Expansion, diversification, and expression of T-box family genes in Porifera

Department of Biology, University of Richmond, 28 Westhampton Way, Richmond, VA, 23173, USA.
Development Genes and Evolution (Impact Factor: 2.44). 11/2010; 220(9-10):251-62. DOI: 10.1007/s00427-010-0344-2
Source: PubMed


Sponges are among the earliest diverging lineage within the metazoan phyla. Although their adult morphology is distinctive, at several stages of development, they possess characteristics found in more complex animals. The T-box family of transcription factors is an evolutionarily ancient gene family known to be involved in the development of structures derived from all germ layers in the bilaterian animals. There is an incomplete understanding of the role that T-box transcription factors play in normal sponge development or whether developmental pathways using the T-box family share similarities between parazoan and eumetazoan animals. To address these questions, we present data that identify several important T-box genes in marine and freshwater sponges, place these genes in a phylogenetic context, and reveal patterns in how these genes are expressed in developing sponges. Phylogenetic analyses demonstrate that sponges have members of at least two of the five T-box subfamilies (Brachyury and Tbx2/3/4/5) and that the T-box genes expanded and diverged in the poriferan lineage. Our analysis of signature residues in the sponge T-box genes calls into question whether "true" Brachyury genes are found in the Porifera. Expression for a subset of the T-box genes was elucidated in larvae from the marine demosponge, Halichondria bowerbanki. Our results show that sponges regulate the timing and specificity of gene expression for T-box orthologs across larval developmental stages. In situ hybridization reveals distinct, yet sometimes overlapping expression of particular T-box genes in free-swimming larvae. Our results provide a comparative framework from which we can gain insights into the evolution of developmentally important pathways.

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    • "The attractiveness of this model, which was highlighted by Yoko Watanabe through the film 'Life of the freshwater sponge' (Tokyo Film Corporation http://tokyocinema.net/EnglVieo.htm), has led to more recent studies on signalling and coordination of sponge behaviour (Elliott and Leys, 2007; Elliott and Leys, 2010), epithelia (Leys et al., 2009; Adams, 2010), patterning (Windsor and Leys, 2010) and most recently, sensory cells (Ludeman et al., 2014). And since freshwater sponges are easily obtained and cultured in Europe, Japan and North America, there is a body of knowledge on the genetics of development (Richelle-Maurer et al., 1998; Richelle- Maurer and Van de Vyver, 1999; Nikko et al., 2001; Funayama et al., 2005a; Funayama et al., 2005b; Mohri et al., 2008; Funayama et al., 2010; Holstien et al., 2010; Funayama, 2013) and even the possibility of using RNA interference methods (Rivera et al., 2011). Typically, gemmules are collected during winter months and kept refrigerated to hatch as needed in the lab, but it is also possible to keep a population over the long term by returning hatched batches to lakes. "
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    • "The availability of full genomic sequences for numerous animal species has confirmed the nearly ubiquitous representation of Brachyury and other Tbx genes throughout different phyla. For example, single-copy Brachyury and Tbx2/3 orthologs have been reported in the placozoan Trichoplax adhaerens [93] and Brachyury and other Tbx genes have been described in sponges (e.g., [94]). Likewise, Brachyury and Tbx2/3 orthologs have been reported in Pleurobrachia pileus, a member of Ctenophora (comb jellies), one of the first metazoan phyla [95]. "
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