Expression of a homologue of the fushi tarazu (ftz) gene in a cirripede crustacean

Abstract

In Metazoa, Hox genes control the identity of the body parts along the anteroposterior axis. In addition to this homeotic function, these genes are characterized by two conserved features: They are clustered in the genome, and they contain a particular sequence, the homeobox, encoding a DNA-binding domain. Analysis of Hox homeobox sequences suggests that the Hox cluster emerged early in Metazoa and then underwent gene duplication events. In arthropods, the Hox cluster contains eight genes with a homeotic function and two other Hox-like genes, zerknullt (zen)/Hox3 and fushi tarazu (ftz). In insects, these two genes have lost their homeotic function but have acquired new functions in embryogenesis. In contrast, in chelicerates, these genes are expressed in a Hox-like pattern, which suggests that they have conserved their ancestral homeotic function. We describe here the characterization of Diva, the homologue of ftz in the cirripede crustacean Sacculina carcini. Diva is located in the Hox cluster, in the same position as the ftz genes of insects, and is not expressed in a Hox-like pattern. Instead, it is expressed exclusively in the central nervous system. Such a neurogenic expression of ftz has been also described in insects. This study, which provides the first information about the Hoxcluster in Crustacea, reveals that it may not be much smaller than the insect cluster. Study of the Diva expression pattern suggests that the arthropod ftz gene has lost its ancestral homeotic function after the divergence of the Crustacea/Hexapoda clade from other arthropod clades. In contrast, the function of ftz during neurogenesis is well conserved in insects and crustaceans.

Hox genes and the crustacean body plan

“…The orthology relationship between Diva and ftz has been vindicated by further sequence and genomic analyses: it is indeed located between the Hox genes Scr and Antp in the Sacculina genome like its Drosophila counterpart. (34) Yet, the Sacculina ftz gene is expressed only in the CNS, in a few cells in each ganglion of the nerve cord, a pattern that recalls the late expression of ftz in Drosophila. Without expression in epidermis or in mesoderm, it is very unlikely that the Sacculina ftz gene could afford a typical homeotic function in morphogenetic differentiation.…”

Variation and constraint inHoxgene evolution

“…1A). ftz is expressed in the embryonic CNS in a broad range of arthropods, including myriapods (28)(29)(30), crustaceans (4,31), insects (14,23,24,26), and a distant lophotrochozoa, where the ftz ortholog Lox5 is expressed in the CNS (10,32). This CNS expression is conserved in arthropods with diverse Ftz sequences and early expression patterns (Fig.…”

Divergence évolutive extrême d’un gène homéotique : le cas bicoid

“…Une divergence évolutive aussi importante n'est pas un cas exceptionnel. Par exemple, toujours au sein du complexe Hox, le gène fushi tarazu a également perdu sa fonction homéotique chez les insectes et les crustacés [4,20,21]. De manière plus générale, la plasticité des mécanismes embryonnaires semble être bien supérieure à ce que l'on pensait lorsque, lors de leur découverte, les premiers gènes du développement fascinaient surtout par leur conservation entre des espèces très différentes.…”