Brain Sensory Organs of the Ascidian Ciona robusta: Structure, Function and Developmental Mechanisms - PubMed (original) (raw)
Review
Brain Sensory Organs of the Ascidian Ciona robusta: Structure, Function and Developmental Mechanisms
Paola Olivo et al. Front Cell Dev Biol. 2021.
Abstract
During evolution, new characters are designed by modifying pre-existing structures already present in ancient organisms. In this perspective, the Central Nervous System (CNS) of ascidian larva offers a good opportunity to analyze a complex phenomenon with a simplified approach. As sister group of vertebrates, ascidian tadpole larva exhibits a dorsal CNS, made up of only about 330 cells distributed into the anterior sensory brain vesicle (BV), connected to the motor ganglion (MG) and a caudal nerve cord (CNC) in the tail. Low number of cells does not mean, however, low complexity. The larval brain contains 177 neurons, for which a documented synaptic connectome is now available, and two pigmented organs, the otolith and the ocellus, controlling larval swimming behavior. The otolith is involved in gravity perception and the ocellus in light perception. Here, we specifically review the studies focused on the development of the building blocks of ascidians pigmented sensory organs, namely pigment cells and photoreceptor cells. We focus on what it is known, up to now, on the molecular bases of specification and differentiation of both lineages, on the function of these organs after larval hatching during pre-settlement period, and on the most cutting-edge technologies, like single cell RNAseq and genome editing CRISPR/CAS9, that, adapted and applied to Ciona embryos, are increasingly enhancing the tractability of Ciona for developmental studies, including pigmented organs formation.
Keywords: ascidians; evolution; molgula; photoreceptor cells; pigmented cells.
Copyright © 2021 Olivo, Palladino, Ristoratore and Spagnuolo.
Conflict of interest statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Figures
FIGURE 1
Pigmented organs in the sensory vesicle. (A) pArr>eGFP expression in photoreceptor territories of Ciona larval trunk (Yoshida et al., 2004) (photo from our lab). (B) Schematic representation of larval trunk. Ocellus (Oc) and otolith (Ot) pigment cells. Photoreceptor cell types I, II are associated with ocellus pigment cell, while photoreceptor cell type III is in close proximity to otolith pigment cell and coronet cells.
FIGURE 2
Schematic representation of Ciona neural plate stage. Neural plate, dorsal view, with 4 columns (1–4) and six rows (I-VI). The turquoise line separates the two bilaterally symmetrical blastomere pairs. The former a9-lineage photoreceptor cell precursors, right a9.33 and a9.37, are in green and red, respectively, while the supposed precursors of coronet cells, left a9.33 and a9.37, are in light green and light pink. The current A9-lineage Group I and II (A9.14) photoreceptor cell precursors is indicated in blue and Group III (A9.16) photoreceptor cell precursors in yellow.
FIGURE 3
Cartoon of a Ciona tadpole larva Central Nervous System showing the minimal visuomotor circuit. D., dorsal; V., ventral; A., anterior; P., posterior; PR-II, photoreceptor group II; PR-I, photoreceptor group I; pr-AMG RN, Photoreceptor Ascending Motor Ganglion Relay Neuron; prRN, photoreceptor Relay Neuron; MGIN, Motor Ganglion InterNeuron; MN, Motor Neuron. BV, Brain Vesicle; VG, Visceral Ganglion. Adapted from Kourakis et al. (2019).
FIGURE 4
Cartoon of a Ciona tadpole larva Central Nervous System showing the minimal gravitaxis circuit. D., dorsal; V., ventral; A., anterior; P., posterior; ClC, ciliated cells; Ants: glutamatergic antennae sensory neurons; antRNS, GABAergic antenna Relay Neurons; MGIN, Motor Ganglion Inter Neuron; MN, Motor Neuron. BV, Brain Vesicle; VG, Visceral Ganglion. Adapted from Kourakis et al. (2019) and Bostwick et al. (2020).
FIGURE 5
Otolith/ocellus cell fate in Ciona robusta. (A) Summary of pigmented cell lineage development within CNS, with the developmental stages (hours post fertilization, hpf) indicated the timeline [from Racioppi et al. (2014)]. (B) Fate determination of otolith and ocellus precursors from a9.49 blastomeres, under the control of FGF [adapted from Racioppi et al. (2014)]. (C) Reconstruction of genes involved in controlling otolith/ocellus determination. Adapted from Racioppi et al. (2014).
Similar articles
- Revised lineage of larval photoreceptor cells in Ciona reveals archetypal collaboration between neural tube and neural crest in sensory organ formation.
