Making very similar embryos with divergent genomes: conservation of regulatory mechanisms of Otx between the ascidians Halocynthia roretzi and Ciona intestinalis

Development, Apr 2005

Izumi Oda-Ishii, Vincent Bertrand, Isao Matsuo, Patrick Lemaire, Hidetoshi Saiga

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Making very similar embryos with divergent genomes: conservation of regulatory mechanisms of Otx between the ascidians Halocynthia roretzi and Ciona intestinalis

Izumi Oda-Ishii 1 2 Vincent Bertrand 0 Isao Matsuo 1 Patrick Lemaire 0 Hidetoshi Saiga ) 2 0 LGPD, IBDM, Case 907, Campus de Luminy , F-13288 Marseille Cedex 09 , France 1 Head Organizer Project, Vertebrate Body Plan Group, RIKEN Center for Developmental Biology , 2-2-3 Minatojima Minamimachi, Chuou-Ku, Kobe, Hyougo 650-0047 , Japan 2 Department of Biological Sciences, Graduate School of Science, Tokyo Metropolitan University , 1-1 Minamiohsawa, Hachiohji, Tokyo 192-0397 , Japan of regulatory mechanisms of Otx between the ascidians - Ascidian embryos develop with a fixed cell lineage into simple tadpoles. Their lineage is almost perfectly conserved, even between the evolutionarily distant species Halocynthia roretzi and Ciona intestinalis, which show no detectable sequence conservation in the non-coding t regions of studied orthologous genes. To address how a en common developmental program can be maintained m without detectable cis-regulatory sequence conservation, p lo we compared in both species the regulation of Otx, a gene ev with a shared complex expression pattern. We found that e in Halocynthia, the regulatory logic is based on the use of D very simple cell line-specific regulatory modules, the activities of which are conserved, in most cases, in the Ciona In recent years, the ascidian larva has often been regarded as an organism close to the ancestral form of chordates, and has served as an interesting and informative model system for understanding the genesis of a simple chordate body plan (Satoh et al., 1996; Satoh et al., 2003). Halocynthia roretzi and Ciona intestinalis are representative species of the two orders, the Pleurogona and the Enterogona, which constitute the class Ascidiacea. Although these two classes probably diverged deep in the history of ascidian evolution, their embryos show remarkable similarity, with almost perfect conservation of the lineages up to the early gastrula stages. In addition, the recent cloning of a large number of genes in both species has shown a remarkable conservation of their embryonic expression profiles. This applies in particular to homeobox genes such as the Otx, Pax and Hox genes, which are expressed along the anteroposterior axis in the larval central nervous system (CNS) with distinct expression domains; these expression domains are also very similar to their vertebrate orthologs (Wada et al., 1998). The conservation of expression domains between ascidian species, and with vertebrates, raises the possibility of the conservation of regulatory logics within the chordate lineage. However, cross-species analysis of the activity of the embryo. The activity of each of these enhancer modules relies on the conservation of a few repeated crucial binding sites for transcriptional activators, without obvious constraints on their precise number, order or orientation, or on the surrounding sequences. We propose that a combination of simplicity and degeneracy allows the conservation of the regulatory logic, despite drastic sequence divergence. The regulation of Otx in the anterior endoderm by Lhx and Fox factors may even be conserved with vertebrates. regulatory regions of Ci-Hox3 in the mouse suggested lack of conservation (Locascio et al., 1999). Even between ascidians, two observations have been made that suggest a possible divergence of regulatory networks in spite of strikingly similar embryonic development. First, existing cDNA/EST and genomic data suggest a very poor sequence conservation between Halocynthia and Ciona. For example, the coding sequences of Halocynthia and Ciona Brachyury, a T-box gene specifically expressed in the notochord of both species, are remarkably different (Marcellini et al., 2003). Second, a previous report has suggested that Brachyury, may be regulated by very different mechanisms in Halocynthia and Ciona (Takahashi et al., 1999). To readdress the question of the conservation of the regulatory logic among ascidians, and with vertebrates, we chose Otx as a model, as it is one of the most phylogenetically conserved developmental genes. Otx/otd genes have been isolated from various animal species, including cnidaria, Drosophila, ascidians and vertebrates (Bally-Cuif et al., 1995; Finkelstein and Perrimon, 1991; Hudson and Lemaire, 2001; Li et al., 1994; Pannese et al., 1995; Simeone et al., 1993; Smith et al., 1999; Wada et al., 1996). They have the same expression domain, in the anterior part of embryos, suggesting the evolutionary conservation of essential roles in the formation and patterning of anterior embryonic territories. Consistently, Drosophila, mouse or ascidian embryos mutated or knocked down for Otx/otd genes exhibit defects in head structures, such as deletion or differentiation deficiency in the anterior central nervous system (CNS) (Acampora et al., 1996; Acampora et al., 1995; Ang et al., 1996; Finkelstein and Perrimon, 1991; Matsuo et al., 1995; Satou et al., 2001, Wada et al., 2004). In mouse embryos, the e (...truncated)


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Izumi Oda-Ishii, Vincent Bertrand, Isao Matsuo, Patrick Lemaire, Hidetoshi Saiga. Making very similar embryos with divergent genomes: conservation of regulatory mechanisms of Otx between the ascidians Halocynthia roretzi and Ciona intestinalis, Development, 2005, pp. 1663-1674, 132/7, DOI: 10.1242/dev.01707