XB-ART-37995
Front Zool
January 1, 2008;
5
9.
Development of the retinotectal system in the direct-developing frog Eleutherodactylus coqui in comparison with other anurans.
Abstract
Frogs primitively have a biphasic life history with an aquatic larva (tadpole) and a usually terrestrial adult. However, direct developing frogs of the genus Eleutherodactylus have lost a free living larval stage. Many larval structures never form during development of Eleutherodactylus, while limbs, spinal cord, and an adult-like cranial musculoskeletal system develop precociously. Here, I compare growth and differentiation of the retina and tectum and development of early axon tracts in the brain between Eleutherodactylus coqui and the biphasically developing frogs Discoglossus pictus, Physalaemus pustulosus, and Xenopus laevis using morphometry, immunohistochemical detection of proliferating cell nuclear antigen (PCNA) and acetylated tubulin, biocytin tracing, and in situ hybridization for NeuroD. Findings of the present study indicate that retinotectal development was greatly altered during evolution of Eleutherodactlyus mostly due to acceleration of cell proliferation and growth in retina and tectum. However, differentiation of retina, tectum, and fiber tracts in the embryonic brain proceed along a conserved slower schedule and remain temporally coordinated with each other in E. coqui. These findings reveal a mosaic pattern of changes in the development of the central nervous system (CNS) during evolution of the direct developing genus Eleutherodactylus. Whereas differentiation events in directly interconnected parts of the CNS such as retina, tectum, and brain tracts remained coordinated presumably due to their interdependent development, they were dissociated from proliferation control and from differentiation events in other parts of the CNS such as the spinal cord. This suggests that mosaic evolutionary changes reflect the modular character of CNS development.
PubMed ID: 18573199
PMC ID: PMC2442589
Article link: Front Zool
Species referenced: Xenopus
Genes referenced: cer1 neurod1 pc.1 pcna ret tuba4b was zic1
Antibodies: Biocytin Lectin1 Pcna Ab1 Tuba4b Ab4
Article Images: [+] show captions
References [+] :
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Morrow, NeuroD regulates multiple functions in the developing neural retina in rodent. 1999, Pubmed
Perron, The genetic sequence of retinal development in the ciliary margin of the Xenopus eye. 1998, Pubmed , Xenbase
Perron, Determination of vertebrate retinal progenitor cell fate by the Notch pathway and basic helix-loop-helix transcription factors. 2000, Pubmed
Picouet, [Architecture of the visual system of Discoglossus pictus (Oth)]. 1978, Pubmed
Potter, Structural characteristics of cell and fiber populations in the optic tectum of the frog (Rana catesbeiana). 1969, Pubmed
Richardson, Limb development and evolution: a frog embryo with no apical ectodermal ridge (AER). 1998, Pubmed , Xenbase
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Schlosser, Loss of ectodermal competence for lateral line placode formation in the direct developing frog Eleutherodactylus coqui. 1999, Pubmed , Xenbase
Schlosser, Mosaic evolution of neural development in anurans: acceleration of spinal cord development in the direct developing frog Eleutherodactylus coqui. 2003, Pubmed , Xenbase
Schlosser, Using heterochrony plots to detect the dissociated coevolution of characters. 2001, Pubmed
Schlosser, Evolution of nerve development in frogs. II. Modified development of the peripheral nervous system in the direct-developing frog Eleutherodactylus coqui (Leptodactylidae). 1997, Pubmed , Xenbase
Schlosser, Distribution of cranial and rostral spinal nerves in tadpoles of the frog Discoglossus pictus (Discoglossidae). 1995, Pubmed , Xenbase
Schlosser, Development of the retina is altered in the directly developing frog Eleutherodactylus coqui (Leptodactylidae). 1997, Pubmed , Xenbase
Schlosser, Evolution of nerve development in frogs. I. The development of the peripheral nervous system in Discoglossus pictus (Discoglossidae). 1997, Pubmed , Xenbase
Straznicky, The development of the tectum in Xenopus laevis: an autoradiographic study. 1972, Pubmed , Xenbase
Straznicky, The growth of the retina in Xenopus laevis: an autoradiographic study. 1971, Pubmed , Xenbase
Taylor, The early development of the frog retinotectal projection. 1993, Pubmed , Xenbase
Tsurimoto, PCNA, a multifunctional ring on DNA. 1999, Pubmed
Wilson, The development of a simple scaffold of axon tracts in the brain of the embryonic zebrafish, Brachydanio rerio. 1990, Pubmed
