Cubozoan jellyfish: an Evo/Devo model for eyes and other sensory systems.

Cnidaria are the most basal phylum containing a well-developed visual system located on specialized sensory structures (rhopalia) with eyes and statocyts. We have been exploring the cubozoan jellyfish, Tripedalia cystophora. In addition to containing simple photoreceptive ocelli, each rhopalium in Tridedalia has a large and small complex, camera-type eye with a cellular lens containing three distinct families of crystallins which apparently serve non-lenticular functions. Thus, Tridpedalia recruited crystallins by a gene sharing strategy as have mollusks and vertebrates. Tripedalia has a single Pax gene, PaxB, which encodes a structural and functional Pax 2/5/8-like paired domain as well as an octapeptide and Pax6-like homeodomain. PaxB binds to and activates Tripedalia crystallin promoters (especially J3-crystallin) and the Drosophila rhodopsin rh6 gene in transfection tests and induces ectopic eyes in Drosophila. In situ hybridization showed that PaxB and crystallin genes are expressed in the lens, retina and statocysts. We suggest from these results that an ancestral PaxB gene was a primordial gene in eye evolution and that eyes and ears (mechanoreceptors) may have had a common evolutionary origin. Thus, the numerous structural and molecular features of Tridpalia rhopalia indicate that ancient cubozoan jellyfish are fascinating models for evo/devo insights into eyes and other sensory systems.

[1]  Z. Kozmík,et al.  J3-crystallin of the jellyfish lens: Similarity to saposins , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[2]  W. Gehring,et al.  Isolation and developmental expression of the amphioxus Pax-6 gene (AmphiPax-6): insights into eye and photoreceptor evolution. , 1998, Development.

[3]  D. Nilsson,et al.  A simple visual system without neurons in jellyfish larvae , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[4]  Craig Montell,et al.  A PDZ protein ushers in new links , 2000, Nature Genetics.

[5]  A. Cvekl,et al.  Pax-6 and αB-crystallin/Small Heat Shock Protein Gene Regulation in the Murine Lens INTERACTION WITH THE LENS-SPECIFIC REGIONS, LSR1 AND LSR2* , 1996, The Journal of Biological Chemistry.

[6]  C. Weber.  Structure, histochemistry, ontogenetic development, and regeneration of the ocellus of Cladonema radiatum dujardin (cnidaria, hydrozoa, anthomedusae) , 1981, Journal of morphology.

[7]  J. Piatigorsky.  Lens crystallins. Innovation associated with changes in gene regulation. , 1992, The Journal of biological chemistry.

[8]  C. Desplan,et al.  Reinventing a Common Strategy for Patterning the Eye , 2001, Cell.

[9]  G. Schaffner,et al.  DNA sequence recognition by Pax proteins: bipartite structure of the paired domain and its binding site. , 1993, Genes & development.

[10]  J. Piatigorsky,et al.  Enzyme/crystallins: Gene sharing as an evolutionary strategy , 1989, Cell.

[11]  G. Mardon,et al.  Synergistic regulation of vertebrate muscle development by Dach2, Eya2, and Six1, homologs of genes required for Drosophila eye formation. , 1999, Genes & development.

[12]  Edward Groth,et al.  Facts and hypotheses , 1999, Nature Biotechnology.

[13]  L. Strong,et al.  Positional cloning and characterization of a paired box- and homeobox-containing gene from the aniridia region , 1991, Cell.

[14]  M. Coates,et al.  Visual Ecology and Functional Morphology of Cubozoa (Cnidaria)1 , 2003, Integrative and comparative biology.

[15]  N. Baker.  Master regulatory genes; telling them what to do. , 2001, BioEssays : news and reviews in molecular, cellular and developmental biology.

[16]  Z. Kozmík,et al.  Complex regulatory element within the γE- and γF-crystallin enhancers mediates Pax6 regulation and is required for induction by retinoic acid , 2002 .

[17]  J. Piatigorsky.  Crystallin genes: specialization by changes in gene regulation may precede gene duplication. , 2003 .

[18]  A. Jacobson.  THE DETERMINATION AND POSITIONING OF THE NOSE, LENS AND EAR. II. THE ROLE OF THE ENDODERM. , 1963, The Journal of experimental zoology.

