The ascidian homolog of the vertebrate homeobox gene Rx is essential for ocellus development and function

D’Aniello, Salvatore; D’Aniello, Enrico; Locascio, Annamaria; Memoli, Alessandra; Corrado, Marcella; Russo, Monia Teresa; Aniello, Francesco; Fucci, Laura; Brown, Euan R.; Branno, Margherita

doi:10.1111/j.1432-0436.2006.00071.x

Cited by 48 publications

(43 citation statements)

References 56 publications

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“…Similar to what has been demonstrated in vertebrates, we found that Ciona ocellus development is dependent on Rx gene function (D'Aniello et al, 2006). Electrophysiological measurements under variable light conditions indicate these Rx-deficient Ciona larvae did not show any light dependent changes in their electrical activity and had a corresponding altered ability to swim spontaneously with respect to control larvae (D'Aniello et al, 2006).…”

Section: Introductionsupporting

confidence: 85%

“…Photoreceptor cells in Ciona exhibit both morphological (ciliary type) (Gorman et al, 1971) and electrophysiological characteristics (hyperpolarization in response to the light) similar to those of vertebrate photoreceptor cells (unpublished data). Furthermore, the ocellus has a photosensitive function during the larval stage, which has been proposed to be ancestral to vertebrate eyes (D'Aniello et al, 2006;Horie et al, 2008;Sakurai et al, 2004;Tsuda et al, 2003). That the Ciona ocellus and its photoreceptors are homologous to the vertebrate eye is also suggested by the similarity of Ci-Opsin1 to the vertebrate ciliary opsin subfamily (Kusakabe et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

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Onecut is a direct neural-specific transcriptional activator of Rx in Ciona intestinalis

D’Aniello

Pezzotti

Locascio

et al. 2011

Developmental Biology

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Retinal homeobox (Rx) genes play a crucial and conserved role in the development of the anterior neural plate of metazoans. During chordate evolution, they have also acquired a novel function in the control of eye formation and neurogenesis. To characterize the Rx genetic cascade and shed light on the mechanisms that led to the acquisition of this new role in eye development, we studied Rx transcriptional regulation using the ascidian, Ciona intestinalis. Through deletion analysis of the Ci-Rx promoter, we have identified two distinct enhancer elements able to induce Ci-Rx specific expression in the anterior part of the CNS and in the photosensory organ at tailbud and larva stages. Bioinformatic analysis highlighted the presence of two Onecut binding sites contained in these enhancers, so we explored the role of this transcription factor in the regulation of Ci-Rx. By in situ hybridization, we first confirmed that these genes are co-expressed in the same cells. Through a series of in vivo and in vitro experiments, we then demonstrated that the two Onecut sites are responsible for enhancer activation in Ci-Rx endogenous territories. We also demonstrated in vivo that Onecut misexpression is able to induce ectopic activation of the Rx promoter. Finally, we demonstrated that Ci-Onecut is able to promote Ci-Rx expression in the sensory vesicle. Together, these results support the conclusion that in Ciona embryogenesis, Ci-Rx expression is under the control of the Onecut transcription factor and that this factor is necessary and sufficient to specifically activate Ci-Rx through two enhancer elements.

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Section: Introductionsupporting

confidence: 85%

Section: Introductionmentioning

confidence: 99%

Onecut is a direct neural-specific transcriptional activator of Rx in Ciona intestinalis

D’Aniello

Pezzotti

Locascio

et al. 2011

Developmental Biology

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“…1B) seems to be evolutionarily conserved (35), the absence of rx in the differentiated photoreceptors of Row1 cells contrasts with its expression in vertebrate differentiated photoreceptors and its involvement in the regulation of phototransduction genes (36). The overlapping expression of rx and ci-opsin1 in the ciliary photoreceptor of tunicates (37,38) suggests either the acquisition of rx for the direct regulation of photoreceptor genes such as opsins at the base of Olfactores or amphioxus-specific loss of rx role for maintaining the differentiated ciliary photoreceptor program. The small population of rx-positive cells lacking the apical cilium might represent, as in vertebrates (39)(40)(41), a progenitor subpopulation needed for further growth of the frontal eye later in development.…”

Section: Discussionmentioning

confidence: 98%

Molecular analysis of the amphioxus frontal eye unravels the evolutionary origin of the retina and pigment cells of the vertebrate eye