Yan, Requirement of neuroD for photoreceptor formation in the chick retina. 2003, Pubmed
Yan, neuroD induces photoreceptor cell overproduction in vivo and de novo generation in vitro. 1998, Pubmed
Analía Púgener, Osteology and skeletal development of Discoglossus sardus (Anura:Discoglossidae). 1997, Pubmed
Anderson, Expression of a novel N-CAM glycoform (NOC-1) on axon tracts in embryonic Xenopus brain. 1997, Pubmed , Xenbase
Anderson, Novel guidance cues during neuronal pathfinding in the early scaffold of axon tracts in the rostral brain. 1999, Pubmed , Xenbase
Beach, Patterns of cell proliferation in the retina of the clawed frog during development. 1979, Pubmed , Xenbase
Beach, Influences of thyroxine on cell proliferation in the retina of the clawed frog at different ages. 1979, Pubmed , Xenbase
Brown, Amphibian metamorphosis. 2007, Pubmed , Xenbase
Burrill, The first retinal axons and their microenvironment in zebrafish: cryptic pioneers and the pretract. 1995, Pubmed
Callery, Thyroid hormone-dependent metamorphosis in a direct developing frog. 2000, Pubmed , Xenbase
Callery, Frogs without polliwogs: evolution of anuran direct development. 2001, Pubmed , Xenbase
Chae, NeuroD: the predicted and the surprising. 2005, Pubmed , Xenbase
Chitnis, Axonogenesis in the brain of zebrafish embryos. 1990, Pubmed
Chung, Regionally specific expression of L1 and sialylated NCAM in the retinofugal pathway of mouse embryos. 2004, Pubmed
Coleman, Patterns of cell division during visual streak formation in the frog Limnodynastes dorsalis. 1985, Pubmed
Constantine-Paton, The relationship between retinal axon ingrowth, terminal morphology, and terminal patterning in the optic tectum of the frog. 1983, Pubmed
Cornel, Precocious pathfinding: retinal axons can navigate in an axonless brain. 1993, Pubmed , Xenbase
Currie, The development of the retino-tectal projection in Rana pipiens. 1975, Pubmed
Dann, Development of the optic tecta in the frog Limnodynastes dorsalis. 1989, Pubmed
Dorsky, Xotch inhibits cell differentiation in the Xenopus retina. 1995, Pubmed , Xenbase
Duellman, Reproductive strategies of frogs. 1992, Pubmed
Eagleson, Forebrain differentiation and axonogenesis in amphibians: I. Differentiation of the suprachiasmatic nucleus in relation to background adaptation behavior. 1998, Pubmed , Xenbase
Easter, The development of the Xenopus retinofugal pathway: optic fibers join a pre-existing tract. 1990, Pubmed , Xenbase
Elinson, Leg development in a frog without a tadpole (Eleutherodactylus coqui). 1994, Pubmed
Fang, Evolutionary alteration in anterior patterning: otx2 expression in the direct developing frog Eleutherodactylus coqui. 1999, Pubmed , Xenbase
Fraser, Fiber optic mapping of the Xenopus visual system: shift in the retinotectal projection during development. 1983, Pubmed , Xenbase
Fritzsch, The evolution of metamorphosis in amphibians. 1991, Pubmed
Gaze, Development of the tectum and diencephalon in relation to the time of arrival of the earliest optic fibres in Xenopus. 1992, Pubmed , Xenbase
Gaze, The evolution of the retinotectal map during development in Xenopus. 1974, Pubmed , Xenbase
Gaze, The relationship between retinal and tectal growth in larval Xenopus: implications for the development of the retino-tectal projection. 1980, Pubmed , Xenbase
Gaze, Optic synapses are found in diencephalic neuropils before development of the tectum in Xenopus. 1993, Pubmed , Xenbase
Gissi, Mitochondrial phylogeny of Anura (Amphibia): a case study of congruent phylogenetic reconstruction using amino acid and nucleotide characters. 2006, Pubmed
Goodhill, Retinotectal maps: molecules, models and misplaced data. 1999, Pubmed
Grant, Ontogeny of the retina and optic nerve in Xenopus laevis. I. Stages in the early development of the retina. 1980, Pubmed , Xenbase
HUGHES, Studies in embryonic and larval development in Amphibia. I. The embryology Eleutherodactylus ricordil, with special reference to the spinal cord. 1959, Pubmed
HUGHES, An experimental study on the relationships between limb and spinal cord in the embryo of Eleutherodactylus martinicensis. 1963, Pubmed
HUGHES, Studies in embryonic and larval development in Amphibia. II. The spinal motor-root. 1960, Pubmed
Hanken, Cranial ontogeny in the direct-developing frog, Eleutherodactylus coqui (Anura: Leptodactylidae), analyzed using whole-mount immunohistochemistry. 1992, Pubmed
Hanken, Limb development in a "nonmodel" vertebrate, the direct-developing frog Eleutherodactylus coqui. 2001, Pubmed , Xenbase
Hanken, Jaw muscle development as evidence for embryonic repatterning in direct-developing frogs. 1997, Pubmed
