, Schmid V (2004) The germ line and somatic stem cell gene Cniwi in the jellyfish Podocoryne carnea. Int J Dev Biol 48:1–7CrossRefPubMedGoogle Scholar
  110. Shibata N, Umesono Y, Orii H et al (1999) Expression of vasa(vas)-related genes in germline cells and totipotent somatic stem cells of planarians. Dev Biol 206:73–87.  https://doi.org/10.1006/dbio.1998.9130 CrossRefPubMedGoogle Scholar
  111. Shikina S, Chung Y-J, Wang H-M et al (2015) Localization of early germ cells in a stony coral, Euphyllia ancora: potential implications for a germline stem cell system in coral gametogenesis. Coral Reefs 34:639–653.  https://doi.org/10.1007/s00338-015-1270-6 CrossRefGoogle Scholar
  112. Shinzato C, Iguchi A, Hayward DC et al (2008) Sox genes in the coral Acropora millepora: divergent expression patterns reflect differences in developmental mechanisms within the Anthozoa. BMC Evol Biol 8:311.  https://doi.org/10.1186/1471-2148-8-311 CrossRefPubMedPubMedCentralGoogle Scholar
  113. Siddall ME, Martin DS, Bridge D et al (1995) The demise of a phylum of protists: phylogeny of Myxozoa and other parasitic cnidaria. J Parasitol 81:961–967CrossRefPubMedGoogle Scholar
  114. Sinclair WK (1965) Hydroxyurea: differential lethal effects on cultured mammalian cells during the cell cycle. Science 150:1729–1731CrossRefPubMedGoogle Scholar
  115. Siomi MC, Sato K, Pezic D, Aravin AA (2011) PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 12:246–258.  https://doi.org/10.1038/nrm3089 CrossRefPubMedGoogle Scholar
  116. Smid I, Tardent P (1986) The potentialities of endoderm interstitial cells in Hydra attenuata Pall. Dev Biol 117:672–675.  https://doi.org/10.1016/0012-1606(86)90336-2 CrossRefGoogle Scholar
  117. Solana J (2013) Closing the circle of germline and stem cells: the primordial stem cell hypothesis. EvoDevo 4:2.  https://doi.org/10.1186/2041-9139-4-2 CrossRefPubMedPubMedCentralGoogle Scholar
  118. Solana J, Kao D, Mihaylova Y et al (2012) Defining the molecular profile of planarian pluripotent stem cells using a combinatorial RNA-seq, RNA interference and irradiation approach. Genome Biol 13:R19.  https://doi.org/10.1186/gb-2012-13-3-r19 CrossRefPubMedPubMedCentralGoogle Scholar
  119. Steele RE, David CN, Technau U (2011) A genomic view of 500 million years of cnidarian evolution. Trends Genet 27:7–13.  https://doi.org/10.1016/j.tig.2010.10.002 CrossRefPubMedGoogle Scholar
  120. Sugiyama T, Fujisawa T (1977) Genetic analysis of developmental mechanisms in Hydra I. Sexual reproduction of Hydra magnipapillata and isolation of mutants. Develop Growth Differ 19:187–200.  https://doi.org/10.1111/j.1440-169X.1977.00187.x CrossRefGoogle Scholar
  121. Sugiyama T, Fujisawa T (1978a) Genetic analysis of developmental mechanisms in Hydra. II. Isolation and characterization of an interstitial cell-deficient strain. J Cell Sci 29:35–52PubMedGoogle Scholar
  122. Sugiyama T, Fujisawa T (1978b) Genetic analysis of developmental mechanisms in Hydra. V. Cell lineage and development of chimera Hydra. J Cell Sci 32:215–232PubMedGoogle Scholar
  123. Sugiyama T, Sugimoto N (1985) Genetic analysis of developmental mechanics in Hydra: XI. Mechanism of sex reversal by heterosexual parabiosis. Dev Biol 110:413–421.  https://doi.org/10.1016/0012-1606(85)90100-9 CrossRefPubMedGoogle Scholar
  124. Takahashi T, Muneoka Y, Lohmann J et al‑ (1997) Systematic isolation of peptide signal molecules regulating development in Hydra: LWamide and PW families. PNAS 94:1241–1246CrossRefPubMedGoogle Scholar
  125. Tardent P (1966) Experimente zur Frage der Geschlechtsbestimmung bei Hydra attenuata (Pall.) Rev Suisse Zool 73:481–492CrossRefGoogle Scholar
