The ascidian pigmented sensory organs: structures and developmental programs

Esposito, Roberto; Racioppi, Claudia; Pezzotti, M.; Branno, Margherita; Locascio, Annamaria; Ristoratore, Filomena

doi:10.1002/dvg.22836

Cited by 17 publications

(18 citation statements)

References 130 publications

(222 reference statements)

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“…Some, but not all, of the photoreceptors associated with the ocellus are glutamatergic, while some appear to be GABA/glycinergic . Photo‐transduction and visual cycle genes of the ocellus photoreceptors have been reviewed elsewhere . The opening of the pigmented cup is ventral‐anterior .…”

Section: Cell Types In the Cnsmentioning

confidence: 99%

“…The pigment cell lineage is also well described (Figure (a)). Pigment cells most likely share an evolutionary relationship with the cephalic neural crest of vertebrates (for more discussion on evolutionary relationships of pigmented cells, see Ref ). Pigment cells arise from the lateral‐most a‐line‐derived CNS.…”

Section: Step‐by‐step Cell Fate Specification In the Cnsmentioning

confidence: 99%

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The central nervous system of ascidian larvae

Hudson

2016

WIREs Developmental Biology

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Ascidians are marine invertebrate chordates. Their tadpole larvae contain a dorsal tubular nervous system, resulting from the rolling up of a neural plate. Along the anterior-posterior (A-P) axis, the central nervous system (CNS) is organized into a sensory vesicle, neck, trunk ganglion, and tail nerve cord and consists of approximately only 330 cells, of which around 100 are thought to be neurons. The organization of distinct neuronal cell types and neurotransmitter gene expression within the CNS has been described. The unique developmental mode of ascidians, with a small number of cells and a fixed cell division pattern, allows individual cells to be traced throughout development. This feature has led to the complete documentation of the cell lineages of certain cell types in the CNS. Thus, a step-by-step understanding of nervous system development from the initial stages of neural induction to the neurogenesis of individual neurons is a feasible goal. The genetic control of neural fate induction and early neural plate patterning are now well understood. The molecular mechanisms specifying the cholinergic neurons of the trunk ganglion as well as the pigment cells of the sensory organs are also well elucidated. In addition, studies have begun on the morphogenetic processes of neurulation. Remaining challenges include building an embryonic atlas integrating gene expression patterns, cell lineage, and neuronal cell types as well as developing the gene regulatory networks of cell fate specification and integrating them with the genetic control of morphogenesis. WIREs Dev Biol 2016, 5:538-561. doi: 10.1002/wdev.239 For further resources related to this article, please visit the WIREs website.

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Section: Cell Types In the Cnsmentioning

confidence: 99%

Section: Step‐by‐step Cell Fate Specification In the Cnsmentioning

confidence: 99%

The central nervous system of ascidian larvae

Hudson

2016

WIREs Developmental Biology

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“…These differentiation events occur very late in development, with melanization of the second of the two pigment cells appearing only just before the larval stage. Much is known about the cell type specification pathways for these cells (Esposito et al, 2015). They are derived from the bilateral a8.25 cells and require induction from vegetal blastomeres at the 32-cell stage for later pigment expression (Nishida, 1987; Nishida and Satoh, 1989; Oonuma et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

High temperature limits on developmental canalization in the ascidian Ciona intestinalis