Hitchcock, Evidence for centripetally shifting terminals on the tectum of postmetamorphic Rana pipiens. 1988, Pubmed
Hollyfield, Differential growth of the neural retina in Xenopus laevis larvae. 1971, Pubmed , Xenbase
Hollyfield, Differential addition of cells to the retina in Rana pipiens tadpoles. 1968, Pubmed
Holt, Order in the initial retinotectal map in Xenopus: a new technique for labelling growing nerve fibres. 1983, Pubmed , Xenbase
Hoskins, Development of the ipsilateral retinothalamic projection in the frog Xenopus laevis. II. Ingrowth of optic nerve fibers and production of ipsilaterally projecting retinal ganglion cells. 1985, Pubmed , Xenbase
Inoue, Math3 and NeuroD regulate amacrine cell fate specification in the retina. 2002, Pubmed
Jacobson, Histogenesis of retina in the clawed frog with implications for the pattern of development of retinotectal connections. 1976, Pubmed , Xenbase
Jacobson, Cessation of DNA synthesis in retinal ganglion cells correlated with the time of specification of their central conections. 1968, Pubmed
Jennings, Mechanistic basis of life history evolution in anuran amphibians: thyroid gland development in the direct-developing frog, Eleutherodactylus coqui. 1998, Pubmed
Kanekar, Xath5 participates in a network of bHLH genes in the developing Xenopus retina. 1997, Pubmed , Xenbase
Klymkowsky, Whole-mount staining of Xenopus and other vertebrates. 1992, Pubmed , Xenbase
Lee, Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. 1995, Pubmed , Xenbase
Lemke, Retinotectal mapping: new insights from molecular genetics. 2005, Pubmed
Levine, An autoradiographic study of the retinal projection in Xenopus laevis with comparisons to Rana. 1980, Pubmed , Xenbase
Mann, Control of retinal growth and axon divergence at the chiasm: lessons from Xenopus. 2001, Pubmed , Xenbase
Marsh-Armstrong, Asymmetric growth and development of the Xenopus laevis retina during metamorphosis is controlled by type III deiodinase. 2000, Pubmed , Xenbase
Moore, Posttranslational mechanisms control the timing of bHLH function and regulate retinal cell fate. 2002, Pubmed , Xenbase
Morrow, NeuroD regulates multiple functions in the developing neural retina in rodent. 1999, Pubmed
Perron, The genetic sequence of retinal development in the ciliary margin of the Xenopus eye. 1998, Pubmed , Xenbase
Perron, Determination of vertebrate retinal progenitor cell fate by the Notch pathway and basic helix-loop-helix transcription factors. 2000, Pubmed
Picouet, [Architecture of the visual system of Discoglossus pictus (Oth)]. 1978, Pubmed
Potter, Structural characteristics of cell and fiber populations in the optic tectum of the frog (Rana catesbeiana). 1969, Pubmed
Richardson, Limb development and evolution: a frog embryo with no apical ectodermal ridge (AER). 1998, Pubmed , Xenbase
Roelants, Archaeobatrachian paraphyly and pangaean diversification of crown-group frogs. 2005, Pubmed
Schlosser, Loss of ectodermal competence for lateral line placode formation in the direct developing frog Eleutherodactylus coqui. 1999, Pubmed , Xenbase
Schlosser, Mosaic evolution of neural development in anurans: acceleration of spinal cord development in the direct developing frog Eleutherodactylus coqui. 2003, Pubmed , Xenbase
Schlosser, Using heterochrony plots to detect the dissociated coevolution of characters. 2001, Pubmed
Schlosser, Evolution of nerve development in frogs. II. Modified development of the peripheral nervous system in the direct-developing frog Eleutherodactylus coqui (Leptodactylidae). 1997, Pubmed , Xenbase
Schlosser, Distribution of cranial and rostral spinal nerves in tadpoles of the frog Discoglossus pictus (Discoglossidae). 1995, Pubmed , Xenbase
Schlosser, Development of the retina is altered in the directly developing frog Eleutherodactylus coqui (Leptodactylidae). 1997, Pubmed , Xenbase
Schlosser, Evolution of nerve development in frogs. I. The development of the peripheral nervous system in Discoglossus pictus (Discoglossidae). 1997, Pubmed , Xenbase
Straznicky, The development of the tectum in Xenopus laevis: an autoradiographic study. 1972, Pubmed , Xenbase
Straznicky, The growth of the retina in Xenopus laevis: an autoradiographic study. 1971, Pubmed , Xenbase
Taylor, The early development of the frog retinotectal projection. 1993, Pubmed , Xenbase
Tsurimoto, PCNA, a multifunctional ring on DNA. 1999, Pubmed
Wilson, The development of a simple scaffold of axon tracts in the brain of the embryonic zebrafish, Brachydanio rerio. 1990, Pubmed
Yan, Requirement of neuroD for photoreceptor formation in the chick retina. 2003, Pubmed
Yan, neuroD induces photoreceptor cell overproduction in vivo and de novo generation in vitro. 1998, Pubmed