Abstract
Dictyostelids were once grouped with fungi because their fruiting structures are superficially similar. However, either group evolved quite distinct strategies to reach this mode of species propagation. This chapter describes the cell communication systems that cause dictyostelid amoebas to aggregate and regulate cell-type specialisation and cell movement during fruiting body formation. It also highlights how increasingly complex morphologies appeared during dictyostelid evolution and how some of these morphological innovations were caused by modification of specific cell–cell signalling systems.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abe H, Uchiyama M, Tanaka Y, Saito H (1976) Structure of discadenine, a spore germination inhibitor from the cellular slime mold. Tetrahedron Lett 17(42):3807–3810
Adhikari N, Kuburich NA, Hadwiger JA (2020) Mitogen-activated protein kinase regulation of the phosphodiesterase RegA in early Dictyostelium development. Microbiology 166(2):129–140. https://doi.org/10.1099/mic.0.000868
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
Amagai A (1984) Induction by ethylene of macrocyst formation in the cellular slime mould Dictyostelium mucuroides. J Gen Microbiol 130:2961–2965
Anjard C, Loomis WF (2005) Peptide signaling during terminal differentiation of Dictyostelium. Proc Natl Acad Sci U S A 102(21):7607–7611
Anjard C, Loomis WF (2008) Cytokinins induce sporulation in Dictyostelium. Development 135:819–827
Anjard C, Zeng CJ, Loomis WF, Nellen W (1998) Signal transduction pathways leading to spore differentiation in dictyostelium discoideum. Dev Biol 193:146–155
Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290(5493):972–977. https://doi.org/10.1126/science.290.5493.972
Baldauf SL, Romeralo M, Fiz-Palacios O, Heidari N (2018) A deep hidden diversity of Dictyostelia. Protist 169(1):64–78. https://doi.org/10.1016/j.protis.2017.12.005
Bichler G, Weijer CJ (1994) A Dictyostelium anterior-like cell mutant reveals sequential steps in the prespore prestalk differentiation pathway. Development 120(10):2857–2868
Bloomfield G (2019) Sex and macrocyst formation in Dictyostelium. Int J Dev Biol 63:439–446. https://doi.org/10.1387/ijdb.190183gb
Bonner JT (1950) Observations on polarity in the slime mold Dictyostelium discoideum. Biol Bull 99:143–151
Bonner JT, Lamont DS (2005) Behavior of cellular slime molds in the soil. Mycologia 97(1):178–184
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 U S A 85(11):3885–3887. https://doi.org/10.1073/pnas.85.11.3885
Brazill DT, Gundersen R, Gomer RH (1997) A cell-density sensing factor regulates the lifetime of a chemoattractant-induced Ga-DTP conformation. FEBS Lett 404:100–104
Brown JM, Firtel RA (1999) Regulation of cell-fate determination in Dictyostelium. Dev Biol 216(2):426–441
Castillo DI, Switz GT, Foster KR, Queller DC, Strassmann JE (2005) A cost to chimerism in Dictyostelium discoideum on natural substrates. Evol Ecol Res 7(2):263–271
Cavallo D, Cervi D, Sands TW, Cotter DA (1999) Differential in vitro activation and deactivation of cysteine proteinases isolated during spore germination and vegetative growth of Dictyostelium discoideum. Eur J Biochem 266(1):132–142
Cavender JC, Vadell EM (2000) The genus Acytostelium. Mycologia 92(5):992–1008
Cavender JC, Worley AC, Raper KB (1981) The yellow-pigmented Dictyostelia. Am J Bot 68:373–382
Cavender JC, Vadell E, Landolt JC, Stephenson SL (2005) New species of small dictyostelids from the Great Smoky Mountains National Park. Mycologia 97(2):493–512. https://doi.org/10.3852/mycologia.97.2.493
