EvoDevo | |
Development and myogenesis of the vermiform Buddenbrockia (Myxozoa) and implications for cnidarian body plan evolution | |
Beth Okamura1  Alexander Gruhl1  | |
[1] Department of Zoology, Natural History Museum, Cromwell Road, London, SW7 5BD, UK | |
关键词: Mesoderm; Musculature; Chirality; Symmetry; Body axes; Development; Endoparasitism; Buddenbrockia; Myxozoa; Cnidaria; | |
Others : 821456 DOI : 10.1186/2041-9139-3-10 |
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received in 2012-02-15, accepted in 2012-05-17, 发布年份 2012 | |
【 摘 要 】
Background
The enigmatic wormlike parasite Buddenbrockia plumatellae has recently been shown to belong to the Myxozoa, which are now supported as a clade within Cnidaria. Most myxozoans are morphologically extremely simplified, lacking major metazoan features such as epithelial tissue layers, gut, nervous system, body axes and gonads. This hinders comparisons to free-living cnidarians and thus an understanding of myxozoan evolution and identification of their cnidarian sister group. However, B. plumatellae is less simplified than other myxozoans and therefore is of specific significance for such evolutionary considerations.
Methods
We analyse and describe the development of major body plan features in Buddenbrockia worms using a combination of histology, electron microscopy and confocal microscopy.
Results
Early developmental stages develop a primary body axis that shows a polarity, which is manifested as a gradient of tissue development, enabling distinction between the two worm tips. This polarity is maintained in adult worms, which, in addition, often develop a pore at the distal tip. The musculature comprises tetraradially arranged longitudinal muscle blocks consisting of independent myocytes embedded in the extracellular matrix between inner and outer epithelial tissue layers. The muscle fibres are obliquely oriented and in fully grown worms consistently form an angle of 12° with respect to the longitudinal axis of the worm in each muscle block and hence confer chirality. Connecting cells form a link between each muscle block and constitute four rows of cells that run in single file along the length of the worm. These connecting cells are remnants of the inner epithelial tissue layer and are anchored to the extracellular matrix. They are likely to have a biomechanical function.
Conclusions
The polarised primary body axis represents an ancient feature present in the last common ancestor of Cnidaria and Bilateria. The tetraradial arrangement of musculature is consistent with a medusozoan affinity for Myxozoa. However, the chiral pattern of muscle fibre orientation is apparently novel within Cnidaria and could thus be a specific adaptation. The presence of independent myocytes instead of Cnidaria-like epitheliomuscular cells can be interpreted as further support for the presence of mesoderm in cnidarians, or it may represent convergent evolution to a bilaterian condition.
【 授权许可】
2012 Gruhl and Okamura; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Schröder O: Buddenbrockia plumatellae, eine neue Mesozoenart aus Plumatella repens L. und Pl. fungosa Pall. Z Wiss Zool 1910, 96:525-537.
- [2]Schröder O: Zur Kenntnis der Buddenbrockia plumatellae Ol. Schröder. Z Wiss Zool 1912, 102:79-91.
- [3]Braem F: Beiträge zur Fauna Turkestans aufgrund des von D. D. Pedaschenko gesammelten Materials. VII. Bryozoen und deren Parasiten. Travaux de la Société Impériale des Naturalists de St. Pétersbourg 1911, 42:1-34.
- [4]Jiménez-Guri E, Okamura B, Holland PWH: Origin and evolution of a myxozoan worm. Int Comp Biol 2007, 47:752-758.
- [5]Okamura B, Curry A, Wood TS, Canning EU: Ultrastructure of Buddenbrockia identifies it as a myxozoan and verifies the bilaterian origin of the Myxozoa. Parasitology 2002, 124:215-223.
- [6]Monteiro AS, Okamura B, Holland PWH: Orphan worm finds a home: Buddenbrockia is a myxozoan. Mol Biol Evol 2002, 19:968-971.
- [7]Weill R: L’interpretation des Cnidosporidies et la valeur taxonomique de leur cnidome. Leur cycle comparé à la phase larvaire des Narcomeduses cuninides. Trav Stn Zool Wimeraux 1938, 13:727-744.
- [8]Siddall ME, Martin DS, Bridge D, Desser SS, Cone DK: The demise of a phylum of protists: Phylogeny of Myxozoa and other parasitic Cnidaria. J Parasitol 1995, 81:961-967.
- [9]Holland JW, Okamura B, Hartikainen H, Secombes CJ: A novel minicollagen gene links cnidarians and myxozoans. Proc Biol Sci 2011, 278:546-553.
- [10]Evans NM, Holder MT, Barbeitos MS, Okamura B, Cartwright P: The phylogenetic position of Myxozoa: exploring conflicting signals in phylogenomic and ribosomal data sets. Mol Biol Evol 2010, 27:2733-2746.
- [11]Jiménez-Guri E, Philippe H, Okamura B, Holland PWH: Buddenbrockia is a cnidarian worm. Science 2007, 317:116-118.
- [12]Canning EU, Okamura B: Biodiversity and evolution of the Myxozoa. Adv Parasitol 2004, 56:43-131.