[19]  D. Nilsson,et al.  A pessimistic estimate of the time required for an eye to evolve , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[20]  Andrew P Jarman,et al.  Studies of mechanosensation using the fly. , 2002, Human molecular genetics.

[21]  P. Callaerts,et al.  Conservation of Pax-6 in a lower chordate, the ascidian Phallusia mammillata. , 1997, Development.

[22]  J. Piatigorsky,et al.  Lens crystallins of invertebrates--diversity and recruitment from detoxification enzymes and novel proteins. , 1996, European journal of biochemistry.

[23]  P. Gruss,et al.  Pax2 contributes to inner ear patterning and optic nerve trajectory. , 1996, Development.

[24]  Masao Yoshida,et al.  Fine structure of complex ocelli of a cubomedusan, Tamoya bursaria Haeckel , 1976, Cell and Tissue Research.

[25]  J. Piatigorsky,et al.  Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. , 1988, Annual review of biochemistry.

[26]  Z. Kozmík,et al.  Structure and expression of the scallop Omega-crystallin gene. Evidence for convergent evolution of promoter sequences. , 2002, The Journal of biological chemistry.

[27]  J. Piatigorsky,et al.  Retinoic acid X receptor in the diploblast, Tripedalia cystophora. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Justin P. Kumar,et al.  EGF Receptor and Notch Signaling Act Upstream of Eyeless/Pax6 to Control Eye Specification , 2001, Cell.

[29]  B. Degnan,et al.  Expression of Pax258 in the gastropod statocyst: insights into the antiquity of metazoan geosensory organs , 2003, Evolution & development.

[30]  Ahmed Mansouri,et al.  Follicular cells of the thyroid gland require Pax8 gene function , 1998, Nature Genetics.

[31]  M. Busslinger,et al.  C‐terminal activating and inhibitory domains determine the transactivation potential of BSAP (Pax‐5), Pax‐2 and Pax‐8. , 1996, The EMBO journal.

[32]  B. Degnan,et al.  Cytological Basis of Photoresponsive Behavior in a Sponge Larva , 2001, The Biological Bulletin.

[33]  M. Busslinger,et al.  DNA-binding and transactivation properties of Pax-6: three amino acids in the paired domain are responsible for the different sequence recognition of Pax-6 and BSAP (Pax-5) , 1995, Molecular and cellular biology.

[34]  I. Ngridfetka.  Cooperation of Pax2 and Pax5 in midbrain and cerebellum development , 1997 .

[35]  T Ian Simpson,et al.  Pax6; A pleiotropic player in development , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[36]  W. D. de Jong,et al.  Evolution of eye lens crystallins: the stress connection. , 1989, Trends in biochemical sciences.

[37]  F. Relaix,et al.  From insect eye to vertebrate muscle: redeployment of a regulatory network. , 1999, Genes & development.

[38]  W. Li,et al.  Isolation of Cladonema Pax-B genes and studies of the DNA-binding properties of cnidarian Pax paired domains. , 2001, Molecular biology and evolution.

[39]  J. Sivak,et al.  Microscopical evaluation of the crystalline lens of the squid (Loligo opalescens) during embryonic development. , 1995, Experimental eye research.

[40]  D. M. Chapman,et al.  Muscular and nervous systems of the cubopolyp (Cnidaria) , 1976, Experientia.

[41]  J. Piatigorsky,et al.  The recruitment of crystallins: new functions precede gene duplication , 1991, Science.

[42]  T. Walsh,et al.  From flies' eyes to our ears: Mutations in a human class III myosin cause progressive nonsyndromic hearing loss DFNB30 , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[43]  M. Noll.  Evolution and role of Pax genes. , 1993, Current opinion in genetics & development.

[44]  C. L. Singla,et al.  Statocysts of hydromedusae , 2004, Cell and Tissue Research.

[45]  V. van Heyningen,et al.  PAX6 in sensory development. , 2002, Human molecular genetics.

[46]  Antone G. Jacobson.  THE DETERMINATION AND POSITIONING OF THE NOSE, LENS AND EAR. I. INTERACTIONS WITHIN THE ECTODERM, AND BETWEEN THE ECTODERM AND UNDERLYING TISSUES. , 1963, The Journal of experimental zoology.

[47]  G. Wistow.  Evolution of a protein superfamily: Relationships between vertebrate lens crystallins and microorganism dormancy proteins , 1990, Journal of Molecular Evolution.