Chang MT, Raper KB, Poff KL (1983) The effect of light on morphogenesis of Dictyostelium mucuroides. Exp Cell Res 143:335–341
Chen ZH, Schaap P (2012) The prokaryote messenger c-di-GMP triggers stalk cell differentiation in Dictyostelium. Nature 488(7413):680–683. https://doi.org/10.1038/nature11313
Chen G, Wang J, Xu X, Wu X, Piao R, Siu CH (2013) TgrC1 mediates cell-cell adhesion by interacting with TgrB1 via mutual IPT/TIG domains during development of Dictyostelium discoideum. Biochem J 452(2):259–269. https://doi.org/10.1042/BJ20121674
Chen ZH, Singh R, Cole C, Lawal HM, Schilde C, Febrer M, Barton GJ, Schaap P (2017) Adenylate cyclase a acting on PKA mediates induction of stalk formation by cyclic diguanylate at the Dictyostelium organizer. Proc Natl Acad Sci U S A 114(3):516–521. https://doi.org/10.1073/pnas.1608393114
Choi AH, O’Day DH (1982) Ammonia and the induction of microcyst differentiation in wild type and mutant strains of the cellular slime mold Polysphondylium pallidum. Dev Biol 92:356–364
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
Cotter DA (1977) The effects of osmotic pressure changes on the germination of Dictyostelium discoideum spores. Can J Microbiol 23(9):1170–1177
De Wit RJW, Konijn TM (1983a) Identification of the acrasin of Dictyostelium minutum as a derivative of folic acid. Cell Differ 12:205–210
De Wit RJW, Konijn TM (1983b) Pterins and folates as extracellular signals for chemotaxis and differentiation in the cellular slime molds. Biochem Clin Aspects Pteridines 2:383–400
Deery WJ, Gao T, Ammann R, Gomer RH (2002) A single cell density-sensing factor stimulates distinct signal transduction pathways through two different receptors. J Biol Chem 277(35):31972–31979
Devreotes PN (1994) G protein-linked signaling pathways control the developmental program of Dictyostelium. Neuron 12:235–241
Dormann D, Weijer CJ (2001) Propagating chemoattractant waves coordinate periodic cell movement in Dictyostelium slugs. Development 128(22):4535–4543
Dormann D, Vasiev B, Weijer CJ (1998) Propagating waves control Dictyostelium discoideum morphogenesis. Biophys Chem 72:21–35
Du Q, Kawabe Y, Schilde C, Chen ZH, Schaap P (2015) The evolution of aggregative multicellularity and cell-cell communication in the Dictyostelia. J Mol Biol 427(23):3722–3733. https://doi.org/10.1016/j.jmb.2015.08.008
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
Escalante R, Sastre L (2002) Regulated expression of the MADS-box transcription factor SrfA mediates activation of gene expression by protein kinase A during Dictyostelium sporulation. Mech Dev 117(1-2):201–208
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
Fey P, Cox EC (1997) Gene trapping with GFP: the isolation of developmental mutants in the slime mold polysphondylium. Curr Biol 7:909–912
Fisher PR, Williams KL (1981) Bidirectional phototaxis by Dictyostelium discoideum slugs. FEMS Microbiol Lett 12:87–89
Forbes G, Chen ZH, Kin K, Lawal HM, Schilde C, Yamada Y, Schaap P (2019) Phylogeny-wide conservation and change in developmental expression, cell-type specificity and functional domains of the transcriptional regulators of social amoebas. BMC Genomics 20(1):890. https://doi.org/10.1186/s12864-019-6239-3
Forbes G, Schilde C, Lawal H, Kin K, Du Q, Chen ZH, Rivero F, Schaap P (2022) Interactome and evolutionary conservation of Dictyostelid small GTPases and their direct regulators. Small GTPases 13(1):239–254. https://doi.org/10.1080/21541248.2021.1984829
