Skip to main content

The Evolution of Developmental Signalling in Dictyostelia from an Amoebozoan Stress Response

  • Chapter
  • First Online:
Evolutionary Transitions to Multicellular Life

Part of the book series: Advances in Marine Genomics ((AMGE,volume 2))

  • 1690 Accesses

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Anjard C, Loomis WF (2006) GABA induces terminal differentiation of Dictyostelium through a GABA(B) receptor. Development 133(11):2253–2261

    Article  CAS  Google Scholar 

  • Anjard C, Loomis WF (2008) Cytokinins induce sporulation in Dictyostelium. Development 135:819–827

    Article  CAS  Google Scholar 

  • 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])

    Article  CAS  Google Scholar 

  • 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])

    Article  Google Scholar 

  • 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])

    Article  CAS  Google Scholar 

  • 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] )

    Google Scholar 

  • 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])

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cotter DA (1977) The effects of osmotic pressure changes on the germination of Dictyostelium discoideum spores. Can J Microbiol 23(9):1170–1177

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Dormann D, Weijer CJ (2001) Propagating chemoattractant waves coordinate periodic cell movement in Dictyostelium slugs. Development 128(22):4535–4543

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Feit IN, Bonner JT, Suthers HB (1990) Regulation of the anterior-like cell state by ammonia in Dictyostelium discoideum. Dev Genetics 11:442–446

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Micro 7(4):263–273

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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])

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Kessin RH (2001) Dictyostelium: Evolution, cell biology and the development of multicellularity. Developmental and cell biology series, vol 38. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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])

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Raper KB (1984) The Dictyostelids. Princeton University Press, Princeton

    Book  Google Scholar 

  • 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])

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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])

    Google Scholar 

  • 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

    Google Scholar 

  • 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])

    Article  CAS  Google Scholar 

  • 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])

    Article  CAS  Google Scholar 

  • Saran S, Schaap P (2004) Adenylyl cyclase G is activated by an intramolecular osmosensor. Mol Biol Cell 15(3):1479–1486

    Article  CAS  Google Scholar 

  • Sawai S, Thomason PA, Cox EC (2005) An autoregulatory circuit for long-range self-organization in Dictyostelium cell populations. Nature 433(7023):323–326

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Schaap P (2007) The evolution of size and pattern in the social amoebas. BioEssays 29:635–644

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Schindler J, Sussman M (1977) Ammonia determines the choice of morphogenetic pathways in Dictyostelium discoideum. JMolBiol 116:161–169

    CAS  Google Scholar 

  • Schulkes C, Schaap P (1995) cAMP-dependent protein kinase activity is essential for preaggegative gene expression in Dictyostelium. FEBS Lett 368:381–384

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Serafimidis I, Kay RR (2005) New prestalk and prespore inducing signals in Dictyostelium. Dev Biol 282(2):432–441

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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])

    Article  Google Scholar 

  • Sun TJ, Devreotes PN (1991) Gene targeting of the aggregation stage cAMP receptor cAR1 in Dictyostelium. Genes Dev 5:572–582

    Article  CAS  Google Scholar 

  • Swanson AR, Vadell EM, Cavender JC (1999) Global distribution of forest soil dictyostelids. J Biogeogr 26(1):133–148

    Article  Google Scholar 

  • Thomason P, Kay R (2000) Eukaryotic signal transduction via histidine-aspartate phosphorelay. J Cell Sci 113(Pt 18):3141–3150

    CAS  Google Scholar 

  • Toama MA, Raper KB (1967) Microcysts of the cellular slime mold Polysphondylium pallidum. I. Factors influencing microcyst formation. J Bacteriol 94(4):1143–1149

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wang M, Schaap P (1989) Ammonia depletion and DIF trigger stalk cell differentiation in intact Dictyostelium discoideum slugs. Development 105:569–574

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • West CM (2003) Comparative analysis of spore coat formation, structure, and function in Dictyostelium. Int Rev Cytol 222:237–293

    Article  Google Scholar 

  • Williams JG (2006) Transcriptional regulation of Dictyostelium pattern formation. EMBO Rep 7(7):694–698

    Article  CAS  Google Scholar 

  • 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])

    Article  CAS  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Pauline Schaap .

Editor information

Editors and Affiliations

Rights and permissions

Reprints 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

Publish with us

Policies and ethics