Advertisement

Reproductive Strategies in Social Amoeba

Chapter
  • 1.1k Downloads
Part of the Diversity and Commonality in Animals book series (DCA)

Abstract

The social amoebozoans live solitarily in the soil and have a unique life history, involving three resistant stages: asexual multicellular development to form fruits with spores supported on a stalk, sexual multicellular development to generate macrocysts, and unicellular formation of a microcyst. Depending on the environmental cues, the social amoeba adopts one of the reproductive modes in order to survive under unfavorable conditions. The model organism, Dictyostelium discoideum, is the most widely studied social amoeba and has three mating types. Macrocysts are the sexual version of spores, and contain recombinant offspring derived from gamete fusion of two mating types followed by meiosis. The mating-type locus was recently identified; single mat genes determine two mating types, and the third type is specified by composite mat homologs. In addition to the heterothallic sexual pathway, some other species, as well as a few known wild-type isolates of D. discoideum, exhibit self-fertile, homothallic behavior. Volatile sex pheromones, including the gaseous plant hormone, ethylene, are known to influence macrocyst production. Thus, the sexual pathway of the social amoeba is interesting, and studies on dictyostelids will provide evolutionary insights into reproductive strategies adapted by simple multicellular organisms. In this chapter, after introducing the unique features of the social amoeba, their sexual development leading to macrocyst formation and the known molecular mechanisms that regulate this process are reviewed.

Keywords

Dictyostelium Social amoeba Gametes Zygote Macrocyst Cell fusion Chemotaxis Cyclic AMP Sexual pheromones 

Notes

Acknowledgement

MF wishes to thank Satoshi Kuwana, Akifumi Maruyama and Shuya Moriai for images. This work is partly supported by JSPS Grant-in-Aid for Scientific Research (KAKENHI) number 24657160.