Forget M, Adiba S, De Monte S (2021) Social conflicts in Dictyostelium discoideum: a matter of scales. Preprints 2020:2020080554. https://doi.org/10.20944/preprints202008.0554.v2
Fosnaugh KL, Loomis WF (1991) Coordinate regulation of the sport coat genes in Dictyostelium discoideum. Dev Gen 12:123–132
Fujimori T, Nakajima A, Shimada N, Sawai S (2019) Tissue self-organization based on collective cell migration by contact activation of locomotion and chemotaxis. Proc Natl Acad Sci U S A 116(10):4291–4296. https://doi.org/10.1073/pnas.1815063116
Fukuzawa M, Hopper N, Williams J (1997) cudA: a Dictyostelium gene with pleiotropic effects on cellular differentiation and slug behaviour. Development 124:2719–2728
Fukuzawa M, Araki T, Adrian I, Williams JG (2001) Tyrosine phosphorylation-independent nuclear translocation of a dictyostelium STAT in response to DIF signaling. Mol Cell 7(4):779–788
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. https://doi.org/10.1371/journal.pone.0013286
Gerisch G (1960) Zellfunktionen und Zelfunktionswechsel in der Entwicklung von Dictyostelium discoideum. I. Zellagglutination und Induktion der Fruchtkörperpolarität. Wilhelm Roux Arch Entwickl Mech Org 152:632–654
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
Ghosh R, Chhabra A, Phatale PA, Samrat SK, Sharma J, Gosain A, Mohanty D, Saran S, Gokhale RS (2008) Dissecting the functional role of polyketide synthases in Dictyostelium discoideum: biosynthesis of the differentiation regulating factor 4-methyl-5-pentylbenzene-1,3-diol. J Biol Chem 283(17):11348–11354. https://doi.org/10.1074/jbc.M709588200
Ginsburg GT, Gollop R, Yu Y, Louis JM, Saxe CL, Kimmel AR (1995) The regulation of Dictyostelium development by transmembrane signalling. J Eukaryot Microbiol 42:200–205
Gloeckner G, Lawal HM, Felder M, Singh R, Singer G, Weijer CJ, Schaap P (2016) The multicellularity genes of dictyostelid social amoebas. Nat Commun 7:12085. https://doi.org/10.1038/ncomms12085
Gomer RH, Jang W, Brazill D (2011) Cell density sensing and size determination. Dev Growth Differ 53(4):482–494. https://doi.org/10.1111/j.1440-169X.2010.01248.x
Hartley AD, Ward MP, Garrett S (1994) The Yak1 protein kinase of Saccharomyces cerevisiae moderates thermotolerance and inhibits growth by an Sch9 protein kinase-independent mechanism. Genetics 136(2):465–474
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
Heidel AJ, Lawal HM, Felder M, Schilde C, Helps NR, Tunggal B, Rivero F, John U, Schleicher M, Eichinger L, Platzer M, Noegel AA, Schaap P, Glöckner G (2011) Phylogeny-wide analysis of social amoeba genomes highlights ancient origins for complex intercellular communication. Genome Res 21(11):1882–1891. https://doi.org/10.1101/gr.121137.111
Hillmann F, Forbes G, Novohradska S, Ferling I, Riege K, Groth M, Westermann M, Marz M, Spaller T, Winckler T, Schaap P, Glockner G (2018) Multiple roots of fruiting body formation in Amoebozoa. Genome Biol Evol 10(2):591–606. https://doi.org/10.1093/gbe/evy011
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. https://doi.org/10.1126/science.1203903
Ho HI, Shaulsky G (2015) Temporal regulation of kin recognition maintains recognition-cue diversity and suppresses cheating. Nat Commun 6:7144. https://doi.org/10.1038/ncomms8144
Ho HI, Hirose S, Kuspa A, Shaulsky G (2013) Kin recognition protects cooperators against cheaters. Curr Biol 23(16):1590–1595. https://doi.org/10.1016/j.cub.2013.06.049
