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Current 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. 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., , (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. 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 and 4621–4627. nuclear pore complex assembly. Cell 15. De Souza, C.P., Horn, K.P., Masker, K., , 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 165, 1071–1081. subcomplex results in nuclei 16. Ovechkina, Y., Maddox, P., Oakley, C.E., devoid of nuclear pores. Mol. Cell 11, Xiang, X., Osmani, S.A., , E.D., DOI: 10.1016/j.cub.2005.36.29 853–864. and Oakley, B.R. (2003). Spindle

Animal : The Enigmatic upper and a lower separated by the ‘fiber cell’ layer 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 adhaerens challenges the traditional view that the phylum -like changes in shape. Placozoa comprises only one . At the morphological level, The upper layer consists of placozoans are amongst the simplest extant , 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 ‘’ Often described as the simplest now the sole recognized species cells that may be adhesive and known , the unassuming in the phylum Placozoa, the levels capable of resorbing 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- and organic The history of Trichoplax and has previously been considered . 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, . Trichoplax sometimes originally greeted with excitement study highlights the need for elevate their center from the as ‘living ’ representing the further research on this enigmatic 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 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 . 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 , and there are intriguing hints that this may be the case. Only a few 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 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 , 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, -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 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 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]. -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 . 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 Cycle — Are abundant neurotransmitter in Moreover, expression for We Missing Something? cnidarians. These expression Brachyury genes cannot easily be In culture, placozoan patterns suggest a possible accommodated by the of a is overwhelmingly asexual and sensory function and that the correspondence between the occurs by binary fission. However, marginal zone of Trichoplax might 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 of cnidarians [14,15]. flagellated round cells believed to calcitic calcium carbonate [13] As morphological landmarks represent appear in the also suggests similarities with the delimiting the marginal zone (e.g. intermediate cell layer of some cnidarian ectoderm, which for a mesogloea or a basal lamina) individuals. Ova are set free when Current Biology Vol 15 No 1 R28 the mother animal disintegrates, evolutionary pedigree of the 5. Collins, A.G. (2002). Phylogeny of and the evolution of and in some cases they have Placozoa. The sequence cnidarian life cycles. J. Evol. Biol. 15, already started to divide, but could provide clues to life style, 418–432. division has never been seen to and perhaps facilitate ‘closing’ the 6. Peterson, K.J., and Ernisse, D.J. (2001). Animal phylogeny and the ancestry of proceed beyond the 64-cell stage, life cycle, which will almost bilaterians: inferences from morphology and the developing certainly be necessary in and 18S rDNA gene sequences. Evol. Dev. 3, 170–205. eventually fragments [1]. evaluating possible relationships 7. Ender, A., and Schierwater, B. (2003). Fertilization and the completion of between the cell layers of Placozoa are not derived cnidarians: have placozoans, cnidarians and higher Evidence from molecular morphology. Mol. Biol. Evol. 20, 130–134. never been observed, but the animals. 8. Jakob, W., Sagasser, S., Dellaporta, S., reasons for this are not clear. Holland, P., Kuhn, K., and Schierwater, B. (2004). The Trox-2 Hox/ParaHox gene Rather than this being a failure in Variation within T. adhaerens of Trichoplax (Placozoa) marks an culture conditions, perhaps The evasiveness of the long- epithelial boundary. Dev. Genes Evol. development can begin without missing Treptoplax and the 214, 170–175. 