Animal Evolution: the Enigmatic Phylum Placozoa Revisited
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Current Biology Vol 15 No 1 R26 networks and have a very low turnover in 12. Rabut, G., Lenart, P., and Ellenberg, J. formation in Aspergillus is coupled to live mammalian cells. J. Cell Biol. 154, (2004). Dynamics of nuclear pore tubulin movement into the nucleus. Mol. 71–84. complex organization through the cell Biol. Cell 14, 2192–2200. 9. Rabut, G., Doye, V., and Ellenberg, J. cycle. Curr. Opin. Cell Biol. 16, 314–321. 17. Lenart, P., Rabut, G., Daigle, N., Hand, (2004). Mapping the dynamic 13. Goldberg, M.W., Rutherford, S.A., A.R., Terasaki, M., and Ellenberg, J. organization of the nuclear pore complex Hughes, M., Cotter, L.A., Bagley, S., (2003). Nuclear envelope breakdown in inside single living cells. Nat. Cell Biol. 6, Kiseleva, E., Allen, T.D., and Clarke, P.R. starfish oocytes proceeds by partial NPC 1114–1121. (2000). Ran Alters Nuclear Pore Complex disassembly followed by a rapidly 10. Walther, T.C., Alves, A., Pickersgill, H., Conformation. J. Mol. Biol. 300, 519–529. spreading fenestration of nuclear Loiodice, I., Hetzer, M., Galy, V., 14. Feldherr, C.M., Akin, D., and Cohen, R.J. membranes. J. Cell Biol. 160, 1055–1068. Hulsmann, B.B., Kocher, T., Wilm, M., (2001). Regulation of functional nuclear Allen, T., et al. (2003). The conserved pore size in fibroblasts. J. Cell Sci. 114, Nup107–160 complex is critical for Department of Biochemistry and 4621–4627. nuclear pore complex assembly. Cell 15. De Souza, C.P., Horn, K.P., Masker, K., Molecular Biology, Baylor College of 113, 195–206. Medicine, One Baylor Plaza, Houston, 11. Harel, A., Orjalo, A.V., Vincent, T., and Osmani, S.A. (2003). The Lachish-Zalait, A., Vasu, S., Shah, S., SONB(NUP98) nucleoporin interacts with Texas 77030, USA. Zimmerman, E., Elbaum, M., and Forbes, the NIMA kinase in Aspergillus nidulans. E-mail: [email protected] D.J. (2003). Removal of a single pore Genetics 165, 1071–1081. subcomplex results in vertebrate nuclei 16. Ovechkina, Y., Maddox, P., Oakley, C.E., devoid of nuclear pores. Mol. Cell 11, Xiang, X., Osmani, S.A., Salmon, E.D., DOI: 10.1016/j.cub.2005.36.29 853–864. and Oakley, B.R. (2003). Spindle Animal Evolution: The Enigmatic upper and a lower epithelium separated by the ‘fiber cell’ layer Phylum Placozoa Revisited (Figure 1B). The latter has a syncytial organization and its contractile properties are often A recent report of high levels of genetic variation between strains of assumed to be responsible for the Trichoplax adhaerens challenges the traditional view that the phylum amoeba-like changes in shape. Placozoa comprises only one species. At the morphological level, The upper layer consists of placozoans are amongst the simplest extant animals, but molecular monociliated ‘cover’ cells, evidence suggests that they may have more complex origins. whereas two cell types make up the lower epithelium — gland David J. Miller1* and [3], all that is known about it is cells, which are non-ciliated and Eldon E. Ball2 based on aquarium cultures. thought to secrete digestive Although T. adhaerens was until enzymes, and ciliated ‘cylinder’ Often described as the simplest now the sole recognized species cells that may be adhesive and known animal, the unassuming in the phylum Placozoa, the levels capable of resorbing digestion marine placozoan Trichoplax of molecular heterogeneity products [1]. Little is known about adhaerens is one of a handful of reported by Voigt et al. [4] the natural diet of Trichoplax, ‘lower’ metazoans that have so far reported in a recent issue of although it is assumed to consist defied being pigeonholed. Current Biology imply that what of micro-algae and organic The history of Trichoplax and has previously been considered detritus. In culture, they have its relatives has the elements of a one species may actually be been maintained for years on a scientific mystery story several. Cryptic molecular diet of Cryptomonas, which are (summarized in [1]). In 1971, Karl diversity thus underlies the more or less dissolved upon Grell [2] formally described a new apparently uniform morphology of contact with the gland cells. The Phylum, the Placozoa, to placozoans and, as the majority of morphology of the cylinder cells accommodate two species that the cell biological studies to date indicates that they are responsible had been reported a hundred have been based on a single for uptake of the dissolved years earlier. These were isolate from the Red Sea, this nutrients. Trichoplax sometimes originally greeted with excitement study highlights the need for elevate their center from the as ‘living fossils’ representing the further research on this enigmatic substrate to form one or more ancestral animal morphology. group of animals. digestive bags, and on glass However, the suggestion that substrates they frequently leave they were, in fact, modified Trichoplax Biology behind an area that is cleared of cnidarian larvae prompted a loss In culture, individual Trichoplax