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
Huang E, Talukder S, Hughes TR, Curk T, Zupan B, Shaulsky G, Katoh-Kurasawa M (2011) BzpF is a CREB-like transcription factor that regulates spore maturation and stability in Dictyostelium. Dev Biol 358(1):137–146. https://doi.org/10.1016/j.ydbio.2011.07.017
Iriki H, Kawata T, Muramoto T (2019) Generation of deletions and precise point mutations in Dictyostelium discoideum using the CRISPR nickase. PLoS One 14(10):e0224128. https://doi.org/10.1371/journal.pone.0224128
Kawabe Y, Kuwayama H, Morio T, Urushihara H, Tanaka Y (2002) A putative serpentine receptor gene tasA required for normal morphogenesis of primary stalk and branch structure in Polysphondylium pallidum. Gene 285(1-2):291–299. https://doi.org/10.1016/s0378-1119(01)00887-3
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. https://doi.org/10.1073/pnas.0901617106
Kawabe Y, Schilde C, Du Q, Schaap P (2015) A conserved signalling pathway for amoebozoan encystation that was co-opted for multicellular development. Sci Rep 5:9644. https://doi.org/10.1038/srep09644
Kay RR, Taylor GW, Jermyn KA, Traynor D (1992) Chlorine-containing compounds produced during Dictyostelium development. Biochem J 281:155–161
Kin K, Forbes G, Cassidy A, Schaap P (2018) Cell-type specific RNA-Seq reveals novel roles and regulatory programs for terminally differentiated Dictyostelium cells. BMC Genomics 19(1):764. https://doi.org/10.1186/s12864-018-5146-3
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. Dev Biol 287(1):146–156
Kriebel PW, Parent CA (2004) Adenylyl cyclase expression and regulation during the differentiation of Dictyostelium discoideum. IUBMB Life 56(9):541–546
Kuwayama H, Kubohara Y (2009) Differentiation-inducing factor-1 and -2 function also as modulators for Dictyostelium chemotaxis. PLoS One 4(8):e6658. https://doi.org/10.1371/journal.pone.0006658
Lawal HM, Schilde C, Kin K, Brown MW, James J, Prescott AR, Schaap P (2020) Cold climate adaptation is a plausible cause for evolution of multicellular sporulation in Dictyostelia. Sci Rep 10(1):8797. https://doi.org/10.1038/s41598-020-65709-3
Leach CK, Ashworth JM, Garrod DR (1973) Cell sorting out during the differentiation of mixtures of metabolically distinct populations of Dictyostelium discoideum. J Embryol Exp Morphol 29:647–661
Lonski J (1976) The effect of ammonia on fruiting body size and microcyst formation in the cellular slime molds. Dev Biol 51(1):158–165. https://doi.org/10.1016/0012-1606(76)90131-7
Lonski JU, Pesut N (1977) Induction of encystment of Polysphondylium pallidum amoeba. Can J Microbiol 23:518–521
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
Maeda M, Lu S, Shaulsky G, Miyazaki Y, Kuwayama H, Tanaka Y, Kuspa A, Loomis WF (2004) Periodic signaling controlled by an oscillatory circuit that includes protein kinases ERK2 and PKA. Science 304(5672):875–878. https://doi.org/10.1126/science.1094647
Mann SKO, Richardson DL, Lee S, Kimmel AR, Firtel RA (1994) Expression of cAMP-dependent protein kinase in prespore cells is sufficient to induce spore cell differentiation in Dictyostelium. Proc Natl Acad Sci U S A 91:10561–10565
McRobbie SJ, Jermyn KA, Duffy K, Blight K, Williams JG (1988) Two DIF-inducible, prestalk-specific mRNAs of Dictyostelium encode extracellular matrix protein of the slug. Development 104:275–284
Meima ME, Schaap P (1999) Fingerprinting of adenylyl cyclase activities during Dictyostelium development indicates a dominant role for adenylyl cyclase B in terminal differentiation. Dev Biol 212(1):182–190
