Molecular evidence from Ciona intestinalis for the evolutionary origin of vertebrate sensory placodes

Abstract

Cranial sensory placodes are focused areas of the head ectoderm of vertebrates that contribute to the development of the cranial sense organs and their associated ganglia. Placodes have long been considered a key character of vertebrates, and their evolution is proposed to have been essential for the evolution of an active predatory lifestyle by early vertebrates. Despite their importance for understanding vertebrate origins, the evolutionary origin of placodes has remained obscure. Here, we use a panel of molecular markers from the Six, Eya, Pax, Dach, FoxI, COE and POUIV gene families to examine the tunicate Ciona intestinalis for evidence of structures homologous to vertebrate placodes. Our results identify two domains of Ciona ectoderm that are marked by the genetic cascade that regulates vertebrate placode formation. The first is just anterior to the brain, and we suggest this territory is equivalent to the olfactory/adenohypophyseal placodes of vertebrates. The second is a bilateral domain adjacent to the posterior brain and includes cells fated to form the atrium and atrial siphon of adult Ciona. We show this bares most similarity to placodes fated to form the vertebrate acoustico-lateralis system. We interpret these data as support for the hypothesis that sensory placodes did not arise de novo in vertebrates, but evolved from pre-existing specialised areas of ectoderm that contributed to sensory organs in the common ancestor of vertebrates and tunicates.

The evolutionary history of placodes: a molecular genetic investigation of the larvacean urochordate Oikopleura dioica

“…Because of the importance of synchronizing sexual maturation and reproductive behavior, the systems for collecting olfactory information, including sex pheromones, and for eliciting maturational and behavioral changes could have been anciently linked (Muske, 1993). Because ascidian pitx is not expressed in the part of the duct proximal to the brain and because vertebrate Pitx is eventually downregulated in the olfactory organ, Boorman and Shimeld (Boorman and Shimeld, 2002) tentatively proposed that the ascidian duct could be homologous to the olfactory component of a combined adenohypophyseal/olfactory organ; this hypothesis, similar to that of Burighel et al (Burighel et al, 1998), implies a conflation of organs in ascidians that is at odds with the separate olfactory and adenophypophyseal homologies that we propose in Oikopleura dioica and Mazet et al (Mazet et al, 2005) propose for ascidians.…”

“…The idea that a single organ served for both olfaction and hormone regulation in a chordate ancestor and that this organ split into separate olfactory and pituitary organs in vertebrates (Gorbman, 1995) is weakened by the existence of separate probable olfactory and adenohypophyseal organs in Oikopleura, and by the finding of Whitlock et al (Whitlock et al, 2003) that cells of the terminal nerve that produce GnRH (otherwise a hormone of the pituitary) are products of neural crest rather than the olfactory placode, as was originally thought. Mazet et al (Mazet et al, 2005) recently proposed that the ascidian palps might be an olfactory organ homolog, based on expression of eya and neuronal marker COE; it seems likely, on the basis of gene expression and topography, that the Oikopleura ventral organ placode is homologous to the ectoderm of the ascidian palps, although, unlike the larvacean ventral organ, no ciliated sensory cells have been identified on the palps. Other olfactory markers in non-vertebrate chordates should be analyzed to resolve these apparent differences among chordates.…”

“…Evidence in favor of an ancient, eochordate origin for placodes, however, has come from analysis of ascidian and cephalochordate molecular embryology (Baker and BronnerFraser, 1997;Holland and Holland, 2001;Manni et al, 2004b;Mazet et al, 2005;Shimeld and Holland, 2000). For example, ascidians have been proposed to possess an otic placode homolog: the paired, thickened, ectodermal primordia of the exhalent siphon (atrium) in Ciona embryos express Pax2/5/8, an ascidian ortholog of the vertebrate otic placode-marking genes Pax2 and Pax8 (Wada et al, 1998), and the adult atrium wall contains 'cupular' cells that are morphologically similar to hair cells of the vertebrate inner ear and lateral line (Bone and Ryan, 1978).…”

Retinoic acid signaling in development: Tissue‐specific functions and evolutionary origins

“…It is thus interesting to assess, whether RA signaling affects the development of these invertebrate tissues. Such tissues include, for example, the adhesive papillae (or palps) in the anteriormost general ectoderm of ascidians, which is thought to be homologous either to the vertebrate olfactory placode (Mazet et al, 2005) or to vertebrate cement and hatching glands (Manni et al, 2004). The vertebrate cement and hatching glands might not be placodes in a strict sense, because they do not share a common developmental origin with placodes (reviewed in Schlosser, 2005).…”

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

“…Comparative analyses of the expression patterns of endostyle genes (e.g., Tpo, Pax2/5/8,FoxE4,FoxQ1,FoxA, in amphioxus and ascidians help us to understand the evolutionary origin of the vertebrate thyroid (Kozmik et al, 1999;Ogasawara et al, 1999;Ristoratore et al, 1999;Venkatesh et al, 1999;Ogasawara, 2000;Murakami et al, 2001;Ogasawara and Satou, 2003;Sasaki et al, 2003;Hiruta et al, 2005;Mazet et al, 2005). Results show that a combinatorial code of molecular markers defines each zone of the endostyle across its dorsoventral axis (Hiruta et al, 2005).…”