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. 2007 Jun 11;29(7):635–644. doi: 10.1002/bies.20599

Evolution of size and pattern in the social amoebas

Pauline Schaap 1
PMCID: PMC3045520  PMID: 17563079

Abstract

A fundamental goal of biology is to understand how novel phenotypes evolved through changes in existing genes. The Dictyostelia or social amoebas represent a simple form of multicellularity, where starving cells aggregate to build fruiting structures. This review summarizes efforts to provide a framework for investigating the genetic changes that generated novel morphologies in the Dictyostelia. The foundation is a recently constructed molecular phylogeny of the Dictyostelia, which was used to examine trends in the evolution of novel forms and in the divergence of genes that shape these forms. There is a major trend towards the formation of large unbranched fruiting bodies, which is correlated with the use of cyclic AMP (cAMP) as a secreted signal to coordinate cell aggregation. The role of cAMP in aggregation arose through co‐option of a pathway that originally acted to coordinate fruiting body formation. The genotypic changes that caused this innovation and the role of dynamic cAMP signaling in defining fruiting body size and pattern throughout social amoeba evolution are discussed. BioEssays 29:635–644, 2007. © 2007 Wiley Periodicals, Inc.

References

  • 1. Baldauf SL, Roger AJ, Wenk‐Siefert I, Doolittle WF. 2000. A kingdom‐level phylogeny of eukaryotes based on combined protein data. Science 290: 972–977. [DOI] [PubMed] [Google Scholar]
  • 2. Stephenson SL, Stempen H. 1994. Myxomycetes: A handbook of slime molds. Portland, Oregon: Timber Press. [Google Scholar]
  • 3. Raper KB. 1984. The Dictyostelids. Princeton, New Jersey: Princeton University Press. [Google Scholar]
  • 4. Spemann H, Mangold H. 1924. Über Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren. Wilhelm Roux Arch Entw Mech Org 100: 599–638. [Google Scholar]
  • 5. Raper KB. 1940. Pseudoplasmodium formation and organization in Dictyostelium discoideum . J Elisha Mitchell Scient Soc 56: 241–282. [Google Scholar]
  • 6. Devreotes P, Janetopoulos C. 2003. Eukaryotic chemotaxis: Distinctions between directional sensing and polarization. J Biol Chem 278: 20445–20448. [DOI] [PubMed] [Google Scholar]
  • 7. Bagorda A, Mihaylov VA, Parent CA. 2006. Chemotaxis: Moving forward and holding on to the past. Thromb Haemost 95: 12–21. [PubMed] [Google Scholar]
  • 8. Uetrecht AC, Bear JE. 2006. Coronins: The return of the crown. Trends Cell Biol 16: 421–426. [DOI] [PubMed] [Google Scholar]
  • 9. Gilbert SF. 2006. Developmental Biology. Sunderland, MA: Sinauer Associates. [Google Scholar]
  • 10. Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, et al. 2005. The genome of the social amoeba Dictyostelium discoideum . Nature 435: 43–57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11. Han Z, Firtel RA. 1998. The homeobox‐containing gene wariai regulates anterior‐posterior patterning and cell‐type homeostasis in Dictyostelium . Development 125: 313–325. [DOI] [PubMed] [Google Scholar]
  • 12. Saran S, Meima ME, Alvarez‐Curto E, Weening KE, Rozen DE, et al. 2002. Camp signaling in Dictyostelium—complexity of cAMP synthesis, degradation and detection. J Muscle Res Cell Mot 23: 793–802. [DOI] [PubMed] [Google Scholar]
  • 13. Anjard C, Loomis WF. 2005. Peptide signaling during terminal differentiation of Dictyostelium . Proc Natl Acad Sci USA 102: 7607–7611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14. Thompson CR, Kay RR. 2000. The role of DIF‐1 signaling in Dictyostelium development. Mol Cell 6: 1509–1514. [DOI] [PubMed] [Google Scholar]
  • 15. Abe Hiroshi, Uchiyama M, Tanaka Y, Saito H. 1976. Structure of discadenine, a spore germination inhibitor from the cellular slime mold. Tetrahedron Lett 17: 3807–3810. [Google Scholar]
  • 16. Lang BF, O'Kelly C, Nerad T, Gray MW, Burger G. 2002. The closest unicellular relatives of animals. Curr Biol 12: 1773–1778. [DOI] [PubMed] [Google Scholar]