Mercer SE, Friedman E (2006) Mirk/Dyrk1B: a multifunctional dual-specificity kinase involved in growth arrest, differentiation, and cell survival. Cell Biochem Biophys 45(3):303–315. https://doi.org/10.1385/CBB:45:3:303
Mesquita A, Cardenal-Muñoz E, Dominguez E, Muñoz-Braceras S, Nuñez-Corcuera B, Phillips BA, Tábara LC, Xiong Q, Coria R, Eichinger L, Golstein P, King JS, Soldati T, Vincent O, Escalante R (2017) Autophagy in Dictyostelium: mechanisms, regulation and disease in a simple biomedical model. Autophagy 13(1):24–40. https://doi.org/10.1080/15548627.2016.1226737
Miermont A, Antolović V, Lenn T, Nichols JME, Millward LJ, Chubb JR (2019) The fate of cells undergoing spontaneous DNA damage during development. Development 146(12):dev174268. https://doi.org/10.1242/dev.174268
Mohanty S, Jermyn KA, Early A, Kawata T, Aubry L, Ceccarelli A, Schaap P, Williams JG, Firtel RA (1999) Evidence that the Dictyostelium Dd-STATa protein is a repressor that regulates commitment to stalk cell differentiation and is also required for efficient chemotaxis. Development 126(15):3391–3405
Mohri K, Kiyota Y, Kuwayama H, Urushihara H (2013) Temporal and non-permanent division of labor during sorocarp formation in the social amoeba Acytostelium subglobosum. Dev Biol 375(2):202–209. https://doi.org/10.1016/j.ydbio.2013.01.003
Mohri K, Tanaka R, Nagano S (2020) Live cell imaging of cell movement and transdifferentiation during regeneration of an amputated multicellular body of the social amoeba Dictyostelium discoideum. Dev Biol 457(1):140–149. https://doi.org/10.1016/j.ydbio.2019.09.014
Mutzel R, Lacombe M-L, Simon M-N, De Gunzburg J, Veron M (1987) Cloning and cDNA sequence of the regulatory subunit of cAMP-dependent protein kinase from Dictyostelium discoideum. Proc Natl Acad Sci U S A 84:6–10
Narita TB, Chen ZH, Schaap P, Saito T (2014) The hybrid type polyketide synthase SteelyA is required for cAMP signalling in early Dictyostelium development. PLoS One 9(9):e106634. https://doi.org/10.1371/journal.pone.0106634
Narita TB, Kawabe Y, Kin K, Gibbs RA, Kuspa A, Muzny DM, Richards S, Strassmann JE, Sucgang R, Worley KC, Schaap P (2020) Loss of the polyketide synthase StlB results in stalk cell overproduction in Polysphondylium violaceum. Genome Biol Evol 12(5):674–683. https://doi.org/10.1093/gbe/evaa079
Nichols JME, Antolović V, Reich JD, Brameyer S, Paschke P, Chubb JR (2020) Cell and molecular transitions during efficient dedifferentiation. eLife 9:e55435. https://doi.org/10.7554/eLife.55435
Obata Y, Abe H, Tanaka Y, Yanagisawa K, Uchiyama M (1973) Isolation of a spore germination inhibitor from a cellular slime mold Dictyostelium discoideum. Agr Biol Chem 37:1989–1990
Oehme F, Schuster SC (2001) Osmotic stress-dependent serine phosphorylation of the histidine kinase homologue DokA. BMC Biochem 2(1):2
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
Pal DS, Li X, Banerjee T, Miao Y, Devreotes PN (2019) The excitable signal transduction networks: movers and shapers of eukaryotic cell migration. Int J Dev Biol 63:407–416. https://doi.org/10.1387/ijdb.190265pd
Parikh A, Miranda ER, Katoh-Kurasawa M, Fuller D, Rot G, Zagar L, Curk T, Sucgang R, Chen R, Zupan B, Loomis WF, Kuspa A, Shaulsky G (2010) Conserved developmental transcriptomes in evolutionarily divergent species. Genome Biol 11(3):R35. https://doi.org/10.1186/gb-2010-11-3-r35