References

  1. Abe K, Orii H, Okada Y, Saga Y, Yanagisawa K (1984) A novel cyclic AMP metabolism exhibited by giant cells and its possible role in the sexual development of Dictyostelium discoideum. Dev Biol 104:477–483PubMedCrossRefGoogle Scholar
  2. Amagai A (1984) Induction by ethylene of macrocyst formation in the cellular slime mould Dictyostelium mucoroides. J Gen Microbiol 130:2961–2965Google Scholar
  3. Amagai A (1989) Induction of zygote formation by ethylene during the sexual development of the cellular slime mold Dictyostelium discoideum. Differentiation 41:176–183CrossRefGoogle Scholar
  4. Amagai A (1992) Induction of heterothallic and homothallic zygotes in Dictyostelium discoideum by ethylene. Develop Growth Differ 34:293–300CrossRefGoogle Scholar
  5. Amagai A (2002) Involvement of a novel gene, zyg1, in zygote formation of Dictyostelium mucoroides. J Muscle Res Cell Motil 23:867–874PubMedCrossRefGoogle Scholar
  6. Amagai A (2011) Ethylene as a potent inducer of sexual development. Develop Growth Differ 53:617–623CrossRefGoogle Scholar
  7. Amagai A (2012) Regulatory mechanism in sexual and asexual cycles of Dictyostelium. Adv Sel Plant Physiol Asp 15:327–344Google Scholar
  8. Amagai A, Soramoto SS, Saito SH, Maeda Y (2007) Ethylene induces zygote formation through an enhanced expression of zyg1 in Dictyostelium mucoroides. Exp Cell Res 313:2493–2503PubMedCrossRefGoogle Scholar
  9. Amagai A et al (2012) PKC-mediated ZYG1 phosphorylation induces fusion of myoblasts as well as of Dictyostelium cells. Int J Cell Biol 2012:657423PubMedPubMedCentralCrossRefGoogle Scholar
  10. Amagai A, Takahashi F, Usui T, Abe T, Maeda Y (2014) Induction of macrocyst wall formation by ZYG1 in Dictyostelium discoideum. Res J Dev Biol 1:1–7CrossRefGoogle Scholar
  11. Anderson DK (1986) Macrocysts in Dictyostelium lacteum. MS Thesis, Ohio University, Athens, OHGoogle Scholar
  12. Anjard C, Loomis WF (2008) Cytokinins induce sporulation in Dictyostelium. Development 135:819–827PubMedCrossRefGoogle Scholar
  13. Araki Y et al (2012) A surface glycoprotein indispensable for gamete fusion in the social amoeba Dictyostelium discoideum. Eukaryot Cell 11:638–644PubMedPubMedCentralCrossRefGoogle Scholar
  14. Basu S et al (2013) DictyBase 2013: integrating multiple Dictyostelid species. Nucleic Acids Res 41:D676–D683PubMedCrossRefGoogle Scholar
  15. Benabentos R et al (2009) Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium. Curr Biol 19:567–572PubMedPubMedCentralCrossRefGoogle Scholar
  16. Blanton RL, Fuller D, Iranfar N, Grimson MJ, Loomis WF (2000) The cellulose synthase gene of Dictyostelium. Proc Natl Acad Sci U S A 97:2391–2396PubMedPubMedCentralCrossRefGoogle Scholar
  17. Blaskovics JC, Raper KB (1957) Encystment stages of Dictyostelium. Biol Bull 113:58–88CrossRefGoogle Scholar
  18. Bloomfield G (2011) Genetics of sex determination in the social amoebae. Develop Growth Differ 53:608–616CrossRefGoogle Scholar
  19. Bloomfield G, Tanaka Y, Skelton J, Ivens A, Kay RR (2008) Widespread duplications in the genomes of laboratory stocks of Dictyostelium discoideum. Genome Biol 9:R75PubMedPubMedCentralCrossRefGoogle Scholar
  20. Bloomfield G, Skelton J, Ivens A, Tanaka Y, Kay RR (2010) Sex determination in the social amoeba Dictyostelium discoideum. Science 330:1533–1536PubMedPubMedCentralCrossRefGoogle Scholar
  21. Bonner JT, Dodd MR (1962) Aggregation territories in the cellular slime molds. Biol Bull 122:13–24CrossRefGoogle Scholar
  22. Brefeld O (1869) Dictyostelium mucoroides. Ein neuer Organismus aus der Verwandtschaft der Myxomyceten. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft Frankfurt 7:85–107Google Scholar
  23. Cavender JC, Kawabe K (1989) Cellular slime molds of Japan. I. Distribution and biogeographical considerations. Mycologia 81:683–691CrossRefGoogle Scholar
