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Modelling Dictyostelium discoideum morphogenesis: The culmination

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Abstract

The culmination of the morphogenesis of the cellular slime mould Dictyostelium discoideum involves complex cell movements which transform a mound of cells into a globule of spores on a slender stalk. We show that cyclic AMP signalling and differential adhesion, combined with cell differentiation and slime production, are sufficient to produce the morphogenetic cell movements which lead to culmination. We have simulated the process of culmination using a hybrid cellular automata/partial differential equation model. With our model we have been able to reproduce the main features that occur during culmination, namely the straight downward elongation of the stalk, its anchoring to the substratum and the formation of the long thin stalk topped by the spore head.

We conclude that the cyclic AMP signalling system is responsible for the elongation and anchoring of the stalk, but in a roundabout way: pressure waves that are induced by the chemotaxis towards cyclic AMP squeeze the stalk through the cell mass. This mechanism forces the stalk to elongate precisely in the direction opposite to that of the chemotactically moving cells. The process turns out to be ‘guided’ by inactive ‘pathfinder’ cells, which form the tip of the stalk. We show that the entire development is enacted by means of the aforementioned building blocks. This means that no global gradients or different modes of chemotaxis are needed to complete the culmination.

MPEG movies of the simulations are available on-line: http://www-binf.bio. uu.nl/stan/bmb.

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References

  • Amagai, A., S. Ishida and I. Takeuchi (1983). Cell differentiation in a temperature-sensitive stalkless mutant of Dictyostelium discoideum. J. Embryol. Exp. Morphol. 74, 235–243.

    Google Scholar 

  • Berks, M. and R. R. Kay (1990). Combinatorial control of cell differentiation by cAMP and DIF-1 during development of Dictyostelium discoideum. Development 110, 977–984.

    Google Scholar 

  • Blanton, R. L. (1997). Cellulose biogenesis in Dictyostelium discoideum, in Dictyostelium: A Model System for Cell and Developmental Biology, Y. Maeda, K. Inouye and I. Takeuchi (Eds), Tokyo: Universal Academy Press, pp. 379–391.

    Google Scholar 

  • Bonner, J. T., A. D. Chiquoine and M. Q. Kolderie (1955). A histochemical study of differentiation in the cellular slime molds. J. Exp. Zool. 130, 133–157.

    Article  Google Scholar 

  • Bonner, J. T. and M. R. Dodd (1962). Aggregation territories in the cellular slime molds. Biol. Bull. 122, 13–24.

    Google Scholar 

  • Bonner, J. T., H. B. Suthers and G. M. Odell (1986). Ammonia orients cell masses and speeds up aggregating cells of slime moulds. Nature 323, 630–632.

    Article  Google Scholar 

  • Bozzaro, S. and E. Ponte (1995). Cell adhesion in the life cycle of Dictyostelium. Experientia 51, 1175–1188.

    Article  Google Scholar 

  • Bretschneider, T., F. Siegert and C. J. Weijer (1995). Three-dimensional scroll waves of cAMP could direct cell movement and gene expression in Dictyostelium slugs. Proc. Natl. Acad. Sci. U.S.A. 92, 4387–4391.

    Article  Google Scholar 

  • Bretschneider, T., B. Vasiev and C. J. Weijer (1999). A model for Dictyostelium slug movement. J. Theor. Biol. 199, 125–136.

    Article  Google Scholar 

  • Chen, T.-L. L., P. A. Kowalczyk, G. Ho and R. L. Chisholm (1995). Targeted disruption of the Dictyostelium myosin essential light chain gene produces cells defective in cytokinesis and morphogenesis. J. Cell Sci. 108, 3207–3218.

    Google Scholar 

  • Chen, T.-L. L., W. A. Wolf and R. L. Chisholm (1998). Cell-type-specific rescue of myosin function during Dictyostelium development defines two distinct cell movements required for culmination. Development 125, 3895–3903.

    Google Scholar 

  • Clow, P. A., T.-L. L. Chen, R. L. Chisholm and J. G. McNally (2000). Three-dimensional in vivo analysis of Dictyostelium mounds reveals directional sorting of prestalk cells and defines a role for the myosin II regulatory light chain in prestalk cell sorting and tip protrusion. Development 127, 2715–2728.

