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The Evolution of Multicellularity and Early Animal Genomes Nina M Brooke and Peter WH Hollandã

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The Evolution of Multicellularity and Early Animal Genomes Nina M Brooke and Peter WH Hollandã 599 The evolution of multicellularity and early animal genomes Nina M Brooke and Peter WH Hollandà Several independent molecular datasets, including complete although some expressed sequence tag screens have mtDNA sequence, indicate that Choanozoa are most closely commenced (Hydra EST Database: http://hampson- related to multicellular animals. There is still confusion pc2.ics.uci.edu/blast/jf/; [1,2]) and gene-expression data concerning basal animal phylogeny, although recent data are accumulating (for cnidarians, these are being indicate that Placozoa are not degenerate cnidarians and hence assembled into a web-accessible database [3]). (along with sponges) occupy a pivotal position. The transition in evolution from diploblast to bilaterian animals is becoming better Models and mechanisms understood, with gene expression data arguing that cnidarians Some organisational principles are shared by different have forerunners of the anteroposterior and dorsoventral body groups of multicellular organisms, such as division of axes, and even a putative homologue of mesoderm. The labour, differentiation and cell communication. Wolpert homeobox and kinase gene families have been further analysed and Szathmary [4] propose that development from a single in basal animals, although more data are required to enable cell is an additional feature shared by all those multicellular detailed comparison with Bilateria. organisms that evolved complexity and diversity. Their reasoning is that an egg creates a genetic bottleneck in Addresses development, removing the potential for conflict between Department of Zoology, University of Oxford, South Parks Road, somatic cells, and allowing coordination to evolve. Oxford OX1 3PS, UK Ãe-mail: [email protected] When we consider molecular mechanisms responsible for that coordination, however, there is no reason to Current Opinion in Genetics & Development 2003, 13:599–603 suspect there will be much similarity between different multicellular lineages. After all, many different mole- This review comes from a themed issue on Genomes and evolution cules are suitable for use as signals, many types of Edited by Evan Eichler and Nipam Patel proteins could mediate adhesion or signal reception, and there are many ways to control differential gene 0959-437X/$ – see front matter expression. It is particularly strange, therefore, that ß 2003 Elsevier Ltd. All rights reserved. Lalucque and Silar [5] report a gene apparently confined DOI 10.1016/j.gde.2003.09.002 to multicellular eukaryotes, and absent from unicellular species, regardless of phylogenetic position. The function of the gene, NADPH oxidase, is unclear, but it may play a Abbreviations dpp Decapentaplegic role in signalling metabolic status between cells. Regard- GFP green fluorescent protein less of its function, however, the phylogenetic distribution mtDNA mitochondrial DNA is puzzling. Independent origins of the gene seems impos- PTK protein tyrosine kinase sible, horizontal transfer unlikely, and loss from unicel- rDNA ribosomal DNA lular taxa illogical because this represents the primitive condition. Further taxonomic sampling is needed to Introduction resolve the picture. Multicellularity has arisen many times in eukaryotic evolution, with independent origins in the lineages lead- Search for the metazoan ancestor ing to animals (Metazoa), green plants, fungi, cellular Over one hundred years ago it was proposed that slime moulds and several other taxa. To find molecular sponges, and by implication all Metazoa, evolved from changes that accompanied the evolution of multicellular- a group of unicellular protists, the choanoflagellates ity, it is necessary to compare genes or genomes between (Figure 2). This hypothesis, made on the basis of a multicellular organisms and their closest unicellular rela- striking structural resemblance of choanoflagellates to tives. Identifying these relatives is therefore an important the choanocyte cells of sponges, has been revisited with task; recent advances in this direction are discussed molecular phylogenetics. Primary sequence analysis of below. In addition, if we want to determine characters 18S rDNA failed to resolve the exact phylogenetic pla- shared across a multicellular group, we must compare cement of choanoflagellates, but protein-coding genes widely divergent species within that group, including are proving more informative. Snell et al. [6] cloned the descendants of the basal branches. For the Metazoa, this cytoplasmic hsp70 gene from a freshwater choanoflagel- means including data from sponges, placozoans (Figure 1), late, Monosiga ovata, and concluded that choanoflagel- cnidarians