  24. Cervantes MD et al (2013) Selecting one of several mating types through gene segment joining and deletion in Tetrahymena thermophila. PLoS Biol 11:e1001518PubMedPubMedCentralCrossRefGoogle Scholar
  25. Chang MT, Raper KB (1981) Mating types and macrocyst formation in Dictyostelium. J Bacteriol 147:1049–1053PubMedPubMedCentralGoogle Scholar
  26. Clark MA, Francis D, Eisenberg R (1973) Mating types in cellular slime molds. Biochem Biophys Res Commun 52:672–678PubMedCrossRefGoogle Scholar
  27. Eichinger L et al (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435:43–57PubMedPubMedCentralCrossRefGoogle Scholar
  28. Erdos GW, Nickerson AW, Raper KB (1972) The fine structure of macrocysts in Polysphondylium violaceum. Cytobiologie 6:351–366Google Scholar
  29. Erdos GW, Raper KB, Vogen LK (1973) Mating types and macrocyst formation in Dictyostelium discoideum. Proc Natl Acad Sci U S A 70:1828–1830PubMedPubMedCentralCrossRefGoogle Scholar
  30. Erdos GW, Raper KB, Vogen LK (1975) Sexuality in the cellular slime mold Dictyostelium giganteum. Proc Natl Acad Sci U S A 72:970–973PubMedPubMedCentralCrossRefGoogle Scholar
  31. Fang H, Aiba K, Higa M, Urushihara H, Yanagisawa K (1993) Antisense RNA inactivation of gp138 gene expression results in repression of sexual cell fusion in Dictyostelium discoideum. J Cell Sci 106(Pt 3):785–788PubMedGoogle Scholar
  32. Ferris PJ, Armbrust EV, Goodenough UW (2002) Genetic structure of the mating-type locus of Chlamydomonas reinhardtii. Genetics 160:181–200PubMedPubMedCentralGoogle Scholar
  33. Fey P et al (2009) dictyBase – a Dictyostelium bioinformatics resource update. Nucleic Acids Res 37:D515–D519PubMedCrossRefGoogle Scholar
  34. Filosa MF, Dengler RE (1972) Ultrastructure of macrocyst formation in the cellular slime mold, Dictyostelium mucoroides: extensive phagocytosis of amoebae by a specialized cell. Dev Biol 29:1–16PubMedCrossRefGoogle Scholar
  35. Flowers JM et al (2010) Variation, sex, and social cooperation: molecular population genetics of the social amoeba Dictyostelium discoideum. PLoS Genet 6:e1001013PubMedPubMedCentralCrossRefGoogle Scholar
  36. Fukuzawa M, Zhukovskaya NV, Yamada Y, Araki T, Williams JG (2006) Regulation of Dictyostelium prestalk-specific gene expression by a SHAQKY family MYB transcription factor. Development 133:1715–1724PubMedCrossRefGoogle Scholar
  37. Funamoto S, Meili R, Lee S, Parry L, Firtel RA (2002) Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell 109:611–623PubMedCrossRefGoogle Scholar
  38. Hagiwara H, Kawakami S, Hwang JY (2004) Mating system and morphology of the temperate form of Dictyostelium purpureum Olive. Bull Natl Sci Mus Tokyo, Ser B 30:71–78Google Scholar
  39. Hagiwara H, Kawakami S, Hwang JY, Li Y (2005) A mating group newly found in the subtropical form of Ddictyostelium purpureum Olive. Bull Natl Sci Mus Tokyo, Ser B 31:5–9Google Scholar
  40. Hata T, Takahashi M, Tanaka Y, Urushihara H (2001) Total tetra knockout of GP138 multigene family implicated in cell interactions in Dictyostelium discoideum. Gene 271:33–42PubMedCrossRefGoogle Scholar
  41. Heidel AJ et al (2011) Phylogeny-wide analysis of social amoeba genomes highlights ancient origins for complex intercellular communication. Genome Res 21:1882–1891PubMedPubMedCentralCrossRefGoogle Scholar
  42. Hirai M et al (2008) Male fertility of malaria parasites is determined by GCS1, a plant-type reproduction factor. Curr Biol 18:607–613PubMedCrossRefGoogle Scholar
  43. Hirose S, Benabentos R, Ho HI, Kuspa A, Shaulsky G (2011) Self-recognition in social amoebae is mediated by allelic pairs of tiger genes. Science 333:467–470PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hohl HR, Miura-Santo LY, Cotter DA (1970) Ultrastructural changes during formation and germination of microcysts in Polysphondylium pallidum, a cellular slime mould. J Cell Sci 7:285–305PubMedGoogle Scholar