Vopálenský

Pergner

Liegertová

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

116

166

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The origin of vertebrate eyes is still enigmatic. The "frontal eye" of amphioxus, our most primitive chordate relative, has long been recognized as a candidate precursor to the vertebrate eyes. However, the amphioxus frontal eye is composed of simple ciliated cells, unlike vertebrate rods and cones, which display more elaborate, surface-extended cilia. So far, the only evidence that the frontal eye indeed might be sensitive to light has been the presence of a ciliated putative sensory cell in the close vicinity of dark pigment cells. We set out to characterize the cell types of the amphioxus frontal eye molecularly, to test their possible relatedness to the cell types of vertebrate eyes. We show that the cells of the frontal eye specifically coexpress a combination of transcription factors and opsins typical of the vertebrate eye photoreceptors and an inhibitory Gi-type alpha subunit of the G protein, indicating an off-responding phototransductory cascade. Furthermore, the pigmented cells match the retinal pigmented epithelium in melanin content and regulatory signature. Finally, we reveal axonal projections of the frontal eye that resemble the basic photosensory-motor circuit of the vertebrate forebrain. These results support homology of the amphioxus frontal eye and the vertebrate eyes and yield insights into their evolutionary origin.evolution | vision | cephalochordate T he evolutionary origin of vertebrate eyes is enigmatic. Charles Darwin appreciated the conceptual difficulty in accepting that an organ as complex as the vertebrate eye could have evolved through natural selection (1). Part of the problem lies in the paucity of extant phyla with useful gradations that occurred during eye evolution, thus providing a scenario that led to the emergence of the vertebrate eye. For example, the eye of the adult lamprey (a jawless vertebrate) is remarkably similar to the eye of jawed vertebrates in the overall design, retina cell types, and multiple classes of opsins (2). Given these similarities, it is likely that the last common ancestor of jawless and jawed vertebrates already possessed an elaborate camera-type lens eye. To understand the seemingly sudden origin of the vertebrate eye, its evolutionary precursor must be identified within the nonvertebrate chordates lacking elaborated eye structures. Because of its basal phylogenetic position within the chordates (3), its slowly evolving genome (4), and its ancestral morphology, the cephalochordate amphioxus represents a traditional model organism for understanding the origin of vertebrate organs. Extensive electron microscopy studies of the cerebral vesicle of the basal chordate amphioxus revealed several putative photoreceptive organs-dorsal ocelli, Joseph cells, lamellar body, and the unpaired "frontal eye" (5). The pigmented dorsal ocelli and the Joseph cells are morphologically and molecularly related to invertebrate eye photoreceptors (6, 7), whereas the frontal eye and the lamellar body traditionally have been homologized to the vertebrate eyes and pineal g...

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“…This stimulus could determine a change in muscle tail contraction frequency, through excitation of interneurone circuits that drive the firing rate of motor neurones in the visceral ganglion. Such interneurones, located close to the photoreceptors and forming part of a retinal territory that sends 'descending' neuronal process to the visceral ganglion, have been detected morphologically (D'Aniello et al, 2006). When the light is on, hyperpolarization of photoreceptors occurs and the motor response frequency begins to wane, following the trend shown in Fig.·4.…”

Section: (N=15)mentioning

confidence: 89%

Development of swimming behaviour in the larva of the ascidianCiona intestinalis

Zega

Thorndyke

Brown

2006

Journal of Experimental Biology

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SUMMARY The aim of this study was to characterize the swimming behaviour of C. intestinalis larvae during the first 6 h after hatching by measuring tail muscle field potentials. This recording method allowed a quantitative description of the responses of the larva under light and dark conditions. Three different larval movements were distinguished by their specific frequencies: tail flicks, `spontaneous' swimming, and shadow response, or dark induced activity, with respective mean frequencies of about 10, 22 and 32 Hz. The shadow response develops at about 1.5 h post hatching (h.p.h.). The frequency of muscle potentials associated with this behaviour became higher than those of spontaneous swimming activity, shifting from 20 to 30 Hz, but only from about 2 h.p.h. onwards. Swimming rate was influenced positively for about 25 s after the beginning of the shadow response. Comparison of swimming activity at three different larval ages (0-2, 2-4 and 4-6 h.p.h.) showed that Ciona larvae swim for longer periods and more frequently during the first hours after hatching. Our results provide a starting point for future studies that aim to characterize the nervous control of ascidian locomotion,in wild-type or mutant larvae.

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The ascidian homolog of the vertebrate homeobox gene Rx is essential for ocellus development and function

Cited by 48 publications

References 56 publications

Onecut is a direct neural-specific transcriptional activator of Rx in Ciona intestinalis

Onecut is a direct neural-specific transcriptional activator of Rx in Ciona intestinalis

Molecular analysis of the amphioxus frontal eye unravels the evolutionary origin of the retina and pigment cells of the vertebrate eye

Development of swimming behaviour in the larva of the ascidianCiona intestinalis

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