Abstract
Dictyostelid social amoebas represent one of several groups of genetically divergent lineages that display aggregative multicellularity. In this chapter, we describe the evolution of developmental complexity in Dictyostelia and discuss the signalling mechanisms that control the developmental programme of the model organism Dictyostelium discoideum. We also reconstruct the evolutionary history of these developmental control mechanisms from environmental sensing in the unicellular ancestors of Dictyostelia. Finally, we explore the parameters that define the boundary between uni- and multicellularity.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Abe H, Hashimoto K, Uchiyama M (1981) Discadenine distribution in cellular slime molds and its inhibitory activity on spore germination. Agric Biol Chem 45:1295–1296
Alvarez-Curto E, Rozen DE, Ritchie AV, Fouquet C, Baldauf SL, Schaap P (2005) Evolutionary origin of cAMP-based chemoattraction in the social amoebae. Proc Natl Acad Sci U S A 102(18):6385–6390
Alvarez-Curto E, Saran S, Meima M, Zobel J, Scott C, Schaap P (2007) cAMP production by adenylyl cyclase G induces prespore differentiation in Dictyostelium slugs. Development 134(5):959–966
Anjard C, Loomis WF (2006) GABA induces terminal differentiation of Dictyostelium through a GABA(B) receptor. Development 133(11):2253–2261
Anjard C, Loomis WF (2008) Cytokinins induce sporulation in Dictyostelium. Development 135:819–827
Anjard C, Su Y, Loomis WF (2009) Steroids initiate a signaling cascade that triggers rapid sporulation in Dictyostelium. Development 136(5):803–812. doi:10.1242/dev.032607 [doi] (dev.032607 [pii])
Asghar A, Groth M, Siol O, Gaube F, Enzensperger C, Glockner G, Winckler T (2011) Developmental gene regulation by an ancient intercellular communication system in social amoebae. Protist 163:25–37. doi:10.1016/j.protis.2010.12.002 (S1434-4610(11)00005-8 [pii])
Benabentos R, Hirose S, Sucgang R, Curk T, Katoh M, Ostrowski EA, Strassmann JE, Queller DC, Zupan B, Shaulsky G, Kuspa A (2009) Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium. Curr Biol 19(7):567–572. doi:10.1016/j.cub.2009.02.037 [doi] (S0960-9822(09)00747-7 [pii])
Brown MW, Spiegel FW, Silberman JD (2009) Phylogeny of the “forgotten” cellular slime mold, Fonticula alba, reveals a key evolutionary branch within Opisthokonta. Mol Biol Evol. doi:10.1093/molbev/msp185 [doi] (msp185 [pii] )
Brown MW, Silberman JD, Spiegel FW (2012) A contemporary evaluation of the acrasids (Acrasidae, Heterolobosea, Excavata). Eur J Protistol. doi:10.1016/j.ejop.2011.10.001 (S0932-4739(11)00075-7 [pii])
Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, Disbennett K, Pfannkoch C, Sumin N, Sutton GG, Viswanathan LD, Walenz B, Goodstein DM, Hellsten U, Kawashima T, Prochnik SE, Putnam NH, Shu S, Blumberg B, Dana CE, Gee L, Kibler DF, Law L, Lindgens D, Martinez DE, Peng J, Wigge PA, Bertulat B, Guder C, Nakamura Y, Ozbek S, Watanabe H, Khalturin K, Hemmrich G, Franke A, Augustin R, Fraune S, Hayakawa E, Hayakawa S, Hirose M, Hwang JS, Ikeo K, Nishimiya-Fujisawa C, Ogura A, Takahashi T, Steinmetz PR, Zhang X, Aufschnaiter R, Eder MK, Gorny AK, Salvenmoser W, Heimberg AM, Wheeler BM, Peterson KJ, Bottger A, Tischler P, Wolf A, Gojobori T, Remington KA, Strausberg RL, Venter JC, Technau U, Hobmayer B, Bosch TC, Holstein TW, Fujisawa T, Bode HR, David CN, Rokhsar DS, Steele RE (2010) The dynamic genome of Hydra. Nature 464(7288):592–596. doi:10.1038/nature08830