- [13]Lom J, Dykova I: Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol (Praha) 2006, 53:1-36.
- [14]Grabner DS, El-Matbouli M: Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) to Fredericella sultana (Bryozoa: Phylactolaemata) by various fish species. Dis Aquat Organ 2008, 79:133-139.
- [15]Anderson CL, Canning EU, Okamura B: Molecular data implicate bryozoans as hosts for PKX (Phylum Myxozoa) and identify a clade of bryozoan parasites within the Myxozoa. Parasitology 1999, 119:555-561.
- [16]Morris DJ, Adams A: Proliferative, presaccular stages of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) within the invertebrate host Fredericella sultana (Bryozoa: Phylactolaemata). J Parasitol 2006, 92:984-989.
- [17]Grabner DS, El-Matbouli M: Experimental transmission of malacosporean parasites from bryozoans to common carp (Cyprinus carpio) and minnow (Phoxinus phoxinus). Parasitology 2010, 137:629-639.
- [18]Canning EU, Curry A, Feist SW, Longshaw M, Okamura B: A new class and order of myxozoans to accommodate parasites of bryozoans with ultrastructural observations on Tetracapsula bryosalmonae (PKX organism). J Eukaryot Microbiol 2000, 47:456-468.
- [19]Burton PM: Insights from diploblasts: the evolution of mesoderm and muscle. J Exp Zool B Mol Dev Evol 2008, 310:5-14.
- [20]Seipel K, Schmid V: Mesodermal anatomies in cnidarian polyps and medusae. Int J Dev Biol 2006, 50:589-599.
- [21]Martindale MQ, Pang K, Finnerty JR: Investigating the origins of triploblasty: “mesodermal” gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 2004, 131:2463-2474.
- [22]Canning EU, Curry A, Okamura B: Early development of the myxozoan Buddenbrockia plumatellae in the bryozoans Hyalinella punctata and Plumatella fungosa, with comments on taxonomy and systematics of the Myxozoa. Folia Parasitol (Praha) 2008, 45:241-255.
- [23]McGurk C, Morris DJ, Adams A: Sequential development of Buddenbrockia plumatellae (Myxozoa: Malacosporea) within Plumatella repens (Bryozoa: Phylactolaemata). Dis Aquat Organ 2006, 73:159-169.
- [24]Morris DJ, Adams A: Sacculogenesis of Buddenbrockia plumatellae (Myxozoa) within the invertebrate host Plumatella repens (Bryozoa) with comments on the evolutionary relationships of the Myxozoa. Int J Parasitol 2007, 37:1163-1171.
- [25]Canning EU, Tops S, Curry A, Wood TS, Okamura B: Ecology, development and pathogenicity of Buddenbrockia plumatellae Schröder, 1910 (Myxozoa, Malacosporea) (syn. Tetracapsula bryozoides) and establishment of Tetracapsuloides n. gen. for Tetracapsula bryosalmonae. J Eukaryot Microbiol 2002, 49:280-295.
- [26]Tops S, Curry A, Okamura B: Diversity and systematics of the Malacosporea (Myxozoa). Invertebr Biol 2005, 124:285-295.
- [27]Hirose M, Dick MH, Mawatari SF: Molecular phylogenetic analysis of phylactolaemate bryozoans based on mitochondrial gene sequences. In Bryozoan Studies 2007. Edited by Hageman GS, Key MMJ, Winston JE. Virginia Museum of Natural History, Martinsville, VA; 2008:346.
- [28]Canning EU, Okamura B, Curry A: Development of a myxozoan parasite Tetracapsula bryozoides gen. n. et sp. n. in Cristatella mucedo (Bryozoa: Phylactolaemata). Folia Parasitol (Praha) 1996, 43:259-261.
- [29]Tops S, Lockwood W, Okamura B: Temperature-driven proliferation of Tetracapsuloides bryosalmonae in bryozoan portends salmonid declines. Dis Aquat Organ 2006, 70:227-236.
- [30]Okamura B, Hartikainen H, Schmidt-Posthaus H, Wahli T: Life cycle complexity, environmental change and the emerging status of salmonid proliferative kidney disease. Freshw Biol 2011, 56:735-753.
- [31]Hartikainen H, Okamura B: Castrating parasites and colonial hosts. Parasitology 2012, 139:547-556.
- [32]Tops S, Hartikainen HL, Okamura B: The effects of infection by Tetracapsuloides bryosalmonae (Myxozoa) and temperature on Fredericella sultana (Bryozoa). Int J Parasitol 2009, 39:1003-1010.
- [33]Duffy DJ, Plickert G, Kuenzel T, Tilmann W, Frank U: Wnt signaling promotes oral but suppresses aboral structures in Hydractinia metamorphosis and regeneration. Development 2010, 137:3057-3066.
- [34]Petersen CP, Reddien PW: Wnt signaling and the polarity of the primary body axis. Cell 2009, 139:1056-1068.
- [35]Guder C, Philipp I, Lengfeld T, Watanabe H, Hobmayer B, Holstein TW: The Wnt code: cnidarians signal the way. Oncogene 2006, 25:7450-7460.