[48]  P. Callaerts,et al.  Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. , 1995, Science.

[49]  M. Bronner‐Fraser,et al.  Vertebrate cranial placodes I. Embryonic induction. , 2001, Developmental biology.

[50]  K Ikeo,et al.  Pax 6: mastering eye morphogenesis and eye evolution. , 1999, Trends in genetics : TIG.

[51]  J. Leunissen,et al.  Evolution of the alpha-crystallin/small heat-shock protein family. , 1993, Molecular biology and evolution.

[52]  P. Callaerts,et al.  Characterization and expression analysis of an ancestor-type Pax gene in the hydrozoan jellyfish Podocoryne carnea , 2000, Mechanisms of Development.

[53]  BERNHARD WERNER,et al.  Life Cycle of Tripedalia cystophora Conant (Cubomedusae) , 1971, Nature.

[54]  W. Gehring,et al.  Isolation of a Pax-6 homolog from the ribbonworm Lineus sanguineus. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[55]  J. Piatigorsky,et al.  The cellular eye lens and crystallins of cubomedusan jellyfish , 1989, Journal of Comparative Physiology A.

[56]  T. Cronin,et al.  Spectral sensitivity in a sponge larva , 2002, Journal of Comparative Physiology A.

[57]  E. Craig,et al.  Four small Drosophila heat shock proteins are related to each other and to mammalian alpha-crystallin. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[58]  K. Kuma,et al.  Sponge Pax cDNA Related to Pax-2/5/8 and Ancient Gene Duplications in the Pax Family , 1998, Journal of Molecular Evolution.

[59]  D. Arendt,et al.  Reconstructing the eyes of Urbilateria. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[60]  J. Sivak,et al.  Immunolocalization of S‐crystallins in the developing squid (Loligo opalescens) lens , 1994, Developmental dynamics : an official publication of the American Association of Anatomists.

[61]  J. Posakony,et al.  An essential role for the Drosophila Pax2 homolog in the differentiation of adult sensory organs. , 1999, Development.

[62]  Lionel A. Walford,et al.  The Invertebrates. Protozoa Through Ctenophora , 1941 .

[63]  G A Horridge,et al.  Statocysts of medusae and evolution of stereocilia. , 1969, Tissue & cell.

[64]  Y Sun,et al.  Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. , 1995, Development.

[65]  Stephen L. Nutt,et al.  Commitment to the B-lymphoid lineage depends on the transcription factor Pax5 , 1999, Nature.

[66]  J. Pearse,et al.  Vision of cubomedusan jellyfishes. , 1978, Science.

[67]  D. Hewett‐Emmett,et al.  Evolution of paired domains: isolation and sequencing of jellyfish and hydra Pax genes related to Pax-5 and Pax-6. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[68]  H. Duan,et al.  shaven and sparkling are mutations in separate enhancers of the Drosophila Pax2 homolog. , 1998, Development.

[69]  D. Hayward,et al.  Localized expression of a dpp/BMP2/4 ortholog in a coral embryo , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[70]  W. Li,et al.  Isolation and expression of a Pax-6 gene in the regenerating and intact Planarian Dugesia(G)tigrina. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[71]  W. Fu,et al.  The Pax2 homolog sparkling is required for development of cone and pigment cells in the Drosophila eye. , 1997, Genes & development.

[72]  B. Degnan,et al.  Developmental expression of a class IV POU gene in the gastropod Haliotis asinina supports a conserved role in sensory cell development in bilaterians , 2002, Development Genes and Evolution.

[73]  A. Hudspeth,et al.  Mutation of the zebrafish choroideremia gene encoding Rab escort protein 1 devastates hair cells. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[74]  M. Busslinger,et al.  Long-term in vivo reconstitution of T-cell development by Pax5-deficient B-cell progenitors , 1999, Nature.

[75]  Sanjaya Singh,et al.  Dissection of the Transactivation Function of the Transcription Factor Encoded by the Eye Developmental Gene PAX6 * , 1998, The Journal of Biological Chemistry.

[76]  J. Piatigorsky,et al.  J1-crystallins of the cubomedusan jellyfish lens constitute a novel family encoded in at least three intronless genes. , 1993, The Journal of biological chemistry.

