Abstract
The development of a higher organism needs many coupled pattern-forming reactions. Crucial are interactions in which a local self-enhancing reaction is coupled to an antagonistic reaction of longer range. Using the pattern of head, tentacle and foot formation in the small freshwater polyp hydra as a model system it is shown (1) how polar pattern can emerge; (2) how a polar pattern can be maintained during substantial growth; (3) how structures next to each other can be generated and (4) how two organizing regions can be forced to appear at a maximum distance from each other at the two terminal poles. The understanding of the organization along the single axis of the radial-symmetric hydra was a key to understand the evolution of bilateral-symmetric body plans. Many observations can be explained under the assumption that the body of hydra-like ancestors evolved into the brain of higher organisms, that generation of a midline was a subtle patterning process for which evolution has found different solutions, that the ancestral hydra-type organizer became the organizer for the AP axis in higher organisms, and that the trunk is a later evolutionary addition.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Bode HR (2003) Head regeneration in Hydra. Dev Dyn 226:225–236
Bosch TCG (2007) Why polyps regenerate and we don’t: towards a cellular and molecular framework for Hydra regeneration. Dev Biol 303:421–433
Gierer A (1977) Biological features and physical concepts of pattern formation exemplified by hydra. Curr Top Dev Biol 11:17–59
Holstein TW, Hobmayer E, Technau U (2003) Cnidarians: an evolutionarily conserved model system for regeneration? Dev Dyn 226:257–267
Gierer A, Berking S, Bode H, David CN, Flick K, Hansmann G, Schaller H, Trenkner E (1972) Regeneration of hydra from reaggregated cells. Nat New Biol 239:98–101
Browne EN (1909) The production of new hydrants in Hydra by insertion of small grafts. J Exp Zool 7:1–23
Broun M, Gee L, Reinhardt B, Bode HR (2005) Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 132:2907–2916
Hobmayer B, Rentzsch F, Kuhn K, Happel CM, Cramer von Laue C, Snyder P, Rothbacher U, Holstein TW (2000) Wnt signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407:186–189
Lengfeld T, Watanabe H, Simakov O, Lindgens D, Gee L, Law L, Schmidt HA, Özbek S, Bode H, Holstein TW (2009) Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev Biol 330:186–199
Meinhardt H (2002) The radial-symmetric hydra and the evolution of the bilateral body plan: an old body became a young brain. Bioessays 24:185–191
Meinhardt H (1989) Models for positional signalling with application to the dorsoventral patterning of insects and segregation into different cell types. Development (Supplement 1989):169–180
Chen G, Handel K, Roth S (2000) The maternal nf-kappa b/dorsal gradient of Tribolium castaneum: dynamics of early dorsoventral patterning in a short-germ beetle. Development 127:5145–5156
Meinhardt H (2004) Different strategies for midline formation in bilaterians. Nat Rev Neurosci 5:502–510
Gierer A, Meinhardt H (1972) A theory of biological pattern formation. Kybernetik 12:30–39
Meinhardt H (1982) Models of biological pattern formation. Academic, London (available at http://www.eb.tuebingen.mpg.de/meinhardt/82-book)
Meinhardt H (2008) Models of biological pattern formation: from elementary steps to the organization of embryonic axes. Curr Top Dev Biol 81:1–63
Turing A (1952) The chemical basis of morphogenesis. Philos Trans R Soc Lond B Biol Sci 237:37–72
Shimizu H, Fujisawa T (2003) Peduncle of Hydra and the heart of higher organisms share a common ancestral origin. Genesis 36:182–186
Meinhardt H (2006) Primary body axes of vertebrates: generation of a near-Cartesian coordinate system and the role of Spemann-type organizer. Dev Dyn 235:2907–2919
Duboc V, Rottinger E, Besnardeau L, Lepage T (2004) Nodal and bmp2/4 signaling organizes the oral-aboral axis of the sea urchin embryo. Dev Cell 6:397–410
Schier AF (2009) Nodal morphogens. Cold Spring Harb Perspect Biol. doi:10.1101/cshperspect.a003459
Huang X, Dong Y, Zhao J (2004) HetR homodimer is a DNA-binding protein required for heterocyst differentiation, and the DNA-binding activity is inhibited by PatS. Proc Natl Acad Sci U S A 101:4848–4853
Meinhardt H (1995) Growth and patterning – dynamics of stripe formation. Nature 376:722–723
Hörstadius S (1939) The mechanics of sea-urchin development studied by operative methods. Biol Rev 14:132–179
Müller WA, Plickert G (1982) Quantitative analysis of an inhibitory gradient field in the hydrozoan stolon. Wilhelm Roux Arch 191:56–63
Meinhardt H (1993) A model for pattern-formation of hypostome, tentacles, and foot in hydra: how to form structures close to each other, how to form them at a distance. Dev Biol 157:321–333
Bode PM, Awad TA, Koizumi O, Nakashima Y, Grimmelikhuijzen CJP, Bode HR (1988) Development of the two-part pattern during regeneration of the head in hydra. Development 102:223–235