    Google Scholar 

  • Dormann, D., B. Vasiev and C. J. Weijer (1998). Propagating waves control Dictyostelium discoideum morphogenesis. Biophys. Chem. 72, 21–35.

    Article  Google Scholar 

  • Dormann, D., B. Vasiev and C. J. Weijer (2000). The control of chemotactic cell movement during Dictyostelium morphogenesis. Phil. Trans. R. Soc. Lond. B. Biol. Sci. 355, 983–991.

    Article  Google Scholar 

  • Feit, I. N. and R. B. Sollitto (1987). Ammonia is the gas used for the spacing of fruiting bodies in the cellular slime mold, Dictyostelium discoideum. Differentiation 33, 193–196.

    Google Scholar 

  • Fontana, D. R. (1995). Dictyostelium discoideum cohesion and adhesion, in Principles of Cell Adhesion, P. D. Richardson and M. Steiner (Eds), Boca Raton: CRC Press, pp. 63–86.

    Google Scholar 

  • Glazier, J. A. and F. Graner (1993). Simulation of the differential adhesion driven rearrangement of biological cells. Phys. Rev. E 47, 2128–2154.

    Article  Google Scholar 

  • Grimson, M. J., C. H. Haigler and R. L. Blanton (1996). Cellulose microfibrils, cell motility, and plasma membrane protein organization change in parallel during culmination in Dictyostelium discoideum. J. Cell Sci. 109, 3079–3087.

    Google Scholar 

  • Harwood, A. J., N. A. Hopper, M.-N. Simon, D. M. Driscoll, M. Veron and J. G. Williams (1992). Culmination in Dictyostelium is regulated by the cAMP-dependent protein kinase. Cell 69, 615–624.

    Article  Google Scholar 

  • Higuchi, G. and T. Yamada (1984). A cinematographical study of cellular slime molds. I. Stalk and disk formation in Dictyostelium discoideum. Cytologia 49, 841–849.

    Google Scholar 

  • Höfer, T., J. A. Sherratt and P. K. Maini (1995). Dictyostelium discoideum: cellular self-organization in an excitable biological medium. Proc. R. Soc. Lond. Ser. B 259, 249–257.

    Google Scholar 

  • Jermyn, K., D. Traynor and J. Williams (1996). The initiation of basal disc formation in Dictyostelium discoideum is an early event in culmination. Development 122, 753–760.

    Google Scholar 

  • Jermyn, K. A. and J. G. Williams (1991). An analysis of culmination in Dictyostelium using prestalk and stalk-specific cell autonomous markers. Development 111, 779–787.

    Google Scholar 

  • Jiang, Y., H. Levine and J. Glazier (1998). Possible cooperation of differential adhesion and chemotaxis in mound formation of Dictyostelium. Biophys. J. 75, 2615–2625.

    Google Scholar 

  • Kawasaki, Y., T. Kiryu, K. Usui and H. Mizutani (1990). Growth of the cellular slime mold, Dictyostelium discoideum, is gravity dependent. Plant Physiol. 93, 1568–1572.

    Google Scholar 

  • Keller, E. F. and L. A. Segel (1970). Initiation of slime mold aggregation viewed as an instability. J. Theor. Biol. 26, 399–415.

    Article  Google Scholar 

  • Kessin, R. H. (2001). Dictyostelium: Evolution, Cell Biology, and the Development of Multicellularity, Developmental and Cell Biology Series 38, Cambridge: Cambridge University Press.

    Google Scholar 

  • Kitami, M. (1984). Chemotactic response of Dictyostelium discoideum cell to c-AMP at the culmination stage. Cytologia 49, 257–264.

    Google Scholar 

  • Kitami, M. (1985). Motive force of the culminating mass of cells in the developing fruiting body of Dictyostelium discoideum. Cytologia 50, 109–115.

    Google Scholar 

  • Levine, H. and W. Reynolds (1991). Streaming instability of aggregating slime mold amoebae. Phys. Rev. Lett. 66, 2400–2403.