Oonuma K, Tanaka M, Nishitsuji K, Kato Y, Shimai K, Kusakabe TG. Oonuma K, et al. Dev Biol. 2016 Dec 1;420(1):178-185. doi: 10.1016/j.ydbio.2016.10.014. Epub 2016 Oct 24. Dev Biol. 2016. PMID: 27789227 - The ascidian homolog of the vertebrate homeobox gene Rx is essential for ocellus development and function.
D'Aniello S, D'Aniello E, Locascio A, Memoli A, Corrado M, Russo MT, Aniello F, Fucci L, Brown ER, Branno M. D'Aniello S, et al. Differentiation. 2006 Jun;74(5):222-34. doi: 10.1111/j.1432-0436.2006.00071.x. Differentiation. 2006. PMID: 16759288 - The peripheral nervous system of the ascidian tadpole larva: Types of neurons and their synaptic networks.
Ryan K, Lu Z, Meinertzhagen IA. Ryan K, et al. J Comp Neurol. 2018 Mar 1;526(4):583-608. doi: 10.1002/cne.24353. Epub 2017 Nov 29. J Comp Neurol. 2018. PMID: 29124768 - The Degenerate Tale of Ascidian Tails.
Fodor ACA, Powers MM, Andrykovich K, Liu J, Lowe EK, Brown CT, Di Gregorio A, Stolfi A, Swalla BJ. Fodor ACA, et al. Integr Comp Biol. 2021 Sep 8;61(2):358-369. doi: 10.1093/icb/icab022. Integr Comp Biol. 2021. PMID: 33881514 Free PMC article. Review. - The neurobiology of the ascidian tadpole larva: recent developments in an ancient chordate.
Meinertzhagen IA, Lemaire P, Okamura Y. Meinertzhagen IA, et al. Annu Rev Neurosci. 2004;27:453-85. doi: 10.1146/annurev.neuro.27.070203.144255. Annu Rev Neurosci. 2004. PMID: 15217340 Review.
Cited by
- Stress granule-related genes during embryogenesis of an invertebrate chordate.
Drago L, Pennati A, Rothbächer U, Ashita R, Hashimoto S, Saito R, Fujiwara S, Ballarin L. Drago L, et al. Front Cell Dev Biol. 2024 Aug 1;12:1414759. doi: 10.3389/fcell.2024.1414759. eCollection 2024. Front Cell Dev Biol. 2024. PMID: 39149517 Free PMC article. - Gene networks and the evolution of olfactory organs, eyes, hair cells and motoneurons: a view encompassing lancelets, tunicates and vertebrates.
Fritzsch B, Glover JC. Fritzsch B, et al. Front Cell Dev Biol. 2024 Mar 12;12:1340157. doi: 10.3389/fcell.2024.1340157. eCollection 2024. Front Cell Dev Biol. 2024. PMID: 38533086 Free PMC article. Review. - Cone photoreceptor phosphodiesterase PDE6H inhibition regulates cancer cell growth and metabolism, replicating the dark retina response.
Yalaz C, Bridges E, Alham NK, Zois CE, Chen J, Bensaad K, Miar A, Pires E, Muschel RJ, McCullagh JSO, Harris AL. Yalaz C, et al. Cancer Metab. 2024 Feb 13;12(1):5. doi: 10.1186/s40170-023-00326-y. Cancer Metab. 2024. PMID: 38350962 Free PMC article. - Development and circuitry of the tunicate larval Motor Ganglion, a putative hindbrain/spinal cord homolog.
Piekarz KM, Stolfi A. Piekarz KM, et al. J Exp Zool B Mol Dev Evol. 2024 May;342(3):200-211. doi: 10.1002/jez.b.23221. Epub 2023 Sep 7. J Exp Zool B Mol Dev Evol. 2024. PMID: 37675754 Review. - A single oscillating proto-hypothalamic neuron gates taxis behavior in the primitive chordate Ciona.
Chung J, Newman-Smith E, Kourakis MJ, Miao Y, Borba C, Medina J, Laurent T, Gallean B, Faure E, Smith WC. Chung J, et al. Curr Biol. 2023 Aug 21;33(16):3360-3370.e4. doi: 10.1016/j.cub.2023.06.080. Epub 2023 Jul 24. Curr Biol. 2023. PMID: 37490920 Free PMC article.
References
- Arshavsky V. Y., Lamb T. D., Pugh E. N., Jr. (2002). G proteins and phototransduction. Annu. Rev. Physiol. 64 153–187. - PubMed
Publication types
LinkOut - more resources
Full Text Sources
Research Materials