  45. Hurst LD (1996) Why are there only two sexes? Proc R Soc B Biol Sci 263:415–422CrossRefGoogle Scholar
  46. Hurst LD, Hamilton WD (1992) Cytoplasmic fusion and the nature of sexes. P Roy Soc B-Biol Sci 247:189–194CrossRefGoogle Scholar
  47. Iijima M, Devreotes P (2002) Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell 109:599–610PubMedCrossRefGoogle Scholar
  48. Ikawa M, Inoue N, Okabe M (2008) Mechanisms of sperm-egg interactions emerging from gene-manipulated animals. Int J Dev Biol 52:657–664PubMedCrossRefGoogle Scholar
  49. Inoue N, Ikawa M, Isotani A, Okabe M (2005) The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 434:234–238CrossRefPubMedGoogle Scholar
  50. Ishida K, Hata T, Urushihara H (2005) Gamete fusion and cytokinesis preceding zygote establishment in the sexual process of Dictyostelium discoideum. Dev Growth Differ 47:25–35PubMedCrossRefGoogle Scholar
  51. Ishikawa T, Urushihara H, Yanagisawa K (1991) Involvement of cell surface carbohydrates in the sexual cell fusion of Dictyostelium discoideum. Dev Growth Differ 33:131–138CrossRefGoogle Scholar
  52. Johnson PR, Ecker JR (1998) The ethylene gas signal transduction pathway: a molecular perspective. Annu Rev Genet 32:227–254PubMedCrossRefGoogle Scholar
  53. Kawabe Y et al (2009) Activated cAMP receptors switch encystation into sporulation. Proc Natl Acad Sci U S A 106:7089–7094PubMedPubMedCentralCrossRefGoogle Scholar
  54. Kawakami S, Hagiwara H (2008) A taxonomic revision of two dictyostelid species, Polysphondylium pallidum and P. album. Mycologia 100:111–121PubMedCrossRefGoogle Scholar
  55. Kessin RH (2001) Dictyostelium – evolution, cell biology, and the development of multicellularity. Cambridge Univ. Press, Cambridge, p xiv + 294CrossRefGoogle Scholar
  56. Lamphier MS, Yanagisawa K (1983) Induction of macrocyst formation by factors secreted by giant cells in Dictyostelium discoideum. Dev Growth Differ 25:495–501CrossRefGoogle Scholar
  57. Langenick J, Araki T, Yamada Y, Williams JG (2008) A Dictyostelium homologue of the metazoan Cbl proteins regulates STAT signalling. J Cell Sci 121:3524–3530PubMedCrossRefGoogle Scholar
  58. Le Naour F, Rubinstein E, Jasmin C, Prenant M, Boucheix C (2000) Severely reduced female fertility in CD9-deficient mice. Science 287:319–321CrossRefPubMedGoogle Scholar
  59. Lewis KE, O’Day DH (1976) Sexual hormone in the cellular slime mould Dictyostelium purpureum. Can J Microbiol 22:1269–1273PubMedCrossRefGoogle Scholar
  60. Lewis KE, O’Day DH (1977) Sex hormone of Dictyostelium discoideum is volatile. Nature 268:730–731CrossRefGoogle Scholar
  61. Lewis KE, O’Day DH (1979) Evidence for a hierarchical mating system operating via pheromones in Dictyostelium giganteum. J Bacteriol 138:251–253PubMedPubMedCentralGoogle Scholar
  62. Lewis KE, O’Day DH (1985) The regulation of sexual development in Dictyostelium discoideum: cannibalistic behaviour of the giant cell. Can J Microbiol 31:423–428CrossRefGoogle Scholar
  63. Lewis KE, O’Day DH (1986) Phagocytic specificity during sexual development in Dictyostelium discoideum. Can J Microbiol 32:79–82PubMedCrossRefGoogle Scholar
  64. Loomis WF (2014) Cell signaling during development of Dictyostelium. Dev Biol 391:1–16PubMedPubMedCentralCrossRefGoogle Scholar
  65. Lydan MA, O’Day DH (1988a) Different developmental functions for calmodulin in Dictyostelium: trifluoperazine and R24571 both inhibit cell and pronuclear fusion but enhance gamete formation. Exp Cell Res 178:51–63PubMedCrossRefGoogle Scholar
  66. Lydan M, O’Day DH (1988b) The role of intracellular Ca2+ during early sexual development in Dictyostelium discoideum: effects of LaCl3, Ins(1,4,5)P3, TMB-8, chlortetracycline and A23187 on cell fusion. J Cell Sci 90:465–473Google Scholar