    Article  Google Scholar 

  • MacKay, S. A. (1978). Computer simulation of aggregation in Dictyostelium discoideum. J. Cell Sci. 33, 1–16.

    Google Scholar 

  • Marée, A. F. M. and P. Hogeweg (2001). How amoeboids self-organize into a fruiting body: multicellular coordination in Dictyostelium discoideum. Proc. Natl. Acad. Sci. U.S.A. 98, 3879–3883.

    Article  Google Scholar 

  • Marée, A. F. M., A. V. Panfilov and P. Hogeweg (1999a). Migration and thermotaxis of Dictyostelium discoideum slugs, a model study. J. Theor. Biol. 199, 297–309.

    Article  Google Scholar 

  • Marée, A. F. M., A. V. Panfilov and P. Hogeweg (1999b). Phototaxis during the slug stage of Dictyostelium discoideum: a model study. Proc. R. Soc. Lond. Ser. B 266, 1351–1360.

    Article  Google Scholar 

  • Miura, K. and F. Siegert (2000). Light affects cAMP signaling and cell movement activity in Dictyostelium discoideum. Proc. Natl. Acad. Sci. U.S.A. 97, 2111–2116.

    Article  Google Scholar 

  • Nanjundiah, V. (1973). Chemotaxis, signal relaying and aggregation morphology. J. Theor. Biol. 42, 63–105.

    Article  Google Scholar 

  • Odell, G. M. and J. T. Bonner (1986). How the Dictyostelium discoideum grex crawls. Phil. Trans. R. Soc. Lond. Ser. B 312, 487–525.

    Google Scholar 

  • Palsson, E. and H. G. Othmer (2000). A model for individual and collective cell movement in Dictyostelium discoideum. Proc. Natl. Acad. Sci. U.S.A. 97, 10448–10453.

    Google Scholar 

  • Panfilov, A. V. and A. M. Pertsov (1984). Vortex ring in a three-dimensional active medium described by reaction-diffusion equations. Dokl. Akad. Nauk SSSR 274, 1500–1503.

    Google Scholar 

  • Parnas, H. and L. A. Segel (1977). Computer evidence concerning the chemotactic signal in Dictyostelium discoideum. J. Cell Sci. 25, 191–204.

    Google Scholar 

  • Rubinow, S. I., L. A. Segel and W. Ebel (1981). A mathematical framework for the study of morphogenetic development in the slime mold. J. Theor. Biol. 91, 99–113.

    Article  Google Scholar 

  • Savill, N. J. and P. Hogeweg (1997). Modeling morphogenesis: from single cells to crawling slugs. J. Theor. Biol. 184, 229–235.

    Article  Google Scholar 

  • Siegert, F. and C. Weijer (1989). Digital image processing of optical density wave propagation in Dictyostelium discoideum and analysis of the effects of caffeine and ammonia. J. Cell Sci. 93, 325–335.

    Google Scholar 

  • Siegert, F. and C. J. Weijer (1992). Three-dimensional scroll waves organize Dictyostelium slugs. Proc. Natl. Acad. Sci. U.S.A. 89, 6433–6437.

    Article  Google Scholar 

  • Siegert, F. and C. J. Weijer (1995). Spiral and concentric waves organize multicellular Dictyostelium mounds. Curr. Biol. 5, 937–943.

    Article  Google Scholar 

  • Smith, D. (2000). Completed and near-complete 80 REMI genes [online] <www-biology.ucsd.edu/others/dsmith/REMIgenes2000.html>.

  • Sternfeld, J. (1992). A study of PstB cells during Dictyostelium migration and culmination reveals a unidirectional cell type conversion process. Roux’s Arch. Dev. Biol. 201, 354–363.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Takeuchi, I., T. Kakutani and M. Tasaka (1988). Cell behavior during formation of prestalk/prespore pattern in submerged agglomerates of Dictyostelium discoideum. Dev. Genet. 9, 607–614.

    Article  Google Scholar 

  • Thomason, P., D. Traynor and R. Kay (1999). Taking the plunge. Terminal differentiation in Dictyostelium. Trends Genet. 15, 15–19.