Paschke P, Knecht DA, Williams TD, Thomason PA, Insall RH, Chubb JR, Kay RR, Veltman DM (2019) Genetic engineering of Dictyostelium discoideum cells based on selection and growth on bacteria. J Vis Exp 143. https://doi.org/10.3791/58981
Peracino B, Borleis J, Jin T, Westphal M, Schwartz JM, Wu L, Bracco E, Gerisch G, Devreotes P, Bozzaro S (1998) G protein beta subunit-null mutants are impaired in phagocytosis and chemotaxis due to inappropriate regulation of the actin cytoskeleton. J Cell Biol 141(7):1529–1537. https://doi.org/10.1083/jcb.141.7.1529
Poff KL, Skokut M (1977) Thermotaxis by pseudoplasmodia of Dictyostelium discoideum. Proc Natl Acad Sci USA 74:2007–2010
Raper KB (1940) Pseudoplasmodium formation and organization in Dictyostelium discoideum. J Elisha Mitchell Sci Soc 56:241–282
Raper KB (1984) The Dictyostelids. Princeton University Press, Princeton, NJ
Raper KB, Fennell DI (1952) Stalk formation in Dictyostelium. Bull Torrey Bot Club 79:25–51
Rathi A, Kayman SC, Clarke M (1991) Induction of gene expression in Dictyostelium by prestarvation factor, a factor secreted by growing cells. Dev Gen 12:82–87
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. https://doi.org/10.1093/molbev/msn156
Roisin-Bouffay C, Jang W, Caprette DR, Gomer RH (2000) A precise group size in Dictyostelium is generated by a cell-counting factor modulating cell-cell adhesion. Mol Cell 6(4):953–959
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(1):84. https://doi.org/10.1186/1471-2148-11-84
Romeralo M, Skiba A, Gonzalez-Voyer A, Schilde C, Lawal H, Kedziora S, Cavender JC, Glöckner G, Urushihara H, Schaap P (2013) Analysis of phenotypic evolution in Dictyostelia highlights developmental plasticity as a likely consequence of colonial multicellularity. Proc Biol Sci 280(1764):20130976. https://doi.org/10.1098/rspb.2013.0976
Römling U, Galperin Michael Y, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77(1):1–52. https://doi.org/10.1128/MMBR.00043-12
Saito T, Kato A, Kay RR (2008) DIF-1 induces the basal disc of the Dictyostelium fruiting body. Dev Biol 317(2):444–453. https://doi.org/10.1016/j.ydbio.2008.02.036
Saran S, Schaap P (2004) Adenylyl cyclase G is activated by an intramolecular osmosensor. Mol Biol Cell 15(3):1479–1486
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 (2021) From environmental sensing to developmental control: cognitive evolution in dictyostelid social amoebas. Philos Trans R Soc Lond Ser B Biol Sci 376(1820):20190756. https://doi.org/10.1098/rstb.2019.0756
Schaap P, Van Lookeren Campagne MM, Van Driel R, Spek W, Van Haastert PJ, Pinas J (1986) Postaggregative differentiation induction by cyclic AMP in Dictyostelium: intracellular transduction pathway and requirement for additional stimuli. Dev Biol 118(1):52–63
Schilde C, Skiba A, Schaap P (2014) Evolutionary reconstruction of pattern formation in 98 Dictyostelium species reveals that cell-type specialization by lateral inhibition is a derived trait. EvoDevo 5:34. https://doi.org/10.1186/2041-9139-5-34
Schilde C, Lawal HM, Kin K, Shibano-Hayakawa I, Inouye K, Schaap P (2019) A well supported multi gene phylogeny of 52 dictyostelia. Mol Phylogenet Evol 134:66–73. https://doi.org/10.1016/j.ympev.2019.01.017
Schindler J, Sussman M (1977) Ammonia determines the choice of morphogenetic pathways in Dictyostelium discoideum. J Mol Biol 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
Shaulsky G, Fuller D, Loomis WF (1998) A cAMP-phosphodiesterase controls PKA-dependent differentiation. Development 125:691–699