Chen ZH, Schaap P (2012) The prokaryote messenger c-di-GMP triggers stalk cell differentiation in Dictyostelium. Nature 488:680–683. doi:10.1038/nature11313
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
Clarke M, Lohan AJ, Liu B, Lagkouvardos I, Roy S, Zafar N, Bertelli C, Schilde C, Kianianmomeni A, Burglin TR, Frech C, Turcotte B, Kopec KO, Synnott JM, Choo C, Paponov I, Finkler A, Soon Heng Tan C, Hutchins AP, Weinmeier T, Rattei T, Chu JS, Gimenez G, Irimia M, Rigden DJ, Fitzpatrick DA, Lorenzo-Morales J, Bateman A, Chiu CH, Tang P, Hegemann P, Fromm H, Raoult D, Greub G, Miranda-Saavedra D, Chen N, Nash P, Ginger ML, Horn M, Schaap P, Caler L, Loftus B (2013) Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling. Genome Biol 14(2):R11. doi:10.1186/gb-2013-14-2-r11
Cotter DA (1977) The effects of osmotic pressure changes on the germination of Dictyostelium discoideum spores. Can J Microbiol 23(9):1170–1177
Cotter DA, Dunbar AJ, Buconjic SD, Wheldrake JF (1999) Ammonium phosphate in sori of Dictyostelium discoideum promotes spore dormancy through stimulation of the osmosensor ACG. Microbiology-Uk 145(Pt8):1891–1901
Dormann D, Weijer CJ (2001) Propagating chemoattractant waves coordinate periodic cell movement in Dictyostelium slugs. Development 128(22):4535–4543
Dynes JL, Clark AM, Shaulsky G, Kuspa A, Loomis WF, Firtel RA (1994) LagC is required for cell-cell interactions that are essential for cell-type differentiation in Dictyostelium. Genes Dev 8:948–958
Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, Hemphill L, Bason N, Farbrother P, Desany B, Just E, Morio T, Rost R, Churcher C, Cooper J, Haydock S, van Driessche N, Cronin A, Goodhead I, Muzny D, Mourier T, Pain A, Lu M, Harper D, Lindsay R, Hauser H, James K, Quiles M, Madan Babu M, Saito T, Buchrieser C, Wardroper A, Felder M, Thangavelu M, Johnson D, Knights A, Loulseged H, Mungall K, Oliver K, Price C, Quail MA, Urushihara H, Hernandez J, Rabbinowitsch E, Steffen D, Sanders M, Ma J, Kohara Y, Sharp S, Simmonds M, Spiegler S, Tivey A, Sugano S, White B, Walker D, Woodward J, Winckler T, Tanaka Y, Shaulsky G, Schleicher M, Weinstock G, Rosenthal A, Cox EC, Chisholm RL, Gibbs R, Loomis WF, Platzer M, Kay RR, Williams J, Dear PH, Noegel AA, Barrell B, Kuspa A (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435(7038):43–57
Feit IN, Bonner JT, Suthers HB (1990) Regulation of the anterior-like cell state by ammonia in Dictyostelium discoideum. Dev Genetics 11:442–446
Feit IN, Medynski EJ, Rothrock MJ (2001) Ammonia differentially suppresses the cAMP chemotaxis of anterior-like cells and prestalk cells in Dictyostelium discoideum. J Biosci 26(2):157–166
Feit IN, Pawlikowski J, Zawilski C (2007) A model for cell type localization in the migrating slug of Dictyostelium discoideum based on differential chemotactic sensitivity to cANIP and differential sensitivity to suppression of chemotaxis by ammonia. J Biosci 32(2):329–338
Fritz-Laylin LK, Prochnik SE, Ginger ML, Dacks JB, Carpenter ML, Field MC, Kuo A, Paredez A, Chapman J, Pham J, Shu S, Neupane R, Cipriano M, Mancuso J, Tu H, Salamov A, Lindquist E, Shapiro H, Lucas S, Grigoriev IV, Cande WZ, Fulton C, Rokhsar DS, Dawson SC (2010) The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140(5):631–642. doi:10.1016/j.cell.2010.01.032
