Evolution of Antp-class genes and differential expression ofHydra Hox/paraHoxgenes in anterior patterning

Abstract

The conservation of developmental functions exerted by Antpclass homeoproteins in protostomes and deuterostomes suggested that homologs with related functions are present in diploblastic animals. Our phylogenetic analyses showed that Antp-class homeodomains belong either to non-Hox or to Hox͞paraHox families. Among the 13 non-Hox families, 9 have diploblastic homologs, Msx, Emx, Barx, Evx, Tlx, NK-2, and Prh͞Hex, Not, and Dlx, reported here. Among the Hox͞paraHox, poriferan sequences were not found, and the cnidarian sequences formed at least five distinct cnox families. Two are significantly related to the paraHox Gsx (cnox-2) and the mox (cnox-5) sequences, whereas three display some relatedness to the Hox paralog groups 1 (cnox-1), 9͞10 (cnox-3) and the paraHox cdx (cnox-4). Intermediate Hox͞paraHox genes (PG 3 to 8 and lox) did not have clear cnidarian counterparts. In Hydra, cnox-1, cnox-2, and cnox-3 were not found chromosomally linked within a 150-kb range and displayed specific expression patterns in the adult head. During regeneration, cnox-1 was expressed as an early gene whatever the polarity, whereas cnox-2 was up-regulated later during head but not foot regeneration. Finally, cnox-3 expression was reestablished in the adult head once it was fully formed. These results suggest that the Hydra genes related to anterior Hox͞paraHox genes are involved at different stages of apical differentiation. However, the positional information defining the oral͞aboral axis in Hydra cannot be correlated strictly to that characterizing the anterior-posterior axis in vertebrates or arthropods. T he discovery of structural and functional homologies between regulatory genes used by Drosophila and vertebrates during their development led to the hypothesis that animals would share a common set of genes for defining the head, trunk, and posterior regions at early developmental stages (1-6). The proposed genes were homeobox genes belonging either to the Antp class, like empty-spiracle (emx), even-skipped (evx), Hox genes, or to the Prd class, like orthodenticle (Otx), goosecoid. Phylogenetic analyses performed on a vast amount of Hox homeodomain (HD) sequences, including representatives from all classes of homeobox genes from animals, protozoa, fungi, and plants, confirmed the monophyly of the Antp class as well as its position as a sister group to the Paired class (7). Within the Antp class, the Hox gene organization is distinctive and enigmatic: the genes map in clusters, and the order of individual genes within a cluster correlates with their temporospatial expression pattern along the anterior-posterior body axis during development (8). Recently, it was proposed that the common bilaterian ancestor of protostomes and deuterostomes had at least seven Hox genes (9). However, the question of the composition of the ancestral HOX cluster remains open. Analysis of Hox homeobox sequences (10) suggested that the conserved HOX cluster emerged early in the evolution of metazoans from an original cluster harboring three ancestral g...

Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system

“…2I, arrow). This timing in the expression during head regeneration is very similar to that observed for the ANTP-class homeogene cnox-2 Gauchat et al (2000), hence TSP1 and cnox-2 can be considered as headspecific « early-late » regeneration genes. During budding, TSP1 transcripts were detected from stage 3 Otto and Campbell (1977) and onwards, in the most distal endodermal cells of the bud (Fig.…”

“…2D). In contrast, the ANTP-CLASS homeogene, msh Schummer et al (1992), Gauchat et al (2000) exhibits an expression pattern restricted to the ectodermal layer of the central part of the body column (Fig. 2B).…”

Reactivation of developmental programs: The cAMP-response element-binding protein pathway is involved in hydra head regeneration

“…Grafting experiments that measure the ability of the grafted regenerating tips to induce a secondary head in the host have shown that, after several hours of postcutting inhibition, head organizer activity is progressively reestablished at the regenerating tip (33). At the gene expression level, some genes are immediately turned on at the wound surface (named ''immediate genes''), whereas the ''immediate-early'' genes start to be expressed within the first 2 hours, most often in endodermal cells of the stump (14,21,34,35). Both immediate and immediate͞early genes are detected in head-and foot-regenerating stumps.…”

Hox, ParaHox, ProtoHox: facts and guesses

“…Again, phylogenetic analyses were puzzling: Evx genes fall basal to the Hox/ParaHox clade (Gauchat et al, 2000;Kourakis and Martindale, 2000). This position suggests that Evx appeared before the duplication event that generated the Hox/ParaHox primordial clusters.…”

“…This position suggests that Evx appeared before the duplication event that generated the Hox/ParaHox primordial clusters. The Mox class has rarely been included in phylogenetic analyses, and has vaguely been referred to as the missing ParaHox central gene (Gauchat et al, 2000;Hill et al, 2003). Two extensive phylogenetic analyses (BanerjeeBasu and Baxevanis, 2001;Minguilló n and GarciaFernàndez, 2003) suggest that Evx and Mox are closely related, forming a clade basal to the Hox/ParaHox group (Figure 4c).…”