  67. Lydan MA, O’Day DH (1988c) Developmental effects of the major ions found in a groundwater sample on sexual cultures of Dictyostelium discoideum. Can J Microbiol 34:207–211CrossRefGoogle Scholar
  68. Macinnes MA, Francis D (1974) Meiosis in Dictyostelium mucoroides. Nature 251:321–324PubMedCrossRefGoogle Scholar
  69. McConachie DR, O’Day DH (1986) The immediate induction of extensive cell fusion by Ca2+ addition in Dictyostelium discoideum. Biochem Cell Biol 64:1281–1287PubMedCrossRefGoogle Scholar
  70. McConachie DR, O’Day DH (1987) Pronuclear migration, swelling, and fusion during sexual development in Dictyostelium discoideum. Can J Microbiol 33:1046–1049CrossRefGoogle Scholar
  71. Mehdiabadi NJ, Kronforst MR, Queller DC, Strassmann JE (2009) Phylogeny, reproductive isolation and kin recognition in the social amoeba Dictyostelium purpureum. Evolution 63:542–548PubMedPubMedCentralCrossRefGoogle Scholar
  72. Mehdiabadi NJ, Kronforst MR, Queller DC, Strassmann JE (2010) Phylogeography and sexual macrocyst formation in the social amoeba Dictyostelium giganteum. BMC Evol Biol 10:17PubMedPubMedCentralCrossRefGoogle Scholar
  73. Miyado K et al (2000) Requirement of CD9 on the egg plasma membrane for fertilization. Science 287:321–324CrossRefPubMedGoogle Scholar
  74. Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T (2006) GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat Cell Biol 8:64–71CrossRefPubMedGoogle Scholar
  75. Morris PS, Lewis KE, O’Day DH (1982) Sexual pheromone accumulation and response in agar plate and liquid cultures of Dictyostelium discoideum. Can J Microbiol 28:1273–1276CrossRefGoogle Scholar
  76. Muramoto T et al (2003) Construction of a gamete-enriched gene pool and RNAi-mediated functional analysis in Dictyostelium discoideum. Mech Dev 120:965–975PubMedCrossRefGoogle Scholar
  77. Muramoto T, Takeda S, Furuya Y, Urushihara H (2005) Reverse genetic analyses of gamete-enriched genes revealed a novel regulator of the cAMP signaling pathway in Dictyostelium discoideum. Mech Dev 122:733–743PubMedCrossRefGoogle Scholar
  78. Nickerson AW, Raper KB (1973) Macrocysts in the life cycle of the Dictyosteliaceae. II. Germination of the macrocysts. Am J Bot 60:247–254CrossRefGoogle Scholar
  79. O’Day DH, Durston AJ (1979) Evidence for chemotaxis during sexual development in Dictyostelium discoideum. Can J Microbiol 25:542–544PubMedCrossRefGoogle Scholar
  80. O’Day DH, Keszei A (2012) Signalling and sex in the social amoebozoans. Biol Rev Camb Philos Soc 87:313–329PubMedCrossRefGoogle Scholar
  81. O’Day DH, Lewis KE (1975) Diffusible mating-type factors induce macrocyst development in Dictyostelium discoideum. Nature 254:431–432PubMedCrossRefGoogle Scholar
  82. O’Day DH, Lewis KE (1981) In: O’Day DH, Horgen PA (eds) Sexual interactions in eukaryotic microbes. Academic Press, New York, pp 199–224Google Scholar
  83. O’Day DH, Rivera J (1987) Lectin binding and inhibition studies reveal the importance of D-glucose, D-mannose and N-acetylglucosamine during early sexual development of Dictyostelium discoideum. Cell Differ 20:231–237PubMedCrossRefGoogle Scholar
  84. O’Day DH, McConachie DR, Rivera J (1987) Appearance and developmental kinetics of a unique cell type in Dictyostelium discoideum: is it the gamete of sexual development? J Exp Zoool 242:153–159CrossRefGoogle Scholar
  85. O'Day DH (1979) Aggregation during sexual development in Dictyostelium discoideum. Can J Microbiol 25:1416–1426PubMedCrossRefGoogle Scholar
  86. Okada H, Hirota Y, Moriyama R, Saga Y, Yanagisawa K (1986) Nuclear fusion in multinucleated giant cells during the sexual development of Dictyostelium discoideum. Dev Biol 118:95–102CrossRefGoogle Scholar