- [36]Lengfeld T, Watanabe H, Simakov O, Lindgens D, Gee L, Law L, Schmidt HA, Ozbek S, Bode H, Holstein TW: Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev Biol 2009, 330:186-199.
- [37]Martin BL, Kimelman D: Wnt signaling and the evolution of embryonic posterior development. Curr Biol 2009, 19:R215-R219.
- [38]Martindale MQ: The evolution of metazoan axial properties. Nat Rev Genet 2005, 6:917-927.
- [39]Nielsen C: Animal Evolution: Interrelationships of the Living Phyla. 3rd edition. Oxford University Press, Oxford; 2012:402.
- [40]Canning EU, Curry A, Hill SLL, Okamura B: Ultrastructure of Buddenbrockia allmani n. sp. (Myxozoa, Malacosporea), a parasite of Lophopus crystallinus (Bryozoa, Phylactolaemata). J Eukaryot Microbiol 2007, 54:247-262.
- [41]Ax P: Das System der Metazoa I. Gustav Fischer, Stuttgart; 1995.
- [42]Schmidt-Rhaesa A: The Evolution of Organ Systems. Oxford University Press, New York; 2007:363.
- [43]Ruppert EE: Introduction to the aschelminth phyla: a consideration of mesoderm, body cavities, and cuticle. In Microscopic Anatomy of Invertebrates: Aschelminthes. Volume 4. Edited by Harrison FW, Ruppert EE. Wiley Liss, New York; 1991:1-17.
- [44]Raikova EV: Life-Cycle, cytology, and morphology of Polypodium hydriforme, a coelenterate parasite of the eggs of acipenseriform fishes. J Parasitol 1994, 80:1-22.
- [45]Technau U, Scholz CB: Origin and evolution of endoderm and mesoderm. Int J Dev Biol 2003, 47:531-539.
- [46]Lipin A: Die Morphologie und Biologie von Polypodium hydriforme Uss. Zoologische Jahrbücher, Abteilung für Anatomie und Ontogenie der Tiere 1911, 31:317-426.
- [47]Raikova EV, Ibragimov AY, Raikova OI: Muscular system of a peculiar parasitic cnidarian Polypodium hydriforme: A phalloidin fluorescence study. Tissue Cell 2007, 39:79-87.
- [48]Rieger MR, Ladurner P: The significance of muscle cells for the origin of mesoderm in Bilateria. Int Comp Biol 2003, 43:47-54.
- [49]Reitzel AM, Daly M, Sullivan JC, Finnerty JR: Comparative anatomy and histology of developmental and parasitic stages in the life cycle of the lined sea anemone Edwardsiella lineata. J Parasitol 2009, 95:100-112.
- [50]Finnerty JR, Pang K, Burton P, Martindale MQ: Origins of bilateral symmetry: Hox and Dpp expression in a sea anemone. Science 2004, 304:1335-1337.
- [51]Ball EE, de Jong DM, Schierwater B, Shinzato C, Hayward DC, Miller DJ: Implications of cnidarian gene expression patterns for the origins of bilaterality: is the glass half full or half empty? Int Comp Biol 2007, 47:701-711.
- [52]de Jong DM, Hislop NR, Hayward DC, Reece-Hoyes JS, Pontynen PC, Ball EE, Miller DJ: Components of both major axial patterning systems of the Bilateria are differentially expressed along the primary axis of a “radiate” animal, the anthozoan cnidarian Acropora millepora. Dev Biol 2006, 298:632-643.
- [53]Manuel M: Early evolution of symmetry and polarity in metazoan body plans. C R Biol 2008, 332:184-209.
- [54]Collins AG, Schuchert P, Marques AC, Jankowski T, Medina M, Schierwater B: Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst Biol 2006, 55:97-115.
- [55]Savriama Y, Klingenberg CP: Beyond bilateral symmetry: geometric morphometric methods for any type of symmetry. BMC Evol Biol 2011, 11:280. BioMed Central Full Text
- [56]Palmer RA: Animal asymmetry. Curr Biol 2009, 19:R473-R477.
- [57]Sendino C, Zágoršek K, Taylor PD: Asymmetry in an Ordovician conulariid cnidarian. Lethaiain press
- [58]Dunn CW: Complex colony-level organization of the deep-sea siphonophore Bargmannia elongata (Cnidaria, Hydrozoa) is directionally asymmetric and arises by the subdivision of pro-buds. Dev Dyn 2005, 234:835-845.
- [59]Tang F, Bengtson S, Wang Y, Wang X, Yin C: Eoandromeda and the origin of Ctenophora. Evol Dev 2011, 13:408-414.
- [60]Palmer RA: Symmetry breaking and the evolution of development. Science 2004, 306:828-833.
- [61]Grande C: Left-right asymmetries in Spiralia. Integr Comp Biol 2010, 50:744-755.
- [62]Vandenberg LN, Levin M: Far from solved: a perspective on what we know about early mechanisms of left-right asymmetry. Dev Dyn 2010, 239:3131-3146.