Sheikh S, Gloeckner G, Kuwayama H, Schaap P, Urushihara H, Baldauf SL (2015) Root of Dictyostelia based on 213 universal proteins. Mol Phylogenet Evol 92:53–62. https://doi.org/10.1016/j.ympev.2015.05.017
Sheikh S, Thulin M, Cavender JC, Escalante R, Kawakami SI, Lado C, Landolt JC, Nanjundiah V, Queller DC, Strassmann JE, Spiegel FW, Stephenson SL, Vadell EM, Baldauf SL (2018) A new classification of the Dictyostelids. Protist 169(1):1–28. https://doi.org/10.1016/j.protis.2017.11.001
Shimomura O, Suthers HLB, Bonner JT (1982) Chemical identity of the acrasin of the cellular slime mold Polysphondylium violaceum. Proc Natl Acad Sci U S A 79:7376–7379
Singer G, Araki T, Weijer CJ (2019) Oscillatory cAMP cell-cell signalling persists during multicellular Dictyostelium development. Commun Biol 2:139. https://doi.org/10.1038/s42003-019-0371-0
Singh R, Schilde C, Schaap P (2016) A core phylogeny of Dictyostelia inferred from genomes representative of the eight major and minor taxonomic divisions of the group. BMC Evol Biol 16(1):251. https://doi.org/10.1186/s12862-016-0825-7
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
Smith J, Queller DC, Strassmann JE (2014) Fruiting bodies of the social amoeba Dictyostelium discoideum increase spore transport by drosophila. BMC Evol Biol 14:105. https://doi.org/10.1186/1471-2148-14-105
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
Steinert M (2011) Pathogen-host interactions in Dictyostelium, legionella, mycobacterium and other pathogens. Semin Cell Dev Biol 22(1):70–76. https://doi.org/10.1016/j.semcdb.2010.11.003
Sternfeld J (1998) The anterior-like cells in Dictyostelium are required for the elevation of the spores during culmination. Dev Genes Evol 208:487–494
Sternfeld J, David CN (1981) Cell sorting daring pattern formation in Dictyostelium. Differentiation 20(1-3):10–21. https://doi.org/10.1111/j.1432-0436.1981.tb01150.x
Sternfeld J, David CN (1982) Fate and regulation of anterior-like cells in Dictyostelium slugs. DevBiol 93:111–118
Strassmann JE, Zhu Y, Queller DC (2000) Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408(6815):965–967
Sucgang R, Kuo A, Tian X, Salerno W, Parikh A, Feasley CL, Dalin E, Tu H, Huang E, Barry K, Lindquist E, Shapiro H, Bruce D, Schmutz J, Salamov A, Fey P, Gaudet P, Anjard C, Babu MM, Basu S, Bushmanova Y, van der Wel H, Katoh-Kurasawa M, Dinh C, Coutinho PM, Saito T, Elias M, Schaap P, Kay RR, Henrissat B, Eichinger L, Rivero F, Putnam NH, West CM, Loomis WF, Chisholm RL, Shaulsky G, Strassmann JE, Queller DC, Kuspa A, Grigoriev IV (2011) Comparative genomics of the social amoebae Dictyostelium discoideum and Dictyostelium purpureum. Genome Biol 12(2). https://doi.org/10.1186/gb-2011-12-2-r20
Swanson AR, Vadell EM, Cavender JC (1999) Global distribution of forest soil dictyostelids. J Biogeogr 26:133–148
Thomason PA, Traynor D, Cavet G, Chang W-T, Harwood AJ, Kay RR (1998) An intersection of the cAMP/PKA and two-component signal transduction systems in Dictyostelium. EMBO J 17:2838–2845
Thomason PA, Traynor D, Stock JB, Kay RR (1999) The RdeA-RegA system, a eukaryotic phospho-relay controlling cAMP breakdown. J Biol Chem 274(39):27379–27384
Thompson CR, Kay RR (2000a) Cell-fate choice in dictyostelium: intrinsic biases modulate sensitivity to DIF signaling. Dev Biol 227(1):56–64
Thompson CR, Kay RR (2000b) The role of DIF-1 signaling in Dictyostelium development. Mol Cell 6(6):1509–1514
Toama MA, Raper KB (1967) Microcysts of the cellular slime mold Polysphondylium pallidum. I Factors influencing microcyst formation. J Bacteriol 94(4):1143–1149