and ctenophores. Unfortunately, there are no lates are indeed closer to animals than fungi. King and complete genome sequences for any of these taxa, Carroll [7] isolated four additional protein-coding genes www.current-opinion.com Current Opinion in Genetics & Development 2003, 13:599–603 600 Genomes and evolution Figure 1 Figure 2 Trichoplax adhaerens (Phylum: Placozoa). Note the irregular shape, without defined polarity or axes of symmetry. Photograph kindly provided by Ana Sara Monteiro. from a marine choanoflagellate, M. brevicollis;theirana- lyses endorse the above conclusion, as does phylogenetic analysis of concatenated mitochondrial protein-coding genes by Lang et al. who sequenced the complete mito- chondrial genome of M. brevicollis [8].Burgeret al. [9] analysed gene content in this mtDNA genome, noting A choanoflagellate (Choanoeca perplexa). The species shown here is the presence of long intergenic regions and many more different from those discussed in the main text, but all choanoflagellate protein-coding genes than animal mtDNA. These species share structural similarities to the feeding cells of sponges. In authors suggest that mtDNA compaction, characteristic particular, notice the long central flagellum, surround by a collar of tentacles used to entrap bacteria. Individual bacterial cells can be of Metazoa, occurred concurrently with the origin of seen adhering to the collar. Photograph kindly provided by Barry multicellularity. Comparison of choanoflagellate, sponge Leadbeater. and Trichoplax mtDNA is needed to test this hypothesis. The choanoflagellates comprise part of the phylum Choanozoa, a diverse group also including some non- The position of the phylum Placozoa, represented by flagellateandamoeboidprotists[10]. Ministeria vibrans is Trichoplax adhaerens, is particularly relevant to discussions a stellate, apparently nonflagellate marine protozoan, about metazoan origins, because of its morphological which has been placed on the basis of morphology simplicity (Figure 1). A recent paper by Cavalier-Smith alongside the filose amoebae Nuclearia sp. in the Class and Chao [11], based upon primary sequence of 18S Cristidiscoidea. 18S rDNA phylogenies from Cavalier- rDNA, places Trichoplax either as a sister group to Cni- Smith and Chao [11] strongly challenge this view and daria, or even within the Cnidaria close to Medusozoa place Ministeria as sister either to the choanoflagellates or (comprising Hydrozoa, Scyphozoa, and Cubozoa). These to animals. authors suggest that Trichoplax may have evolved from a scyphozoan (jellyfish) ancestor. This seems unlikely, how- Phylogeny of basal animals ever, in the light of two novel and informative molecular There is still much confusion concerning the early evolu- characters studied by Ender and Schierwater [14]. These tionary history of animals, and morphological characters researchers report that Trichoplax possesses a circular often contradict molecular data [12]. Aleshin and Petrov mtDNA molecule, plesiomorphic with all metazoans, [13] analysed the variable V7 and V2 regions of 18S rRNA including basal Cnidaria (Anthozoa), whereas medusozo- and coded secondary structure characters for cladistic ans possess linear mtDNA molecules. Their second mar- analysis. They suggest that Cnidaria are a sister group ker, the predicted secondary structure of 16S rRNA, shows to the Bilateria, that Ctenophora and Porifera (sponges) great disparity between Placozoa and Cnidaria with may be earlier derivatives of Metazoa, and that Placozoa respect to the number and length of stem and loop regions. have a close affiliation with Cnidaria. It seems unlikely that Trichoplax is a derived cnidarian. Current Opinion in Genetics & Development 2003, 13:599–603 www.current-opinion.com The evolution of multicellularity and early animal genomes Brooke and Holland 601 Whereas Trichoplax remains a key animal for understand- conclusion is tentative until further comparative and func- ing the evolution of multicellularity, the same is not true tional analyses are conducted; indeed, Scholz and Tech- for Myxozoa. Once thought to be protists, and then nau [21] report a somewhat different expression for elevated to within the basal animals, a recent finding Brachyury in another cnidarian (an anthozoan or sea ane- supports the view that they are actually highly degenerate mone, Nematostella), including exclusion from the differ- bilaterians. Monteiro et al. [15] found that the 18S rDNA entiated mesenteric muscle tissue. The two studies are not sequence of one myxozoan is almost identical to that of a necessarily contradictory, however, because the Podocoryne rare and enigmatic worm, known as Buddenbrockia. Find- work included the medusa stage, while the Nematostella ing a myxozoan with muscles and a worm-like body (i.e. work studied the polyp stage only (medusae being absent Buddenbrockia) strongly indicates
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