    Article  Google Scholar 

  • Tyson, J. J. and J. D. Murray (1989). Cyclic AMP waves during aggregation of Dictyostelium amoebae. Development 106, 421–426.

    Google Scholar 

  • Van Oss, C., A. V. Panfilov, P. Hogeweg, F. Siegert and C. J. Weijer (181). Spatial pattern formation during aggregation of the slime mould Dictyostelium discoideum. J. Theor. Biol. 203–213.

  • Vasiev, B. and C. J. Weijer (1999). Modeling chemotactic cell sorting during Dictyostelium discoideum mound formation. Biophys. J. 76, 595–605.

    Article  Google Scholar 

  • Vasiev, B. N., P. Hogeweg and A. V. Panfilov (1994). Simulation of Dictyostelium discoideum aggregation via reaction-diffusion model. Phys. Rev. Lett. 73, 3173–3176.

    Article  Google Scholar 

  • Verkerke-Van Wijk, I. and P. Schaap (1997). cAMP, a signal for survival, in Dictyostelium: A Model System for Cell and Developmental Biology, Y. Maeda, K. Inouye and I. Takeuchi (Eds), Tokyo: Universal Academy Press, pp. 145–162.

    Google Scholar 

  • Watts, D. J. and T. E. Treffry (1976). Culmination in the slime mould Dictyostelium discoideum studied with a scanning electron microscope. J. Embryol. Exp. Morphol. 35, 323–333.

    Google Scholar 

  • Weijer, C. J. (1999). The role of chemotactic cell movement in Dictyostelium morphogenesis, in On Growth and Form: Spatio-temporal Pattern Formation in Biology, Wiley Series in Mathematical and Computational Biology, M. A. J. Chaplain, G. D. Singh and J. C. McLachlan (Eds), Chichester: John Wiley & Sons, pp. 173–199.

    Google Scholar 

  • Whittingham, W. F. and K. B. Raper (1960). Non-viability of stalk cells in Dictyostelium. Proc. Natl. Acad. Sci. U.S.A. 46, 642–649.

    Article  Google Scholar 

  • Wilkins, M. R. and K. L. Williams (1995). The extracellular matrix of the Dictyostelium discoideum slug. Experientia 51, 1189–1196.

    Article  Google Scholar 

  • Williams, G. B., E. M. Elder and M. Sussman (1984). Modulation of the cAMP relay in Dictyostelium discoideum by ammonia and other metabolites: possible morphogenetic consequences. Dev. Biol. 105, 377–388.

    Article  Google Scholar 

  • Williams, J. (1997). Prestalk and stalk cell heterogeneity in Dictyostelium, in Dictyostelium: a Model System for Cell and Developmental Biology, Y. Maeda, K. Inouye and I. Takeuchi (Eds), Tokyo: Universal Academy Press, pp. 293–304.

    Google Scholar 

  • Williams, J., N. Hopper, A. Early, D. Traynor, A. Harwood, T. Abe, M. N. Simon and M. Véron (1993). Interacting signalling pathways regulating prestalk cell differentiation and movement during the morphogenesis of Dictyostelium. Development Suppl, 1–7.

    Google Scholar 

  • Williams, J. G., K. A. Jermyn and K. T. Duffy (1989). Formation and anatomy of the prestalk zone of Dictyostelium. Development Suppl, 91–97.

    Google Scholar 

  • Zeeman, E. C. (1977). Slime mold culmination, in Catastrophe Theory: Selected Papers, Reading, MA: Addison-Wesley, pp. 216–233.

    Google Scholar 

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  1. Athanasius F. M. Marée

    Present address: Department of Mathematics, University of British Columbia, Vancouver BC, Canada, V6T 1Z2

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  1. Theoretical Biology and Bioinformatics, University of Utrecht, Padualaan 8, 3584 CH, Utrecht, The Netherlands

    Athanasius F. M. Marée & Paulien Hogeweg

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Marée, A.F.M., Hogeweg, P. Modelling Dictyostelium discoideum morphogenesis: The culmination. Bull. Math. Biol. 64, 327–353 (2002). https://doi.org/10.1006/bulm.2001.0277

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