Traub F, Hohl HR, Cavender JC (1981) Cellular slime molds of Switzerland. I. Description of new species. Am J Bot 68:162–171
Urushihara H, Kuwayama H, Fukuhara K, Itoh T, Kagoshima H, Shin-I T, Toyoda A, Ohishi K, Taniguchi T, Noguchi H, Kuroki Y, Hata T, Uchi K, Mohri K, King JS, Insall RH, Kohara Y, Fujiyama A (2015) Comparative genome and transcriptome analyses of the social amoeba Acytostelium subglobosum that accomplishes multicellular development without germ-soma differentiation. BMC Genomics 16(1):80. https://doi.org/10.1186/s12864-015-1278-x
Vadell EM, Cavender JC (2007) Dictyostelids living in the soils of the Atlantic forest, Iguazu region, Misiones, Argentina: description of new species. Mycologia 99(1):112–124. https://doi.org/10.3852/mycologia.99.1.112
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
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
Waddell DR (1982) A predatory slime mould. Nature 298(5873):464–466. https://doi.org/10.1038/298464a0
Wang M, Van Haastert PJM, Schaap P (1986) Multiple effects of differentiation-inducing factor on prespore differentiation and cyclic-AMP signal transduction in Dictyostelium. Differentiation 33:24–28
Wang M, Aerts RJ, Spek W, Schaap P (1988a) Cell cycle phase in Dictyostelium discoideum is correlated with the expression of cyclic AMP production, detection, and degradation. Dev Biol 125:410–416
Wang M, Van Driel R, Schaap P (1988b) 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
Weijer CJ, Duschl G, David CN (1984) Dependence of cell-type proportioning and sorting on cell cycle phase in Dictyostelium discoideum. J Cell Sci 70:133–145
West CM (2003) Comparative analysis of spore coat formation, structure, and function in Dictyostelium. Int Rev Cytol 222:237–293
Wilkins MR, Williams KL (1995) The extracellular matrix of the Dictyostelium discoideum slug. Experientia 51:1189–1196
Yamada Y, Cassidy A, Schaap P (2018) The transcription factor spores absent A is a PKA dependent inducer of Dictyostelium sporulation. Sci Rep 8(1):6643. https://doi.org/10.1038/s41598-018-24915-w
Yamamoto A, Takeuchi I (1983) Vital staining of autophagic vacuoles in differentiating cells of Dictyostelium discoideum. Differentiation 24:83–87
Zinda MJ, Singleton CK (1998) The hybrid histidine kinase dhkB regulates spore germination in Dictyostelium discoideum. Dev Biol 196:171–183
Zucko J, Skunca N, Curk T, Zupan B, Long PF, Cullum J, Kessin RH, Hranueli D (2007) Polyketide synthase genes and the natural products potential of Dictyostelium discoideum. Bioinformatics 23(19):2543–2549. https://doi.org/10.1093/bioinformatics/btm381
Acknowledgements
This chapter is based on the previous edition of Evolution of Signalling and Morphogenesis in the Dictyostelids in The Mycota XIV authored by Pauline Schaap. I would like to express my immense gratitude for her input into the generation of the updated version and her help with the manuscript.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Schilde, C. (2023). Evolution of Signalling and Morphogenesis in the Dictyostelids. In: Pöggeler, S., James, T. (eds) Evolution of Fungi and Fungal-Like Organisms. The Mycota, vol 14. Springer, Cham. https://doi.org/10.1007/978-3-031-29199-9_2
Download citation
DOI: https://doi.org/10.1007/978-3-031-29199-9_2
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-29198-2
Online ISBN: 978-3-031-29199-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)