Technau U, Holstein TW (1995) Head formation in hydra is different at apical and basal levels. Development 121:1273–1282
Meinhardt H (2009) The algorithmic beauty of sea shells, 4th enlarged edn (with programs on CD). Springer, Heidelberg/New York
Wilby OK, Webster G (1970) Experimental studies on axial polarity in hydra. J Embryol Exp Morphol 24:595–613
Meinhardt H, Gierer A (1980) Generation and regeneration of sequences of structures during morphogenesis. J Theor Biol 85:429–450
Holley SA, Jackson PD, Sasai Y, Lu B, De Robertis EM, Hoffmann FM, Ferguson EL (1995) The Algorithmic Beauty of Sea Shells. A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and Chordin. Nature 376:249–253
Schubert M, Holland LZ, Stokes MD, Holland ND (2001) Three amphioxus Wnt genes (amphiwnt3, amphiwnt5, and amphiwnt6) associated with the tail bud: the evolution of somitogenesis in chordates. Dev Biol 240:262–273
Reinhardt B, Broun M, Blitz IL, Bode HR (2004) Hybmp5-8b, a BMP5-8 orthologue, acts during axial patterning and tentacle formation in Hydra. Dev Biol 267:43–59
Wacker SA, Jansen HJ, McNulty CL, Houtzager E, Durston AJ (2004) Timed interactions between the Hox expressing non-organiser mesoderm and the Spemann organiser generate positional information during vertebrate gastrulation. Dev Biol 268:207–219
Ben-Zvi D, Shilo BZ, Fainsod A, Barkai N (2008) Scaling of the BMP activation gradient in Xenopus embryos. Nature 453:1205–1211
Palmeirim I, Henrique D, Ish-Horowicz D, Pourquie O (1997) Avian hairy gene-expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91:639–648
Kiecker C, Niehrs C (2001) A morphogen gradient of Wnt/β-catenin signalling regulates anteroposterior neural patterning in Xenopus. Development 128:4189–4201
Nordström U, Jessell TM, Edlund T (2002) Progressive induction of caudal neural character by graded Wnt signaling. Nat Neurosci 5:525–532
Ober EA, Schulte-Merker S (1999) Signals from the yolk cell induce mesoderm, neuroectoderm, the trunk organizer, and the notochord in zebrafish. Dev Biol 215:167–181
Meinhardt H (2001) Organizer and axes formation as a self-organizing process. Int J Dev Biol 45:177–188
Arendt D, Nübler-Jung K (1994) Inversion of dorsoventral axis. Nature 371:26
Levin M, Palmer AR (2007) Left-right patterning from the inside out: widespread evidence for intracellular control. Bioessays 29:271–287
Raya A, Izpisúa Belmonte JC (2006) Left-right asymmetry in the vertebrate embryo: from early information to higher-level integration. Nat Rev Genet 7:283–293
Vandenberg LN, Levin M (2009) Perspectives and open problems in the early phases of left-right patterning. Semin Cell Dev Biol 20:456–463
Nonaka S, Tanaka Y, Okada Y, Takeda S, Harada A, Kanai Y, Kido M, Hirokawa N (1998) Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motorprotein. Cell 95:829–837
Nakamura T, Mine N, Nakaguchi E, Mochizuki A, Yamamoto M, Yashiro K, Meno C, Hamada M (2006) Generation of robust left-right asymmetry in the mouse embryo requires a self-enhancement and lateral-inhibition system. Dev Cell 11:495–504
Meinhardt H (1978) Space-dependent cell determination under the control of a morphogen gradient. J Theor Biol 74:307–321
Nieuwkoop PD (1952) Activation and organization of the central nervous system in amphibians. III Synthesis of a new working hypothesis. J Exp Zool 120:83–108
Duboule D (2007) The rise and fall of Hox gene clusters. Development 134:2549–2560
Keller R (2005) Cell migration during gastrulation. Curr Opin Cell Biol 17:533–541
Rentzsch F, Guder C, Vocke D, Hobmayer B, Holstein TW (2007) An ancient Chordin-like gene in organizer formation of Hydra. Proc Natl Acad Sci U S A 104:3249–3254
Keynes RJ, Stern CD (1988) Mechanisms of vertebrate segmentation. Development 103:413–429
Stern CD, Keynes RJ (1987) Interaction between somite cells: the formation and maintenance of segment boundaries in the chick embryo. Development 99:261–272
Keynes RJ, Stern CD (1984) Segmentation in the vertebrate nervous system. Nature 310:786–789
Cooke J (1981) The problem of periodic patterns in embryos. Philos Trans R Soc Lond B Biol Sci 295:509–524
Dubrulle J, McGrew MJ, Pourquie O (2001) FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106:219–232
Cooke J, Zeeman EC (1976) A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. J Theor Biol 58:455–476
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer-Verlag Berlin Heidelberg
About this paper
Cite this paper
Meinhardt, H. (2013). From Hydra to Vertebrates: Models for the Transition from Radial- to Bilateral-Symmetric Body Plans. In: Capasso, V., Gromov, M., Harel-Bellan, A., Morozova, N., Pritchard, L. (eds) Pattern Formation in Morphogenesis. Springer Proceedings in Mathematics, vol 15. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-20164-6_17
Download citation
DOI: https://doi.org/10.1007/978-3-642-20164-6_17
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-20163-9
Online ISBN: 978-3-642-20164-6
eBook Packages: Mathematics and StatisticsMathematics and Statistics (R0)