  • 17. Lewis LA, McCourt RM. 2004. Green algae and the origin of land plants. Am J Bot 91: 1535–1556. [DOI] [PubMed] [Google Scholar]
  • 18. Baldauf SL. 2003. The deep roots of eukaryotes. Science 300: 1703–1706. [DOI] [PubMed] [Google Scholar]
  • 19. Carroll SB. 2005. Endless forms most beautiful. The new science of evo devo and the making of the animal kingdom. New York: Norton, W.W. & Company. [Google Scholar]
  • 20. Stern DL. 1998. A role of ultrabithorax in morphological differences between Drosophila species. Nature 396: 463–466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21. Wilkins AS. 2001. The evolution of developmental pathways. Sunderland, MA: Sinauer Associates Inc. [Google Scholar]
  • 22. Irish VF. 2003. The evolution of floral homeotic gene function. Bioessays 25: 637–646. [DOI] [PubMed] [Google Scholar]
  • 23. Hay A, Tsiantis M. 2006. The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta . Nat Genet 38: 942–947. [DOI] [PubMed] [Google Scholar]
  • 24. Schaap P, Winckler T, Nelson M, Alvarez‐Curto E, Elgie B, et al. 2006. Molecular phylogeny and evolution of morphology in the social amoebas. Science 314: 661–663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25. Alvarez‐Curto E, Rozen DE, Ritchie AV, Fouquet C, Baldauf SL, et al. 2005. Evolutionary origin of cAMP‐based chemoattraction in the social amoebae. Proc Natl Acad Sci USA 102: 6385–6390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26. Olive EG. 1902. Monograph of the Acrasieae. Proc Boston Soc Nat His 30: 451–513. [Google Scholar]
  • 27. Stechmann A, Cavalier‐Smith T. 2003. Phylogenetic analysis of eukaryotes using heat‐shock protein Hsp90. J Mol Evol 57: 408–419. [DOI] [PubMed] [Google Scholar]
  • 28. Richards TA, Cavalier‐Smith T. 2005. Myosin domain evolution and the primary divergence of eukaryotes. Nature 436: 1113–1118. [DOI] [PubMed] [Google Scholar]
  • 29. Swanson AR, Spiegel FW, Cavender JC. 2002. Taxonomy, slime molds, and the questions we ask. Mycologia 94: 968–979. [PubMed] [Google Scholar]
  • 30. Hagiwara H. 1989. The taxonomic study of Japanese Dictyostelid cellular slime molds. Tokyo: Nat Science Museum. [Google Scholar]
  • 31. Traub F, Hohl R. 1976. A new concept for the taxonomy of the family dictyosteliaceae (cellular slime molds). Amer J Bot 63: 664–672. [Google Scholar]
  • 32. Konijn TM, Van De Meene JG, Bonner JT, Barkley DS. 1967. The acrasin activity of adenosine‐3′,5′‐cyclic phosphate. Proc Natl Acad Sci USA 58: 1152–1154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33. Dormann D, Vasiev B, Weijer CJ. 2000. The control of chemotactic cell movement during Dictyostelium morphogenesis. Phil Trans R Soc Sci 355: 983–991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34. Wang M, Van Driel R, Schaap P. 1988. Cyclic AMP‐phosphodiesterase induces dedifferentiation of prespore cells in Dictyostelium discoideum slugs: Evidence that cyclic AMP is the morphogenetic signal for prespore differentiation. Development 103: 611–618. [Google Scholar]
  • 35. Alvarez‐Curto E, Saran S, Meima M, Schaap P. 2007. cAMP production by adenylyl cyclase G induces prespore differentiation in Dictyostelium slugs. Development 134: 959–966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36. Wang M, Schaap P. 1989. Ammonia depletion and DIF trigger stalk cell differentiation in intact Dictyostelium discoideum slugs. Development 105: 569–574. [Google Scholar]
  • 37. Hopper NA, Harwood AJ, Bouzid S, Véron M, Williams JG. 1993. Activation of the prespore and spore cell pathway of Dictyostelium differentiation by cAMP‐dependent protein kinase and evidence for its upstream regulation by ammonia. EMBO J 12: 2459–2466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38. Feit IN, Bonner JT, Suthers HB. 1990. Regulation of the anterior‐like cell state by ammonia in Dictyostelium discoideum . Dev Gen 11: 442–446. [DOI] [PubMed] [Google Scholar]
