Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity

Abstract

Demosponges are considered part of the most basal evolutionary lineage in the animal kingdom. Although the sponge body plan fundamentally differs from that of other metazoans, their development includes many of the hallmarks of bilaterian and eumetazoan embryogenesis, namely fertilization followed by a period of cell division yielding distinct cell populations, which through a gastrulation-like process become allocated into different cell layers and patterned within these layers. These observations suggest that the last common ancestor (LCA) to all living animals was developmentally more sophisticated than is widely appreciated and used asymmetric cell division and morphogen gradients to establish localized populations of specified cells within the embryo. Here we demonstrate that members of a range of transcription factor gene classes, many of which appear to be metazoan-specific, are expressed during the development of the demosponge Reniera, including ANTP, Pax, POU, LIM-HD, Sox, nuclear receptor, Fox (forkhead), T-box, Mef2, and Ets genes. Phylogenetic analysis of these genes suggests that not only the origin but the diversification of some of the major developmental metazoan transcription factor classes took place before sponges diverged from the rest of the Metazoa. Their expression during demosponge development suggests that, as in today's sophisticated metazoans, these genes may have functioned in the regulatory network of the metazoan LCA to control cell specification and regionalized gene expression during embryogenesis.

Early origin of the bilaterian developmental toolkit

“…Moreover, based on a comparison of the intergenic regions within the NK homeobox cluster of Amphimedon, Fahey et al (2008) propose that demosponges possess more limited regulatory machinery than eumetazoans. Thus, the last common ancestor of all metazoa was able to specify multiple cell types, establish body axes and array different cell types along these axes and produce multicellular structures (Larroux et al 2006), but evidently lacked the regulatory complexity and depth of transcription factors and microRNAs required to produce complex gene regulatory networks (GRNs), and thus more complex morphological structures.…”

“…The Wnt/catenin and TGF-b pathways provide axial and D/V patterning (Adamska et al 2007). Other transcription factors have been identified, including a variety of ANTP (HOX), Pax, POU, T-box, Sox, Mef2, PRD and LIM class genes; some are expressed in specific tissues and thus establish regionalized domains of gene expression (Muller et al 2004;Larroux et al 2006Larroux et al , 2008. Complicating the issue is that demosponges have almost certainly lost a number of transcription factors, including NK and ANTP genes There are, however, important differences between demosponges and eumetazoans: there are relatively few genes within each class of transcription factors; the expansion of most of classes occurred after the origin of the demosponges (Kusserow et al 2005;Simionato et al 2007).…”

Ancient linkage of a POU class 6 and an anterior hox‐like gene in cnidaria: implications for the evolution of homeobox genes

“…POU domain proteins also interact with transcription factors of the same or unrelated families like the SOX proteins, thereby controlling gene expression from various DNA enhancers in a combinatorial fashion, which is thought to provide a higher level of functional diversity (Remenyi et al, 2004). POU genes play important roles in many developmental systems, notably in the nervous system (Zhou et al,'96;Latchman,'99), and they have been detected in virtually all metazoan taxa, including Cnidaria and sponges (Seimiya et al, '97;Shah et al, 2000;Larroux et al, 2006;Ryan et al, 2006). On the basis of sequence similarity of the POU domain six subclasses are recognized commonly (Ryan and Rosenfeld,'97).…”

Le génome de l’épongeAmphimedon queenslandicanous aide à reconstruire notre ancêtre précambrien

“…En revanche, pendant le déve-loppement embryonnaire, une éponge est plus évidemment animale. Le plan d'organisation de la larve parenchymella d'Amphimedon est clairement radiaire et environ onze types de cellules sont organisés en trois couches cellulaires le long de l'axe de symétrie (Figure 2) (Figure 1) [4,5]. Plus tard, une importante diversification de toutes les classes de facteurs de transcription a conduit à un ancêtre eumétazoaire avec un complément de gènes très similaire à celui de l'ancê-tre bilatérien [5][6][7][8].…”

“…L'objectif était d'avoir une idée de la fonction hypothétique d'un gène chez l'ancêtre métazoaire [4]. L'expression des composants des voies de signalisation a suggéré que l'on pouvait retrouver chez l'ancêtre métazoaire des rôles similaires à ceux des bilaté-riens.…”