  126. Tardent P (1968) Experiments about sex determination in Hydra attenuata Pall. Dev Biol 17:483–511.  https://doi.org/10.1016/0012-1606(68)90001-8 CrossRefGoogle Scholar
  127. Tardent P (1995) The cnidarian cnidocyte, a hightech cellular weaponry. BioEssays 17:351–362.  https://doi.org/10.1002/bies.950170411 CrossRefGoogle Scholar
  128. Technau U, Steele RE (2011) Evolutionary crossroads in developmental biology: Cnidaria. Development 138:1447–1458.  https://doi.org/10.1242/dev.048959 CrossRefPubMedPubMedCentralGoogle Scholar
  129. Technau U, Miller MA, Bridge D, Steele RE (2003) Arrested apoptosis of nurse cells during Hydra oogenesis and embryogenesis. Dev Biol 260:191–206.  https://doi.org/10.1016/S0012-1606(03)00241-0 CrossRefPubMedGoogle Scholar
  130. Teragawa CK, Bode HR (1995) Migrating interstitial cells differentiate into neurons in hydra. Dev Biol 171:286–293.  https://doi.org/10.1006/dbio.1995.1281 CrossRefPubMedGoogle Scholar
  131. Torras R, Yanze N, Schmid V, González-Crespo S (2004) nanos expression at the embryonic posterior pole and the medusa phase in the hydrozoan Podocoryne carnea. Evol Dev 6:362–371.  https://doi.org/10.1111/j.1525-142X.2004.04044.x CrossRefPubMedGoogle Scholar
  132. van Wolfswinkel JC, Wagner DE, Reddien PW (2014) Single-cell analysis reveals functionally distinct classes within the planarian stem cell compartment. Cell Stem Cell 15:326–339.  https://doi.org/10.1016/j.stem.2014.06.007 CrossRefPubMedPubMedCentralGoogle Scholar
  133. Voronina E, Seydoux G, Sassone-Corsi P, Nagamori I (2011) RNA granules in germ cells. Cold Spring Harb Perspect Biol.  https://doi.org/10.1101/cshperspect.a002774
  134. Wagner DE, Wang IE, Reddien PW (2011) Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332:811–816.  https://doi.org/10.1126/science.1203983 CrossRefPubMedPubMedCentralGoogle Scholar
  135. Wanek N, Marcum BA, Campbell RD (1980) Histological structure of epithelial Hydra and evidence for the complete absence of interstitial and nerve cells. J Exp Zool 212:1–11.  https://doi.org/10.1002/jez.1402120102 CrossRefGoogle Scholar
  136. Wolenski FS, Bradham CA, Finnerty JR, Gilmore TD (2013) NF-κB is required for cnidocyte development in the sea anemone Nematostella vectensis. Dev Biol 373:205–215.  https://doi.org/10.1016/j.ydbio.2012.10.004 CrossRefPubMedGoogle Scholar
  137. Woodland HR (2016) Chapter thirty-six – the birth of animal development: multicellularity and the germline. In: Wassarman PM (ed) Current topics in developmental biology. Academic Press, pp 609–630, https://www.sciencedirect.com/science/article/pii/S0070215315001180?via%3Dihub Google Scholar
  138. Yanze N, Gröger H, Müller P, Schmid V (1999) Reversible inactivation of cell-type-specific regulatory and structural genes in migrating isolated striated muscle cells of jellyfish. Dev Biol 213:194–201.  https://doi.org/10.1006/dbio.1999.9347 CrossRefPubMedGoogle Scholar
  139. Zhu SJ, Hallows SE, Currie KW et al (2015) A mex3 homolog is required for differentiation during planarian stem cell lineage development. eLife 4:e07025.  https://doi.org/10.7554/eLife.07025 CrossRefPubMedCentralGoogle Scholar
  140. Zihler J (1972) Zur Gametogenese und Befruchtungsbiologie von Hydra. W Roux’ Arch f Entwicklungsmechanik 169:239–267.  https://doi.org/10.1007/BF00582555 CrossRefGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Molecular Evolution & Genomics, Centre for Organismal Studies HeidelbergHeidelberg UniversityHeidelbergGermany
  2. 2.Life Science Center for Survival Dynamics, Tsukuba Advanced Research Alliance (TARA)University of TsukubaTsukubaJapan

Personalised recommendations