  • 39. Bonner JT, Chiang A, Lee J, Suthers HB. 1988. The possible role of ammonia in phototaxis of migrating slugs of Dictyostelium discoideum . Proc Natl Acad Sci USA 85: 3885–3887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40. Clarke M, Gomer RH. 1995. PSF and CMF, autocrine factors that regulate gene expression during growth and early development of Dictyostelium . Experientia 51: 1124–1134. [DOI] [PubMed] [Google Scholar]
  • 41. Kay RR, Taylor GW, Jermyn KA, Traynor D. 1992. Chlorine‐containing compounds produced during Dictyostelium development. Detection by labelling with Cl Biochem J 281: 155–161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42. Van Es S, Hodgkinson S, Schaap P, Kay RR. 1994. Metabolic pathways for differentiation‐inducing factor‐1 and their regulation are conserved between closely related Dictyostelium species, but not between distant members of the family. Differentiation 58: 95–100. [DOI] [PubMed] [Google Scholar]
  • 43. Schaap P, Konijn TM, Van Haastert PJM. 1984. cAMP pulses coordinate morphogenetic movement during fruiting body formation of Dictyostelium minutum . Proc Natl Acad Sci USA 81: 2122–2126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44. Schaap P, Wang M. 1984. The possible involvement of oscillatory cAMP signaling in multicellular morphogenesis of the cellular slime molds. Dev Biol 105: 470–478. [DOI] [PubMed] [Google Scholar]
  • 45. Schaap P. 1985. cAMP relay during early culmination of Dictyostelium minutum . Differentiation 28: 205–208. [DOI] [PubMed] [Google Scholar]
  • 46. Kim J‐Y, Van Haastert P, Devreotes PN. 1996. Social senses: G‐protein‐coupled receptor signaling pathways in Dictyostelium discoideum . Chem and Biol 3: 239–243. [DOI] [PubMed] [Google Scholar]
  • 47. Louis JM, Saxe CL III, Kimmel AR. 1993. Two transmembrane signaling mechanisms control expression of the cAMP receptor gene cAR1 during Dictyostelium development. Proc Natl Acad Sci USA 90: 5969–5973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48. Faure M, Franke J, Hall AL, Podgorski GJ, Kessin RH. 1990. The cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum contains three promoters specific for growth, aggregation, and late development. Mol Cell Biol 10: 1921–1930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49. Leyser O. 2005. The fall and rise of apical dominance. Curr Opin Genet Dev 15: 468–471. [DOI] [PubMed] [Google Scholar]
  • 50. Lee KJ, Goldstein RE, Cox EC. 2002. cAMP waves in Dictyostelium territories. Nonlinearity 15: C1–C5. [Google Scholar]
  • 51. Kopachik WJ. 1982. Size regulation in Dictyostelium . J Embryol Exp Morph 68: 23–35. [PubMed] [Google Scholar]
  • 52. Newell PC, Ross FM. 1982. Inhibition by adenosine of aggregation centre initiation and cyclic AMP binding in Dictyostelium . J Gen Microbiol 128: 2715–2724. [Google Scholar]
  • 53. Schaap P, Wang M. 1986. Interactions between adenosine and oscillatory cAMP signaling regulate size and pattern in Dictyostelium . Cell 45: 137–144. [DOI] [PubMed] [Google Scholar]
  • 54. Martiel J‐L, Goldbeter A. 1987. A model based on receptor desensitization for cyclic AMP signaling in Dictyostelium cells. Biophys J 52: 807–828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55. Kriebel PW, Parent CA. 2004. Adenylyl cyclase expression and regulation during the differentiation of Dictyostelium discoideum . IUBMB Life 56: 541–546. [DOI] [PubMed] [Google Scholar]
  • 56. Laub MT, Loomis WF. 1998. A molecular network that produces spontaneous oscillations in excitable cells of Dictyostelium . Mol Biol Cell 9: 3521–3532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57. Hagiwara H. 2003. Dictyostelids in Japan. XII. Dictyostelium gloeosporum, a new species from the grounds of the Imperial palace, Tokyo. Bull Natn Sci Mus Tokyo 29: 127–132. [Google Scholar]
  • 58. Bonner JT, Chiquoine AD, Kolderie MQ. 1955. A histochemical study of differentiation in the cellular slime molds. J Exp Zool 130: 133–157. [Google Scholar]
  • 59. Schaap P, Pinas JE, Wang M. 1985. Patterns of cell differentiation in several cellular slime mold species. Dev Biol 111: 51–61. [Google Scholar]

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