The origin of patterning systems in bilateria-insights from the Hox and ParaHox genes in Acoelomorpha

Abstract

Hox and ParaHox genes constitute two families of developmental regulators that pattern the Anterior-Posterior body axis in all bilaterians. The members of these two groups of genes are usually arranged in genomic clusters and work in a coordinated fashion, both in space and in time. While the mechanistic aspects of their action are relatively well known, it is still unclear how these systems evolved. For instance, we still need a proper model of how the Hox and ParaHox clusters were assembled over time. This problem is due to the shortage of information on gene complements for many taxa (mainly basal metazoans) and the lack of a consensus phylogenetic model of animal relationships to which we can relate our new findings. Recently, several studies have shown that the Acoelomorpha most probably represent the first offshoot of the Bilateria. This finding has prompted us, and others, to study the Hox and ParaHox complements in these animals, as well as their activity during development. In this review, we analyze how the current knowledge of Hox and ParaHox genes in the Acoelomorpha is shaping our view of bilaterian evolution.

Figure 1

A. A consensus metazoan phylogenetic tree showing the relationships of all major clades. The Bilateria are subdivided into two major groups, the Acoelomorpha and the Nephrozoa (containing the superclades: Deuterostomia, Lophotrochozoa and Ecdysozoa). The Cnidaria is considered the sister group to the Bilateria. B. Diagrammatic view of the general morphology of Acoela from the dorsal side: st, statocyst (gravity receptor organ); cb, commissural brain; nc, nerve cords; mo, mouth opening; cp, central parenchyma or gut; pp, peripheral parenchyma; ep, epidermis. C. Adult specimen of Isodiametra pulchra under light microscope. The position of the statocyst is indicated by the arrow; arrowheads point to the developing eggs; the male and female copulatory organs are surrounded by the oval. D. Adult specimen of Symsagittifera roscoffensis under light microscope. The green cells correspond to the symbiotic algae Tetraselmis colvolutae. The position of the statocyst is indicated by the arrow; arrowheads point to the nerve cords.

Figure 2

S. roscoffensis BACs containing the anterior (A), central (B) and posterior (C) Hox genes harbor at least one copy of a class I TE (green) that belongs to the Ty3-Gypsy or Bel-Pao clades. Traces of ancient copies of TEs are also present (orange).

Figure 3

SrCdx expression patterns in juveniles (A and B) and adult specimens (C) of S. roscoffensis. In juveniles, SrCdx is mainly expressed in the nervous system. It labels thin nerve tracts running in parallel from the commissures around the statocyst along the AP body axis (arrowheads). In adults, expression is found around the male gonopore (arrows), in two rows of cells of peripheral parenchyma running along the AP axis, and in the central parenchyma. All pictures show a dorsal view, with the anterior to the left.

Figure 4

A model of the evolution of HOX and ParaHox clusters in metazoans from a single ProtoHox cluster after the divergence of Porifera. The model integrates data from recent phylogenetic studies in Cnidaria, and tries to combine the most parsimonious hypothesis for Hox–ParaHox evolution. A unique ANTP gene in the lineage leading to the C-BLCA duplicated several times in tandem, giving rise to an ancestral Hox–ParaHox gene cluster, which later split (broken line) and moved to different regions of the genome. Since orthologies between posterior Hox genes in cnidarians and bilaterians are still not clear, it is fair to suppose that cnidarian and bilaterian posterior Hox genes were produced independently in both lineages from the PPHox present in the C-BLCA. This gene duplicated in the C-BLCA, giving rise to two posterior Hox genes, one inherited by the CPHox and the other by the bilaterian lineage. These genes were the precursors of all the extant cnidarian and bilaterian (PG9/15) posterior Hox genes . In the lineage leading to the LCBA, another tandem duplication gave rise to the PG5 gene. From the LCBA, two sister-groups formed: one leading to present day acoelomorphs, and another giving rise to the NLCA. In the acoel lineage, the original cluster might have disintegrated (at least in S. roscoffensis) and some genes were lost (tentatively but not proven, the genes PG2, Gsx and Xlox), here represented by empty boxes. A similar process (yet to be proven) could have occurred in nemertodermatids, although the absence of anterior genes (empty boxes) is more probably the result of limited sampling. A further tandem duplication in the Nemertodermatida lineage originated a second PG5 gene. Finally, a series of tandem duplications, involving the central Hox class, gave rise to the extended HOX cluster present in the NLCA.