everything edible. of interest for the next fifty years. are flat and irregular disc-like One of the species upon which animals a few millimeters in Is Trichoplax Secondarily Simple? Placozoa was founded, diameter (environmental isolates Although it would be hard to Treptoplax reptans, has never are often smaller) and 10–15 µm imagine a simpler animal than been seen since its original thick (Figure 1A). Although Trichoplax, it is unclear whether it description, and is assumed not molecular studies point to had more complex ancestors, or to exist; T. adhaerens, on the additional cellular complexity (see whether its simplicity reflects its other hand, appears to be widely below), Trichoplax has been humble origins. Trichoplax has distributed and relatively common repeatedly described as some of the morphological in warm marine environments [1]. comprising just four cell types characteristics that are However, other than field surveys arranged in three layers — an considered to define higher Dispatch R27 animals, but not others. For example, the ectodermal cell junctions of Placozoa are similar to those of higher animals, but placozoan epithelia differ by their lack of a basal lamina. Grell’s original description of the phylum assumed a basal position amongst metazoans and implied that its simplicity is ancestral. However, according to recent molecular and morphological phylogenies [5,6] the Placozoa branch off after the ctenophores and sometimes the cnidarians, both of which are morphologically much more complex. Nevertheless, the issue is still controversial (e.g., [7]). If Trichoplax is secondarily simple, then it has lost typical animal features such as a nervous system, and there are intriguing hints that this may be the case. Only a few genes have been cloned from Trichoplax, but amongst these are several that are expressed in cnidarian nervous systems. In Trichoplax, these genes are expressed in small cells that are relatively evenly spaced in the marginal Figure 1. Trichoplax adhaerens, a simple amoeboid metazoan. zone and which do not appear to (A) A top view of an FITC-stained specimen (diameter about 1 mm) reveals the shiny spheres characteristically found in the upper epithelium as white dots. Reproduced correspond to any of the four with permission from [8]. (B) The four classically recognized cell types of Trichoplax: known cell types. For example, cover cells of the upper epithelium, fiber cells of the intermediate layer, and cylinder the placozoan homeobox gene cells and gland cells of the lower layer (modified after [1]). (C) Secp1, which encodes a Trox2 (Figure 1D) is clearly related putative small secreted protein, is expressed uniformly in the marginal zone, as shown to the Gsx/ind genes, which in the top view (upper panel), and in all three layers, as shown in the transverse function in dorso-ventral section (lower panel). Reproduced with permission from [14]. (D) The Gsx-type homeobox gene, Trox-2 is also expressed in the marginal zone, but in discrete cells patterning of the central nervous (unpublished photo, courtesy of B. Schierwater). (E) Another homeobox gene, Not, is system in higher animals and to expressed in folds in intact animals, as shown here, as well as in regenerating cnox2-Am from the cnidarian wounds. Reproduced with permission from [18]. (F) Birefringent granules, possibly of Acropora millepora, which is also calcitic calcium carbonate, are also limited to the marginal zone. Reproduced with differentially expressed in the permission from [13]. (G) The T-box transcription factor Brachyury is expressed in a nervous system [8–10]. Likewise few cells or groups of cells in the marginal outgrowth zones of large Trichoplax individuals. Reproduced with permission from [14]. Pax-B type genes are expressed in the Trichoplax marginal zone and in the cnidarian nervous example produces the calcium are lacking, it is unclear whether system [8,11]. Intriguingly, cells in carbonate skeleton in corals. the limits of the ‘marginal zone’ this marginal region also appear However, it is difficult to relate are the same for all genes. to express the neuropeptide this apparent similarity to the RFamide [12], which is the most overall structure of Trichoplax. The Placozoan Life Cycle — Are abundant neurotransmitter in Moreover, expression data for We Missing Something? cnidarians. These expression Brachyury genes cannot easily be In culture, placozoan reproduction patterns suggest a possible accommodated by the idea of a is overwhelmingly asexual and sensory function and that the correspondence between the occurs by binary fission. However, marginal zone of Trichoplax might ectoderm and marginal zone, as as Trichoplax cultures reach high correspond to the ectoderm of they are expressed in the densities and begin to degenerate, cnidarians. The presence in this Trichoplax marginal zone (Figure oocytes are developed. Under layer of birefringent granules 1G), but in the presumptive such conditions, small non- (Figure 1F) of what appears to be endoderm of cnidarians [14,15].