Ancestral role of caudal genes in axis elongation and segmentation

Abstract

caudal (cad͞Cdx) genes are essential for the formation of posterior structures in Drosophila, Caenorhabditis elegans, and vertebrates. In contrast to Drosophila, the majority of arthropods generate their segments sequentially from a posteriorly located growth zone, a process known as short-germ development. caudal homologues are expressed in the growth zone of diverse short-germ arthropods, but until now their functional role in these animals had not been studied. Here, we use RNA interference to examine the function of caudal genes in two short-germ arthropods, the crustacean Artemia franciscana and the beetle Tribolium castaneum. We show that, in both species, caudal is required for the formation of most body segments. In animals with reduced levels of caudal expression, axis elongation stops, resulting in severe truncations that remove most trunk segments. We also show that caudal function is required for the early phases of segmentation and Hox gene expression. The observed phenotypes suggest that in arthropods caudal had an ancestral role in axis elongation and segmentation, and was required for the formation of most body segments. Similarities to the function of vertebrate Cdx genes in the presomitic mesoderm, from which somites are generated, indicate that this role may also predate the origin of the Bilateria.caudal͞Cdx genes ͉ short-germ development ͉ Artemia ͉ Tribolium ͉ evolution T he caudal (cad͞Cdx) genes are homeobox genes involved in posterior patterning in diverse species (1-11). In early Drosophila embryos Caudal protein is distributed in a posterior to anterior concentration gradient that is needed for the activation of segmentation genes and segment formation in posterior parts of the animal. caudal mutant embryos have severe segmentation problems affecting posterior segments; in the most severely affected mutants, most abdominal segments are missing (1). This function of caudal is characteristic of long-germ development, found in Drosophila, where all of the body segments are molecularly determined during the blastoderm stage. This mode is thought to be evolutionarily derived within the higher insects and does not represent the ancestral mode of development (12). On the contrary, short-germ development is found in diverse and phylogenetically basal groups of insects and other arthropods, suggesting that this represents the ancestral mode for generating segments within the arthropods. In short-germ arthropods (which we take to include intermediate-germ species), only the most anterior segments are laid down in the blastoderm (e.g., Fig. 1A), whereas more posterior segments are generated sequentially from a posteriorly located presegmental zone, usually referred to as the ''growth zone '' (12-14). caudal homologues have been cloned in some short-germ arthropods and found to be expressed consistently in this presegmental zone (15-22), but until now their function in these species had not been studied.To explore the functional role of caudal genes in the growth zone of short-germ arthropods, we ...

Evolutionary conservation and divergence of the segmentation process in arthropods

“…Further research is required to solve the role of wg/Wnt in the growth zone of arthropods. Of equal interest is that also caudal (cad) is expressed in the posterior growth zone of short germ arthropods (Copf et al, 2004;Shinmyo et al, 2005;Chipman et al, 2004;AkiyamaOda and Oda, 2003;Damen, unpublished data). In the beetle Tribolium, the cricket Gryllus, and the brine shrimp Artemia cad is required in an early phase of segmentation for the formation of most body segments (Copf et al, 2004;Shinmyo et al, 2005).…”

“…Of equal interest is that also caudal (cad) is expressed in the posterior growth zone of short germ arthropods (Copf et al, 2004;Shinmyo et al, 2005;Chipman et al, 2004;AkiyamaOda and Oda, 2003;Damen, unpublished data). In the beetle Tribolium, the cricket Gryllus, and the brine shrimp Artemia cad is required in an early phase of segmentation for the formation of most body segments (Copf et al, 2004;Shinmyo et al, 2005). cad orthologs also are involved in the posterior addition of segments in annelids (de Rosa et al, 2005) and somites in vertebrates (e.g., van den Akker et al, 2002;Chawengsaksophak et al, 2004;Shimizu et al, 2005).…”

Predicting embryonic patterning using mutual entropy fitness and in silico evolution

“…The morphogen increases from anterior to posterior, in analogy with Caudal, which is conserved from insects to vertebrates and believed to be an ancestral morphogen in arthropods (Copf et al, 2004;Olesnicky et al, 2006).…”

Acoel development supports a simple planula-like urbilaterian

“…In an effort to compare the molecular zootype of a potential proxy for the urbilaterian to that proposed for the protostome-deuterostome ancestry (Slack et al 1993), we present the expression patterns of orthologues from two of the genes predicted to be 'posterior' patterning genes, even-skipped/evx (Patel et al 1992) and caudal/cdx (Wu & Lengyel 1998;Copf et al 2004;de Rosa et al 2005) in the acoel species Convolutriloba longifissura (Cl; figure 4). We show (figure 4a-d ) that ClEvx expression in the acoel is more similar to the pattern found in cnidarians and, at least in the hatchling, is expressed exclusively in distinct neurons of the brain anterior and posterior to the statocyst (figure 4b).…”