Galardi-Castilla M, Garciandia A, Suarez T, Sastre L (2010) The Dictyostelium discoideum acaA gene is transcribed from alternative promoters during aggregation and multicellular development. PLoS One 5(10):e13286. doi:10.1371/journal.pone.0013286
Gerisch G, Fromm H, Huesgen A, Wick U (1975) Control of cell-contact sites by cyclic AMP pulses in differentiating Dictyostelium cells. Nature 255:547–549
Harwood AJ, Hopper NA, Simon M-N, Driscoll DM, Veron M, Williams JG (1992) Culmination in Dictyostelium is regulated by the cAMP-dependent protein kinase. Cell 69:615–624
Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Micro 7(4):263–273
Hirose S, Benabentos R, Ho H-I, Kuspa A, Shaulsky G (2011) Self-recognition in social amoebae is mediated by allelic pairs of tiger genes. Science 333(6041):467–470. doi:10.1126/science.1203903
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
Jenal U, Malone J (2006) Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet 40:385–407. doi:10.1146/annurev.genet.40.110405.090423
Jin J, Pawson T (2012) Modular evolution of phosphorylation-based signalling systems. Philos Trans R Soc Lond B Biol Sci 367 (1602):2540–2555. doi:10.1098/rstb.2012.0106
Kawabe Y, Morio T, James JL, Prescott AR, Tanaka Y, Schaap P (2009) Activated cAMP receptors switch encystation into sporulation. Proc Natl Acad Sci U S A 106(17):7089–7094. doi:10.1073/pnas.0901617106 (0901617106 [pii])
Kawabe Y, Weening KE, Marquay-Markiewicz J, Schaap P (2012) Evolution of self-organisation in Dictyostelia by adaptation of a non-selective phosphodiesterase and a matrix component for regulated cAMP degradation. Development 139(7):1336–1345. doi:10.1242/dev.077099
Kay RR, Thompson CR (2001) Cross-induction of cell types in Dictyostelium: evidence that DIF-1 is made by prespore cells. Development 128(24):4959–4966
Kessin RH (2001) Dictyostelium: Evolution, cell biology and the development of multicellularity. Developmental and cell biology series, vol 38. Cambridge University Press, Cambridge
Kibler K, Svetz J, Nguyen TL, Shaw C, Shaulsky G (2003) A cell-adhesion pathway regulates intercellular communication during Dictyostelium development. Dev Biol 264 (2):506–521
Kim SK, Kaiser D, Kuspa A (1992) Control of cell density and pattern by intercellular signaling in Myxococcus development. Annu Rev Microbiol 46:117–139. doi:10.1146/annurev.mi.46.100192.001001
Kirsten JH, Xiong YH, Dunbar AJ, Rai M, Singleton CK (2005) Ammonium transporter C of Dictyostelium discoideum is required for correct prestalk gene expression and for regulating the choice between slug migration and culmination. Developmental Biology 287(1):146–156
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 U S A 90:5969–5973
O’Day DH, Keszei A (2011) Signalling and sex in the social amoebozoans. Biol Rev Cambridge Phil Soc. doi:10.1111/j.1469-185X.2011.00200.x
Olive LS (1978) Sorocarp development by a newly discovered ciliate. Science 202(4367):530–532. doi:10.1126/science.202.4367.530 (202/4367/530 [pii])
Otto GP, Wu MY, Kazgan N, Anderson OR, Kessin RH (2003) Macroautophagy is required for multicellular development of the social amoeba Dictyostelium discoideum. J Biol Chem 278(20):17636–17645
Raper KB (1984) The Dictyostelids. Princeton University Press, Princeton