[77]  R. Schäfer,et al.  Alpha B-crystallin is a small heat shock protein. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[78]  A. Mansour,et al.  A defect in harmonin, a PDZ domain-containing protein expressed in the inner ear sensory hair cells, underlies Usher syndrome type 1C , 2000, Nature Genetics.

[79]  W. Gehring.  The genetic control of eye development and its implications for the evolution of the various eye-types. , 2002, The International journal of developmental biology.

[80]  B. Burnside,et al.  Myo3A, one of two class III myosin genes expressed in vertebrate retina, is localized to the calycal processes of rod and cone photoreceptors and is expressed in the sacculus. , 2003, Molecular biology of the cell.

[81]  Claude Desplan,et al.  Crystal structure of a paired domain-DNA complex at 2.5 å resolution reveals structural basis for pax developmental mutations , 1995, Cell.

[82]  Franck Pichaud,et al.  Pax genes and eye organogenesis. , 2002, Current opinion in genetics & development.

[83]  I. Hanson.  Mammalian homologues of the Drosophila eye specification genes. , 2001, Seminars in cell & developmental biology.

[84]  D. Hayward,et al.  Pax gene diversity in the basal cnidarian Acropora millepora (Cnidaria, Anthozoa): implications for the evolution of the Pax gene family. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[85]  V. Schmid,et al.  Larval development in Cnidaria: A connection to bilateria? , 2001, Genesis.

[86]  Gecko iota-crystallin: how cellular retinol-binding protein became an eye lens ultraviolet filter. , 2000 .

[87]  G. Saunders,et al.  Mouse Small eye results from mutations in a paired-like homeobox-containing gene , 1991, Nature.

[88]  R. M. Eakin.  Evolutionary Significance of Photoreceptors: In Retrospect , 1979 .

[89]  R. Maas,et al.  Genomic structure, evolutionary conservation and aniridia mutations in the human PAX6 gene , 1992, Nature Genetics.

[90]  J. A. Westfall,et al.  FINE STRUCTURE OF PHOTORECEPTORS IN THE HYDROMEDUSAN, POLYORCHIS PENICILLATUS. , 1962, Proceedings of the National Academy of Sciences of the United States of America.

[91]  Randall R. Reed,et al.  Role of Olf-1 and Pax-6 Transcription Factors in Neurodevelopment , 1996, The Journal of Neuroscience.

[92]  Craig Montell,et al.  Termination of phototransduction requires binding of the NINAC myosin III and the PDZ protein INAD , 1999, Nature Neuroscience.

[93]  L. Thim,et al.  J. Gen. Appl. Microbiol , 2020 .

[94]  K. Beisel,et al.  Keeping Sensory Cells and Evolving Neurons to Connect Them to the Brain: Molecular Conservation and Novelties in Vertebrate Ear Development , 2004, Brain, Behavior and Evolution.

[95]  Z. Kozmík,et al.  Role of Pax genes in eye evolution: a cnidarian PaxB gene uniting Pax2 and Pax6 functions. , 2003, Developmental cell.

[96]  A. Cvekl,et al.  Dual Roles for Pax-6: a Transcriptional Repressor of Lens Fiber Cell-Specific β-Crystallin Genes , 1998, Molecular and Cellular Biology.

[97]  J. Zigler,et al.  Alterations of lens protein synthesis in galactosemic rats. , 1979, Investigative ophthalmology & visual science.

[98]  S. Morris.  The Cambrian "explosion": slow-fuse or megatonnage? , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[99]  Michael Schubert,et al.  Functional equivalency of amphioxus and vertebrate Pax258 transcription factors suggests that the activation of mid-hindbrain specific genes in vertebrates occurs via the recruitment of Pax regulatory elements. , 2002, Gene.

[100]  S. Kumar,et al.  Evolution of functional diversification of the paired box (Pax) DNA-binding domains. , 1997, Molecular biology and evolution.

[101]  S. Hodgson,et al.  The human PAX6 gene is mutated in two patients with aniridia , 1992, Nature Genetics.

[102]  D. Schmucker,et al.  Direct regulation of rhodopsin 1 by Pax-6/eyeless in Drosophila: evidence for a conserved function in photoreceptors. , 1997, Genes & development.

[103]  J. Epstein,et al.  Getting your Pax straight: Pax proteins in development and disease. , 2002, Trends in genetics : TIG.

