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WIREs Dev Biol
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Formation of adult organs through metamorphosis in ascidians

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The representative characteristic of ascidians is their vertebrate‐like, tadpole shape at the larval stage. Ascidians lose the tadpole shape through metamorphosis to become adults with a nonmotile, sessile body and a shape generally considered distinct from that of vertebrates. Solitary ascidians including Ciona species are extensively studied to understand the developmental mechanisms of ascidians, and to compare these mechanisms with their counterparts in vertebrates. In these ascidian species, the digestive and circulatory systems are not well developed in the larval trunk and the larvae do not take food. This is in contrast with the inner conditions of vertebrate tadpoles, which have functional organs comparable to those of adults. The adult organs and tissues of these ascidians become functional during metamorphosis that is completed quickly, suggesting that the ascidian larvae of solitary species are a transient stage of development. We here discuss how the cells and tissues in the ascidian larval body are converted into those of adults. The hearts of ascidians and vertebrates use closely related cellular and molecular mechanisms that suggest their shared origin. Hox genes of ascidians are essential for forming adult endodermal structures. To fully understand the development and evolution of chordates, a complete elucidation of the mechanisms underlying the adult tissue/organ formation of ascidians will be needed. WIREs Dev Biol 2018, 7:e304. doi: 10.1002/wdev.304 This article is categorized under: Comparative Development and Evolution > Body Plan Evolution Early Embryonic Development > Development to the Basic Body Plan
The resemblance of the larval and juvenile CNS, revealed by the fluorescent labeling of neuronal cells. (a) Transgenic Ciona expressing Kaede (green) in the pan‐neuronal manner with the aid of the cis element of the gene encoding prohormone convertase 2 (PC2). Left: Larval stage. Right: A magnified image of the juvenile CNS. SV, sensory vesicle; MG, motor ganglion; NC, nerve cord. Arrows illustrate the anterior limit of the juvenile CNS. (b) Transgenic Ciona expressing Kaede (green) under the control of the cis element of the gene encoding VGLUT. In the larval CNS, the fluorescence is seen in the SV, which is the anterior part of larval CNS. In the juvenile CNS, the fluorescence is seen mostly at the anterior region of the CNS. (c) Transgenic Ciona expressing Kaede (green) under the control of the cis element of the gene encoding VACHT. In the larval CNS, the fluorescence is seen in the posterior SV and MG, which are located at the relatively middle part of the CNS. In the juvenile CNS, the fluorescence is seen mostly at the middle region of the CNS. The names of the transgenic lines are Tg[MiCiPC2K]3, Tg[MiCiVGLUT43K]1 and Tg[MiCiVACHTK]5.
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Fluorescent labeling of larval cells with Kaede to chase the cells during metamorphosis. (a) A Ciona larva expressing Kaede in the endodermal strand. Magenta and green illustrate Kaede‐red and Kaede‐green fluorescence, respectively. In this larva, the posterior half of the endodermal strand was irradiated with UV. (b) A juvenile emerged from a larva with photo‐converted Kaede in the endodermal strand as shown in (a). *: The intestinal region appears to be derived from the endodermal strand. The magenta color in other regions is autofluorescence. Please note that the juvenile is not necessarily from the larva in panel (a), though they are derived from the same experimental series. The photographs are of a transgenic line provided by the National BioResource Project Japan. The name of the line is Tg[MiCiZipCiFkhK]1, in the database of the Ciona transgenic line resource (http://marinebio.nbrp.jp/ciona/).
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The metamorphosis of ascidians. (a) Metamorphosing Ciona. Left: a larva during tail regression. Right: a juvenile just after the completion of tail regression. Tu, tunic; RT, regressed tail. After tail regression, larvae undergo the subsequent morphogenesis and growth to form a complete juvenile as shown in the right panel of (b). (b) The relationships between larval structures and adult organs. The photographs are the same as those shown in Figure . Bottom: The rough positions of adult organ primordia or the regions where adult organs will be created in the larval trunk (left) and adult organs in the juvenile body (right). CG, cerebral ganglion (adult CNS); ES, endostyle; OS, oral siphon; SV, sensory vesicle. (c) A larva of the compound ascidian Trididemnus nublum. This photograph was provided by Dr. Euichi Hirose. The inset is the same photograph of a larva of Ciona shown in (b). The size of the two photographs was adjusted to the same scale.
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The characteristics of ascidians. (a) A Ciona intestinalis Type A larva, lateral view. Anterior is toward the left. The sensory vesicle is a major part of the CNS. Note that this is the merged panel of two photographs of a single larva. (b) A juvenile C. intestinalis Type A at approximately 1 week after the initiation of metamorphosis. (c) An adult C. intestinalis Type A. OS, oral siphon; AS, atrial siphon. (d) The phylogenetic relationships of chordate groups.
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Mesoderms in an ascidian larva and juvenile. Mesodermal cells and tissues are labeled with green fluorescence. (a) Larval muscle cells. Green fluorescent protein (GFP) is expressed with the cis element of the gene encoding muscle‐type troponin I. This photograph is of the transgenic line Tg[MiCiTnIG]3. (b) Mesenchyme. Kaede‐green is expressed with the cis element of AKR. This photograph is of the transgenic line Tg[MiCiAKRK]1. (c) Musculature tissues and organs in a juvenile. ASM, atrial siphon muscle; BWM, body wall muscle that elongates toward the posterior end of the endostyle (PE); Ht, heart; OSM, oral siphon muscle. (d) Juvenile mesoderms derived from the larval mesenchyme. Bd, blood; Tc, a cluster of tunic cells. Tunic cells are dispersed throughout the tunic; only a few are identified here.
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Hox genes in ascidians. (a) Schematic illustration (not to scale) of the ideal Hox cluster in chordates. (b) Hox cluster of C. intestinalis. (c) A mutant larva of Hox1 exhibiting apparently normal trunk structure. (d,e) Juveniles of the enhancer trap line of Hox1. (d) A hemizygous animal recapitulating Hox1 expression with green fluorescence. GS, gill slit. (e) A homozygous mutant of Hox1 showing the absence of gill slits and malformation of the endostyle (bracket). (f,g) The enhancer trap line (EJ[MiTSAdTPOG]107) showing GFP expression in the gut (f) and a Hox10 morphant (g). The arrow in (f) indicates the intestine. In (g), the arrow suggests the absence of the intestine. (h) The intestine of a juvenile expressing Kaede‐green with the cis element of Hox12 (Tg[MiCiHox12K]1). The Kaede expression recapitulates the expression of Hox12. (i) The intestine of the Hox12‐knockout juvenile generated by TALEN‐mediated genome editing. In (h,i), the brackets suggest the corresponding subdomain of the intestine.
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Specification of heart muscle in ascidians. (a) Schematic illustration of a 110‐cell ascidian embryo, vegetal view. B7.5 is shown in red. (b) Specification of the heart and atrial siphon/body wall muscle. The cross‐talk between muscle and endostyle is also indicated.
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Expression of the markers for adult organs in the larval body. The settlement of the larvae was arrested by cutting their tails. (a) Gill and pyloric gland (PG). The white lines suggest the corresponding GFP expressions among larval and adult tissues. The enhancer trap line E[MiTSAdTPOG]6 was used in this photograph. (b) Adult neurons. The enhancer trap line E[MiTSAdTPOG]15 was used. (c) Endostyle. The enhancer trap line E[MiCiTPOG]2 was used.
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