  87. Raper KB (1935) Dictyostelium discoideum, a new species of slime mold from decaying forest leaves. J Agric Res 50:135–147Google Scholar
  88. Raper KB, Thom C (1941) Interspecific mixtures in the Dictyosteliaceae. Am J Bot 28:69–78CrossRefGoogle Scholar
  89. Raudaskoski M, Kothe E (2010) Basidiomycete mating type genes and pheromone signaling. Eukaryot Cell 9:847–859PubMedPubMedCentralCrossRefGoogle Scholar
  90. Robson GE, Williams KL (1979) Vegetative incompatibility and the mating-type locus in the cellular slime mold Dictyostelium discoideum. Genetics 93:861–875PubMedPubMedCentralGoogle Scholar
  91. Robson GE, Williams KL (1980) The mating system of the cellular slime mould Dictyostelium discoideum. Curr Genet 1:229–232PubMedCrossRefGoogle Scholar
  92. Saga Y, Yanagisawa K (1982) Macrocyst development in Dictyostelium discoideum. I. Induction of synchronous development by giant cells and biochemical analysis. J Cell Sci 55:341–352PubMedGoogle Scholar
  93. Shimizu H, Morio T, Shimizu HD, Urushihara H (1997) A mutation in the cAMP signaling pathway affects sexual development of Dictyostelium discoideum. Dev Growth Differ 39:227–234PubMedCrossRefGoogle Scholar
  94. Singleton CK, Xiong Y (2013) Loss of the histidine kinase DhkD results in mobile mounds during development of Dictyostelium discoideum. PLoS One 8:e75618PubMedPubMedCentralCrossRefGoogle Scholar
  95. Suzuki K, Yanagisawa K (1989) Environmental factors inducing sexual development in Dictyostelium discoideum. Bot Mag Tokyo 102:53–61CrossRefGoogle Scholar
  96. Szabo SP, O’Day DH, Chagla AH (1982) Cell fusion, nuclear fusion, and zygote differentiation during sexual development of Dictyostelium discoideum. Dev Biol 90:375–382PubMedCrossRefGoogle Scholar
  97. Thompson CR, Reichelt S, Kay RR (2004) A demonstration of pattern formation without positional information in Dictyostelium. Dev Growth Differ 46:363–369PubMedCrossRefGoogle Scholar
  98. Urushihara H (1992) Review – sexual development of cellular slime mold. Dev Growth Differ 34:1–8CrossRefGoogle Scholar
  99. Urushihara H, Muramoto T (2006) Genes involved in Dictyostelium discoideum sexual reproduction. Eur J Cell Biol 85:961–968PubMedCrossRefGoogle Scholar
  100. Urushihara H, Habata Y, Yanagisawa K (1988) A membrane protein with possible relevance to sexual cell fusion in Dictyostelium discoideum. Cell Differ Dev 25:81–87PubMedCrossRefGoogle Scholar
  101. Urushihara H et al (2015) Comparative genome and transcriptome analyses of the social amoeba Acytostelium subglobosum that accomplishes multicellular development without germ-soma differentiation. BMC Genomics 16:80PubMedPubMedCentralCrossRefGoogle Scholar
  102. von Besser K, Frank AC, Johnson MA, Preuss D (2006) Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development 133:4761–4769CrossRefGoogle Scholar
  103. Wallace MA, Raper KB (1979) Genetic exchanges in the macrocysts of Dictyostelium discoideum. J Gen Microbiol 113:327–337PubMedCrossRefGoogle Scholar
  104. Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14(Suppl):S131–S151PubMedPubMedCentralCrossRefGoogle Scholar
  105. Williams JG (2003) In: Sehgal PB, Levy DE, Hirano T (eds) Signal Transducers and Activators of Transcription (STATs). Activation and biology. Kluwer Academic Publishers, Boston, pp 105–121CrossRefGoogle Scholar
  106. Williams JG (2010) Dictyostelium finds new roles to model. Genetics 185:717–726PubMedPubMedCentralCrossRefGoogle Scholar
  107. Williams JG et al (1989) Origins of the prestalk-prespore pattern in Dictyostelium development. Cell 59:1157–1163PubMedCrossRefGoogle Scholar
  108. Wong JL, Johnson MA (2010) Is HAP2-GCS1 an ancestral gamete fusogen? Trends Cell Biol 20:134–141PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biology, Faculty of Agriculture and Life ScienceHirosaki UniversityAomoriJapan

Personalised recommendations