Ritchie AV, van Es S, Fouquet C, Schaap P (2008) From drought sensing to developmental control: evolution of cyclic AMP signaling in social amoebas. Mol Biol Evol 25(10):2109–2118. doi:10.1093/molbev/msn156 [doi] (msn156 [pii])
Rogers KW, Schier AF (2011) Morphogen gradients: from generation to interpretation. Annu Rev Cell Dev Biol 27:377–407. doi:10.1146/annurev-cellbio-092910-154148
Romeralo M, Cavender JC, Landolt JC, Stephenson SL, Baldauf SL (2011) An expanded phylogeny of social amoebas (Dictyostelia) shows increasing diversity and new morphological patterns. BMC Evol Biol 11:84. doi:10.1186/1471-2148-11-84 (1471-2148-11-84 [pii])
Romeralo M, Skiba A, Schilde C, Gonzalez-Voyer A, Lawal H, Kedziora S, Cavender JC, Gloeckner G, Urushihara H, Schaap P (2013) Detailed mapping of phenotypic evolution in social amoebas highlights developmental plasticity as a consequence of colonial multicellularity. Proc Biol Sci 280(1764):20130976
Saito T, Taylor GW, Yang JC, Neuhaus D, Stetsenko D, Kato A, Kay RR (2006) Identification of new differentiation inducing factors from Dictyostelium discoideum. Biochim Biophys Acta 1760(5):754–761. doi:10.1016/j.bbagen.2005.12.006 (S0304-4165(05)00392-2 [pii])
Saito T, Kato A, Kay RR (2008) DIF-1 induces the basal disc of the Dictyostelium fruiting body. Dev Biol 317(2):444–453. doi:10.1016/j.ydbio.2008.02.036 [doi] (S0012-1606(08)00150-4 [pii])
Saran S, Schaap P (2004) Adenylyl cyclase G is activated by an intramolecular osmosensor. Mol Biol Cell 15(3):1479–1486
Sawai S, Thomason PA, Cox EC (2005) An autoregulatory circuit for long-range self-organization in Dictyostelium cell populations. Nature 433(7023):323–326
Schaap P (1983) Quantitative analysis of the spatial distribution of ultrastructural differentiation markers during development of Dictyostelium discoideum. Roux’s Arch Dev Biol 192:86–94
Schaap P (2007) The evolution of size and pattern in the social amoebas. BioEssays 29:635–644
Schaap P, Winckler T, Nelson M, Alvarez-Curto E, Elgie B, Hagiwara H, Cavender J, Milano-Curto A, Rozen DE, Dingermann T, Mutzel R, Baldauf SL (2006) Molecular phylogeny and evolution of morphology in the social amoebas. Science 314(5799):661–663
Schindler J, Sussman M (1977) Ammonia determines the choice of morphogenetic pathways in Dictyostelium discoideum. JMolBiol 116:161–169
Schulkes C, Schaap P (1995) cAMP-dependent protein kinase activity is essential for preaggegative gene expression in Dictyostelium. FEBS Lett 368:381–384
Schuster SC, Noegel AA, Oehme F, Gerisch G, Simon MI (1996) The hybrid histidine kinase DokA is part of the osmotic response system of Dictyostelium. EMBO J 15:3880–3889
Serafimidis I, Kay RR (2005) New prestalk and prespore inducing signals in Dictyostelium. Dev Biol 282(2):432–441
Singleton CK, Zinda MJ, Mykytka B, Yang P (1998) The histidine kinase dhkC regulates the choice between migrating slugs and terminal differentiation in Dictyostelium discoideum. Dev Biol 203:345–357
Singleton CK, Kirsten JH, Dinsmore CJ (2006) Function of ammonium transporter A in the initiation of culmination of development in Dictyostelium discoideum. Eukaryot Cell 5(7):991–996
Soderbom F, Anjard C, Iranfar N, Fuller D, Loomis WF (1999) An adenylyl cyclase that functions during late development of Dictyostelium. Development 126:5463–5471