9. Weiss, J.B., Von Ohlen, T., Mellerick, fertilization but is then not morphological homogeneity of D.M., Dressler, G., Doe, C.Q., and Scott, completed. When an embryo does Trichoplax isolates have led to M.P. (1998). Dorsoventral patterning in the central nervous system: develop, will we recognize the Phylum Placozoa being regarded the intermediate neuroblasts defective resulting , or is there a life as monotypic, but the new homeobox gene specifies intermediate column identity. Genes Dev. 12, cycle stage that has not previously observations clearly contradict 3591–3602. been recognized as Trichoplax? this view [4]. Trichoplax appears to 10. Hayward, D.C., Catmull, J., Reece-Hoyes, Perhaps, like the mesozoans with be found throughout the tropics, J.S., Berghammer, H., Dodd, H., Hann, S.J., , D.J., and Ball, E.E. (2001). which Trichoplax has sometimes and natural isolates are generally Gene structure and larval expression of been grouped, there is a parasitic below the size threshold (about 1 cnox-2Am from the . Dev. Genes Evol. 211, 10–19. stage that requires an intermediate mm) above which significant 11. Kozmik, Z., Daube, M., Frei, E., Norman, for completion of the life biogeographic structuring is to be B., Kos, L., Dishaw, L.J., Noll, M., and Piatigorsky, J. (2003). Role of cycle.The view that placozoans expected [17]. Hence, minimal in evolution: a cnidarian PaxB gene represent an aberrant hydrozoan genetic variation would be uniting Pax2 and Pax6 functions. Dev. is clearly incorrect as, expected. However, Voigt et al. [4] Cell 5, 773–785. 12. Schuchert, P. (1993). Trichoplax like anthozoans but unlike other detected surprising levels of adhaerens (Phylum Placozoa) has cells cnidarians, the mitochondrial heterogeneity amongst the 31 that react with against the neuropeptide RFamide. Acta Zool. 74, genome of Trichoplax is animal- isolates — for example, eight 115–117. like, i.e. circular and relatively small different mitochondrial 16S 13. Pearse, V.B., Uehara, T., and Miller, R.L. [7]. However, the possibility that haplotypes were identified, varying (1994). Birefringent granules in placozoans (Trichoplax adhaerens). placozoans are descended from a in length by up to 145 bp. As yet, Trans. Am. Microsc. Soc. 113, 385–389. neotenic anthozoan larva may still we have no real idea of how 14. Martinelli, C., and Spring, J. (2003). Distinct expression patterns of the two be worthy of consideration. variable Trichoplax is — the high T-box homologues Brachyury and levels of variation detected at each Tbx2/3 in the placozoan Trichoplax adhaerens. Dev. Genes Evol. 213, Genomics of Lower Animals of four loci thus far probably 492–499. With a genome size of around represent the tip of the iceberg, as 15. Scholz, C.B., and Technau, U. (2003). 40 Mb [16] — a little over 3 the number of isolates studied The ancestral role of Brachyury: Expression of NemBra1 in the basal that of yeast (12 Mb) and just 10 was small. Hopefully, more cnidarian vectensis. Dev. times that of E. coli (4 Mb) — T. comprehensive surveys of Genes Evol. 212, 563–570. 16. Ruthmann, A. (1977). Cell differentiation, adhaerens has the smallest variation are in progress, and it will DNA content and of genome of all animals surveyed to be fascinating to see if molecular Trichoplax adhaerens F. E. Schulze. date. In 2005, the complete variation within the Placozoa Cytobiologie 15, 58–64. 17. Finlay, B.J. (2002). Global dispersal of genome sequences of Trichoplax approaches that within phyla such free-living microbial species. and of the Reniera are as the Nematoda, which are also Science 296, 1061–1063. 18. Martinelli, C., and Spring, J. (2004). scheduled for determination by characterized by very limited Expression pattern of the homeobox the U.S. Department of ’s morphological diversity. gene Not in the basal metazoan Joint Genome Institute (JGI). In Trichoplax adherns. Gene Expression References Patterns 4, 443–447. addition, the availability of several 1. Grell, K.G., and Ruthman, A. (1991). complete cnidarian genome Placozoa. In Microscopic of 1Comparative Genomics Centre, sequences will provide a much , Vol.2: Placozoa, Porifera, Molecular Sciences Building 21, James and , F.W. Harrison better understanding of the basic and J. A. Westfall, eds. (New York: Wiley- Cook University, Townsville, metazoan gene complement. At Liss), pp. 13–27. Queensland 4811, Australia. 2Centre for present, the phylogenetic 2. Grell, K.G. (1971). Trichoplax adhaerens: the Molecular Genetics of Development F.E. Schulze und die Entstehung der and Molecular Genetics and Evolution relationships at the base of the Metazoen. Naturwiss. Rundschau 24, Group, Research School of Biological Metazoa are essentially 160–161. 3. Maruyama, Y.K. (2004). Occurrence in Sciences, Australian National University, unresolved, but with the pending the field of a long-term, year-round, P.O. Box 475, Canberra, ACT 2601, complete genome sequences in stable population of placozoans. Biol. Australia. Bull. 206, 55–60. *E-mail: [email protected] hand, it should be possible to 4. Voigt, O., Collins, A.G., Buchsbaum reconstruct the phylogeny of the Pearse, V., Pearse, J.S., Ender, A., Hadrys, H., and Schierwater, B. (2004). ‘lower’ Metazoa and to Placozoa: no longer a phylum of one. unequivocally establish the Curr. Biol. 14, R944–R945. DOI: 10.1016/j.cub.2005.36.30