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, 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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    ABSTRACT: Genomic and transcriptomic analyses show that sponges possess a large repertoire of genes associated with neuronal processes in other animals, but what is the evidence these are used in a coordination or sensory context in sponges? The very different phylogenetic hypotheses under discussion today suggest very different scenarios for the evolution of tissues and coordination systems in early animals. The sponge genomic 'toolkit' either reflects a simple, pre-neural system used to protect the sponge filter or represents the remnants of a more complex signalling system and sponges have lost cell types, tissues and regionalization to suit their current suspension-feeding habit. Comparative transcriptome data can be informative but need to be assessed in the context of knowledge of sponge tissue structure and physiology. Here, I examine the elements of the sponge neural toolkit including sensory cells, conduction pathways, signalling molecules and the ionic basis of signalling. The elements described do not fit the scheme of a loss of sophistication, but seem rather to reflect an early specialization for suspension feeding, which fits with the presumed ecological framework in which the first animals evolved. © 2015. Published by The Company of Biologists Ltd.
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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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