Souza GM, Lu SJ, Kuspa A (1998) Yaka, a protein kinase required for the transition from growth to development in dictyostelium. Development 125:2291–2302
Souza GM, daSilva AM, Kuspa A (1999) Starvation promotes Dictyostelium development by relieving PufA inhibition of PKA translation through the YakA kinase pathway. Development 126 (14):3263–3274
Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466(7307):720–726. doi:10.1038/nature09201
Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209. doi:10.1146/annurev.micro.56.012302.160705
Sugimoto H, Endoh H (2006) Analysis of fruiting body development in the aggregative ciliate Sorogena stoianovitchae (Ciliophora, Colpodea). J Eukaryot Microbiol 53(2):96–102. doi:10.1111/j.1550-7408.2005.00077.x (JEU77 [pii])
Sun TJ, Devreotes PN (1991) Gene targeting of the aggregation stage cAMP receptor cAR1 in Dictyostelium. Genes Dev 5:572–582
Swanson AR, Vadell EM, Cavender JC (1999) Global distribution of forest soil dictyostelids. J Biogeogr 26(1):133–148
Thomason P, Kay R (2000) Eukaryotic signal transduction via histidine-aspartate phosphorelay. J Cell Sci 113(Pt 18):3141–3150
Toama MA, Raper KB (1967) Microcysts of the cellular slime mold Polysphondylium pallidum. I. Factors influencing microcyst formation. J Bacteriol 94(4):1143–1149
Van Es S, Virdy KJ, Pitt GS, Meima M, Sands TW, Devreotes PN, Cotter DA, Schaap P (1996) Adenylyl cyclase G, an osmosensor controlling germination of Dictyostelium spores. J Biol Chem 271:23623–23625
Virdy KJ, Sands TW, Kopko SH, van Es S, Meima M, Schaap P, Cotter DA (1999) High cAMP in spores of Dictyostelium discoideum: association with spore dormancy and inhibition of germination. Microbiology 145(Pt8):1883–1890
Wang M, Schaap P (1989) Ammonia depletion and DIF trigger stalk cell differentiation in intact Dictyostelium discoideum slugs. Development 105:569–574
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
Wang N, Soderbom F, Anjard C, Shaulsky G, Loomis WF (1999) SDF-2 induction of terminal differentiation in Dictyostelium discoideum is mediated by the membrane-spanning sensor kinase DhkA. Mol Cell Biol 19(7):4750–4756
West CM (2003) Comparative analysis of spore coat formation, structure, and function in Dictyostelium. Int Rev Cytol 222:237–293
Williams JG (2006) Transcriptional regulation of Dictyostelium pattern formation. EMBO Rep 7(7):694–698
Yamada Y, Kay RR, Bloomfield G, Ross S, Ivens A, Williams JG (2010) A new Dictyostelium prestalk cell sub-type. Dev Biol 339(2):390–397. doi:10.1016/j.ydbio.2009.12.045 (S0012-1606(10)00005-9 [pii])
Acknowledgements
YK, CS and HL are supported by project grant BB/G020426/1 from the Biotechnology and Biological Sciences Research Council, and ZC and QD by project grant 090276 from the Wellcome Trust.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Kawabe, Y., Schilde, C., Chen, Zh., Du, Q., Lawal, H., Schaap, P. (2015). The Evolution of Developmental Signalling in Dictyostelia from an Amoebozoan Stress Response. In: Ruiz-Trillo, I., Nedelcu, A. (eds) Evolutionary Transitions to Multicellular Life. Advances in Marine Genomics, vol 2. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9642-2_21
Download citation
DOI: https://doi.org/10.1007/978-94-017-9642-2_21
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-017-9641-5
Online ISBN: 978-94-017-9642-2
eBook Packages: Earth and Environmental ScienceEarth and Environmental Science (R0)