Remodelling of the homeobox gene complement in the tunicate Oikopleura dioica

Edvardsen, Rolf B.; Seo, Hee-Chan; Jensen, Marit Flo; Mialon, Antoine; Mikhaleva, Jana; Bjordal, Marianne; Cartry, Jérôme; Reinhardt, Richard; Weissenbach, Jean; Wincker, Patrick; Chourrout, Daniel

doi:10.1016/j.cub.2004.12.010

Cited by 64 publications

(46 citation statements)

References 46 publications

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“…The larvacean six3/6 genes, therefore, are co-orthologs of ascidian six3/6, and are named six3/6a and six3/6b to reflect an independent duplication in the larvacean lineage. This finding is consistent with the expansion of several larvacean homeobox gene families, including the Six genes (Edvardsen et al, 2005).…”

Section: Development 132 (19)supporting

confidence: 88%

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

Bassham

Postlethwait

2005

Development

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The evolutionary origin of vertebrate placodes remains controversial because divergent morphologies in urochordates, cephalochordates and vertebrates make it difficult to recognize organs that are clearly homologous to placode-derived features, including the olfactory organ, adenohypophysis, lens, inner ear, lateral line and cranial ganglia. The larvacean urochordate Oikopleura dioica possesses organs that morphologically resemble the vertebrate olfactory organ and adenohypophysis. We tested the hypothesis that orthologs of these vertebrate placodes exist in a larvacean urochordate by analyzing the developmental expression of larvacean homologs of the placode-marking gene families Eya, Pitx and Six. We conclude that extant chordates inherited olfactory and adenohypophyseal placodes from their last common ancestor, but additional independent proliferation and perhaps loss of placode types probably occurred among the three subphyla of Chordata.

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Section: Development 132 (19)supporting

confidence: 88%

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

Bassham

Postlethwait

2005

Development

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“…This dataset covers the genome Ϸ14ϫ and virtually all the coding sequences Edvardsen et al, 2005). Several hits were found and assembled with the Cap program and part of the intron-exon organizations could be determined using alignments on expressed sequence tags.…”

Section: Cloning Of Oikopleura Chatmentioning

confidence: 99%

Development of the caudal nerve cord, motoneurons, and muscle innervation in the appendicularian urochordate Oikopleura dioica

Søviknes

Chourrout

Glover

2007

J of Comparative Neurology

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The development of the caudal nerve cord and muscle innervation in the appendicularian Oikopleura dioica was assessed using differential interference contrast and confocal microscopy, phalloidin staining of actin, and in situ hybridization for the neuronal markers tubulin and choline acetyltransferase (ChAT). The caudal nerve cord first appears as a stream of tubulin mRNA-positive neurons that extends into the tail from the caudal ganglion. By this stage a few actin-rich nerve fibers course longitudinally along the cord. As the tail lengthens, the caudal nerve cord extends and becomes more fasciculated and the neurons cluster at stereotyped longitudinal positions. The number of neurons in the nerve cord reaches a relatively stable maximum of about 29. A subset of neurons in the caudal ganglion and caudal nerve cord expresses ChAT mRNA. These putative motoneurons are distributed along nearly the full extent of the tail in numbers consistent with an independent innervation of each tail muscle cell. The longitudinal series of putative motoneurons is not aligned with the muscle cells, but peripheral nerve fibers extending to the muscle cells are, indicating that motor axons grow along the cord before exiting adjacent to their peripheral target. Muscle innervation occurs roughly coincident with the onset of ChAT mRNA expression. Our results provide the first molecular identification of motoneurons and the first developmental characterization of the motor system in an appendicularian and help set the stage for gene expression studies aimed at understanding the evolution of developmental patterning in this part of the chordate central nervous system.

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“…1). The serine/asparagine replacement observed at position 39 of the planarian Rx homeodomain probably represents a peculiarity of these organisms, shared only by Oikopleura dioica Rx (Edvardsen et al, 2005). Finally, planarian Rx do not show the 14 amino acid OAR domain identified in the C-terminal region of vertebrate and Drosophila Rx, and considered important for transactivation (Furukawa et al, 1997).…”

mentioning

confidence: 91%

Expression of a retinal homeobox (Rx) gene during planarian regeneration

Mannini¹,

Deri²,

Picchi³

et al. 2008

Int. J. Dev. Biol.

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Retinal homeobox (Rx) genes, with representatives in vertebrates and invertebrates, encode fundamental regulators of early eye and brain formation. Here we describe the spatiotemporal expression profile of a candidate planarian orthologue of Rx during regeneration in Dugesia japonica and Schmidtea mediterranea. Although low levels of Rx transcripts were found throughout the body of intact planarians, high levels of Rx expression were specific to regenerating tissue in both head and tail fragments. We also observed that Rx was never expressed in the simple rhabdomeric planarian eyes, supporting the notion that only formation of eyes that use the ciliary type of photoreceptors requires Rx function. KEY WORDS: paired-class homeobox gene, Rx, planarian, regeneration, eyeRx paired-type homeobox transcription factors have been isolated in several vertebrate and invertebrate species (Arendt et al., 2004; Bailey et al., 2004 and references therein;D'Aniello et al., 2006). A growing body of evidence suggests that Rx genes, early expressed in the anterior neural plate, are essential for the proliferation and specification of retina progenitor cells in chordates. In invertebrates, such as Drosophila, Rx does not seem to play a similar role. In fact, Drosophila Rx is not required for the formation of the visual system, but only for brain and clypeus development (Davis et al., 2003). In addition, an Rx ortholog of the annelid Platynereis has been found expressed in the ciliary photoreceptor cells of the brain, but not in the rhabdomeric photoreceptors of the larval and differentiating adult eyes (Arendt et al., 2004). Based on these observations, it has been proposed that an Rx ancestral function was related to the regulation of genes involved in brain development. During evolution, Rx genes became then essential for development of photoreceptors of ciliary type. No data are available on the function of Rx genes in a context different from the embryonic development, such as regeneration. Planarians (Platyhelminthes, Lophotrochozoa) offer a suitable model to investigate the role of Rx during regeneration. These organisms indeed can regenerate heads, including a complete brain, as well as other body parts in a short time, by virtue of the activity of adult stem cells, called neoblasts Saló 2006;Sánchez Alvarado, 2006). Planarian brain consists of two anterior cephalic ganglia connected to two ventral Int. J. Dev. Biol. 52: 1113-1117 (2008) nerve cords that run along the body (Cebrià, 2007). A pair of simple rhabdomeric eyes is generally located on its dorsal side. Despite the planarian central nervous system (CNS) seems quite simple at the morphological level, it possesses a functionally and molecularly complex structure (Cebrià, 2007 and references therein).We have cloned and sequenced the cDNA of a planarian Rx homolog in Dugesia japonica (GI strain) and Schmidtea mediterranea (asexual strain). Animals were maintained in autoclaved stream water at 18°C and starved for two weeks before being used in the experimen...

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Remodelling of the homeobox gene complement in the tunicate Oikopleura dioica

Cited by 64 publications

References 46 publications

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

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

Development of the caudal nerve cord, motoneurons, and muscle innervation in the appendicularian urochordate Oikopleura dioica

Expression of a retinal homeobox (Rx) gene during planarian regeneration

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