Irvine

McNulty

Siler

et al. 2018

Preprint

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20The normal embryogenesis of marine animals is typically confined to a species-specific range of 21 temperatures. Within that temperature range development results in a consistent, or canalized, phenotype, 22whereas above and below the range abnormal phenotypes are produced. This study reveals an abrupt high 23 temperature limit, occurring over a 1-2°C range, for normal embryonic development in C. intestinalis. 24Above that threshold morphological abnormalities in the notochord and other organs are observed, 25 beginning with cleavage and gastrula stages, and becoming more pronounced as embryogenesis proceeds. 26However, even in highly morphologically abnormal temperature disrupted (TD) embryos, cell type 27 specification, including muscle, endoderm, notochord, and sensory pigment cells is accomplished. An 28 explanation for this finding is that in C. intestinalis cell type specification occurs relatively early in 29 embryogenesis, due to cleavage stage segregation of maternal cytoplasmic determinants and short-range 30 cell interactions, which are largely intact in TD embryos. On the other hand, morphogenesis of the 31 notochord and other structures is dependent on precise cell movement and shape changes after the 32 gastrula stage, which appear to be disrupted above the high temperature threshold. These findings have 33 implications for the relationship between ecology and reproduction in C. intestinalis. More broadly they 34 point to mechanisms behind canalization in animals, such as ascidians, characterized by early, largely 35 autonomous, cell type specification. 36 37 38 39 42 temperature is a major determinant. This study seeks to establish which aspects of embryogenesis are the 43 most susceptible to high temperature in the model marine invertebrate Ciona. 44C. intestinalis, like many if not all animals, has a "normal" embryonic phenotype that is produced 45 over a range of environmental conditions. The ability for a developmental program to produce a 46 stereotyped outcome in spite of environmental variation has been termed "canalization" (Siegal and 47 Bergman, 2002; Waddington, 1942). 48While there has been much work done on the effects of water temperature on the overall life 49 history of marine invertebrates, a literature search reveals little work examining in detail water 50 temperature effects on embryogenesis itself. However, it is likely that the ability to develop to a 51 functional larval stage is an imporftant factor limiting the ranges of many marine invertebrates (Byrne et 52 al., 2009). It is also likely that embryologists historically have been more interested in how normal

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“…The sensory vesicle contains different sensory receptor cells, including the anterior geotactic otolith (Ot; Dilly, ; Tsuda, Sakurai, & Goda, ) and the posterior photoreceptive ocellus (Oc; Dilly, ; Tsuda et al, ). The Ot is a gravity‐sensing organ made of a single pigment cell, whereas the photo‐sensing Oc is a multicellular structure (composed of one pigment cell, three lens cells, and 37 photoreceptors cells in C. robusta ; Esposito et al, ; Ryan, Lu, & Meinertzhagen, ) and the complete GRN driving the specification of pigmented cells has been described (Racioppi et al, ).…”

Section: Ascidian Neurodevelopment and Edcs Toxicitymentioning

confidence: 99%

“…Within the sensory vesicle, two pigmented cells are visible: the otolith (Ot) and the ocellus (Oc). The otolith is a gravity‐sensing organ made of a single pigment cell, whereas the photo‐sensing ocellus is a multicellular structure composed of one pigment cell, three lens cells and 37 photoreceptors cells (Esposito et al, ; Racioppi et al, ; Ryan et al, ). Other sensory cells are also present, such as antenna cells and coronet cells (Ryan et al, ; adapted from Hudson, ).…”

Section: Ascidian Neurodevelopment and Edcs Toxicitymentioning

confidence: 99%

Potential roles of nuclear receptors in mediating neurodevelopmental toxicity of known endocrine‐disrupting chemicals in ascidian embryos

Gomes

Gazo

Besnardeau

et al. 2019

Molecular Reproduction Devel

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Endocrine Disrupting Chemicals (EDCs) are molecules able to interfere with the vertebrate hormonal system in different ways, a major one being the modification of the activity of nuclear receptors (NRs). Several NRs are expressed in the vertebrate brain during embryonic development and these NRs are suspected to be responsible for the neurodevelopmental defects induced by exposure to EDCs in fishes or amphibians and to participate in several neurodevelopmental disorders observed in humans. Known EDCs exert toxicity not only on vertebrate forms of marine life but also on marine invertebrates. However, because hormonal systems of invertebrates are poorly understood, it is not clear whether the teratogenic effects of known EDCs are because of endocrine disruption. The most conserved actors of endocrine systems are the NRs which are present in all metazoan genomes but their functions in invertebrate organisms are still insufficiently characterized. EDCs like bisphenol A have recently been shown to affect neurodevelopment in marine invertebrate chordates called ascidians. Because such phenotypes can be mediated by NRs expressed in the ascidian embryo, we review all the information available about NRs expression during ascidian embryogenesis and discuss their possible involvement in the neurodevelopmental phenotypes induced by EDCs. K E Y W O R D S endocrine-disrupting chemicals, marine invertebrate, mode-of-action, neurodevelopment, nuclear receptors

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The ascidian pigmented sensory organs: structures and developmental programs

Cited by 17 publications

References 130 publications

The central nervous system of ascidian larvae

The central nervous system of ascidian larvae

High temperature limits on developmental canalization in the ascidian Ciona intestinalis

Potential roles of nuclear receptors in mediating neurodevelopmental toxicity of known endocrine‐disrupting chemicals in ascidian embryos

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