Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica

Abstract

Tunicate embryos and larvae have small cell numbers and simple anatomical features in comparison with other chordates, including vertebrates. Although they branch near the base of chordate phylogenetic trees, their degree of divergence from the common chordate ancestor remains difficult to evaluate. Here we show that the tunicate Oikopleura dioica has a complement of nine Hox genes in which all central genes are lacking but a full vertebrate-like set of posterior genes is present. In contrast to all bilaterians studied so far, Hox genes are not clustered in the Oikopleura genome. Their expression occurs mostly in the tail, with some tissue preference, and a strong partition of expression domains in the nerve cord, in the notochord and in the muscle. In each tissue of the tail, the anteroposterior order of Hox gene expression evokes spatial collinearity, with several alterations. We propose a relationship between the Hox cluster breakdown, the separation of Hox expression domains, and a transition to a determinative mode of development.

Additional molecular support for the new chordate phylogeny

“…This genome compaction is also associated with a high rate of genomic evolution at the levels of both primary sequences Edvardsen et al, 2004) and genome organization (Holland and GibsonBrown, 2003). One of the most spectacular rearrangements of tunicate genomes is the lost of several Hox genes, the disintegration of the Hox cluster, and the lost of temporal colinearity in Hox gene expression during development (Ikuta et al, 2004;Seo et al, 2004). These observations raise the question of how tunicates, with their altered Hox clusters, are still able to develop a chordate body plan.…”

Organization of Hox genes in ascidians: Present, past, and future

“…The cluster organization of Hox genes has been investigated in a variety of chordates: larvacean (Seo et al, 2004), amphioxus (Garcia-Fernandez and Holland, 1994;Ferrier et al, 2000), lamprey (Force et al, 2002;Irvine et al, 2002), horn shark (Kim et al, 2000;Chiu et al, 2002), coelacanth (Koh et al, 2003), ray-fin fish, bichir (Chiu et al, 2004), zebrafish (Amores et al, 1998;Chiu et al, 2002), medaka (Misof and Wagner, 1996), cichlid (Malaga-Trillo and Meyer, 2001), puffer fish (Aparicio et al, 1997), newt (Belleville et al, 1992), mouse (Duboule and Dolle, 1989), and human (Acampora et al, 1989). Nonchordate Hox clusters have been reported with Drosophila (Lewis, 1978;Von Allmen et al, 1996), mosquito (Devenport et al, 2000;Powers et al, 2000), red flour beetle (Brown et al, 2002), silk moth (Ueno et al, 1992), a grasshopper (Ferrier and Akam, 1996), nematode, Caenorhabditis elegans (Wang et al, 1993;Van Auken et al, 2000), ribbon worm (Kmita-Cunisse et al, 1998), and sea urchin (Popodi et al, 1996;Martinez et al, 1999).…”

“…In the gut endoderm, the temporal correlation is also obscure (Ikuta et al, 2004). Fourth, in the mesoderm, ascidian Hox genes do not appear to achieve the coordinated expression, unlike Oikopleura Hox genes, in which Hox genes exhibit an expression pattern reminiscent of vertebrate collinear expression in the notochord (Seo et al, 2004). Ci-Hox2, 4, and 5 do not exhibit either spatially or temporally coordinated expression in the mesodermal tissues (Ikuta et al, 2004).…”

Evolution of the thyroid: Anterior–posterior regionalization of theOikopleuraendostyle revealed byOtx,Pax2/5/8, andHox1expression

“…Amphioxus has just one Pax2/5/8 gene, and most vertebrates have three paralogs (Pax2, Pax5, and Pax8), which likely arose during two rounds of whole genome duplication after the divergence of urochordate and vertebrate lineages (Kozmik et al, 1999;Dehal and Boore, 2005). Oikopleura, like ascidians and amphioxus, has a single Hox1 gene, in contrast to three found in vertebrates (Hoxa1, Hoxb1, Hoxd1), again arising in the vertebrate genome duplication events (Seo et al, 2004;Cañ estro et al, 2005;Dehal and Boore, 2005).…”