[104]  H. Kondoh,et al.  Pax6 and SOX2 form a co-DNA-binding partner complex that regulates initiation of lens development. , 2001, Genes & development.

[105]  J. Piatigorsky.  Delta crystallins and their nucleic acids , 2004, Molecular and Cellular Biochemistry.

[106]  J. Nathans,et al.  Vascular Development in the Retina and Inner Ear Control by Norrin and Frizzled-4, a High-Affinity Ligand-Receptor Pair , 2004, Cell.

[107]  P. Gruss,et al.  Conserved biological function between Pax-2 and Pax-5 in midbrain and cerebellum development: evidence from targeted mutations. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[108]  K. Beisel,et al.  Evolution and development of the vertebrate ear , 2001, Brain Research Bulletin.

[109]  J. Horwitz.  Alpha-crystallin can function as a molecular chaperone. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[110]  M. Brand,et al.  Characterization of three novel members of the zebrafish Pax2/5/8 family: dependency of Pax5 and Pax8 expression on the Pax2.1 (noi) function. , 1998, Development.

[111]  A. Jacobson.  THE DETERMINATION AND POSITIONING OF THE NOSE, LENS AND EAR. III. EFFECTS OF REVERSING THE ANTERO-POSTERIOR AXIS OF EPIDERMIS, NEURAL PLATE AND NEURAL FOLD. , 1963, The Journal of experimental zoology.

[112]  M. Noll,et al.  Conservation of a large protein domain in the segmentation gene paired and in functionally related genes of Drosophila , 1986, Cell.

[113]  B. Galliot,et al.  Cnidarians as a model system for understanding evolution and regeneration. , 2002, The International journal of developmental biology.

[114]  C. Desplan,et al.  The paired box encodes a second DNA-binding domain in the paired homeo domain protein. , 1991, Genes & development.

[115]  J. Piatigorsky,et al.  Lens Crystallins of Invertebrates , 1996 .

[116]  W. Gehring,et al.  Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. , 1994, Science.

[117]  Y. Hiromi,et al.  A conserved developmental program for sensory organ formation in Drosophila melanogaster , 2004, Nature Genetics.

[118]  P. Callaerts,et al.  Squid Pax-6 and eye development. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[119]  D. Hayward,et al.  Coral development: from classical embryology to molecular control. , 2002, The International journal of developmental biology.

[120]  S. Krauss,et al.  Zebrafish Pax9 Encodes Two Proteins with Distinct C-terminal Transactivating Domains of Different Potency Negatively Regulated by Adjacent N-terminal Sequences* , 1996, The Journal of Biological Chemistry.

[121]  Z. Kozmík,et al.  Complex regulatory element within the gammaE- and gammaF-crystallin enhancers mediates Pax6 regulation and is required for induction by retinoic acid. , 2002, Gene.

[122]  J A Epstein,et al.  Crystal structure of the human Pax6 paired domain-DNA complex reveals specific roles for the linker region and carboxy-terminal subdomain in DNA binding. , 1999, Genes & development.

[123]  J. Piatigorsky,et al.  Puzzle of crystallin diversity in eye lenses , 1993, Developmental dynamics : an official publication of the American Association of Anatomists.

[124]  M. Busslinger,et al.  The characterization of novel Pax genes of the sea urchin and Drosophila reveal an ancient evolutionary origin of the Pax2/5/8 subfamily , 1997, Mechanisms of Development.

[125]  A. Cvekl,et al.  Lens development and crystallin gene expression: many roles for Pax‐6 , 1996, BioEssays : news and reviews in molecular, cellular and developmental biology.

[126]  A. Packard,et al.  CEPHALOPODS AND FISH: THE LIMITS OF CONVERGENCE , 1972 .

[127]  K. Moses,et al.  Eye specification in Drosophila: perspectives and implications. , 2001, Seminars in cell & developmental biology.

[128]  M. Busslinger,et al.  Nephric lineage specification by Pax2 and Pax8. , 2002, Genes & development.

[129]  C. Dieckmann,et al.  Characterization of the EYE2 gene required for eyespot assembly in Chlamydomonas reinhardtii. , 2001, Genetics.

[130]  C. L. Singla.  Ocelli of hydromedusae , 1974, Cell and Tissue Research.

[131]  Giuseppina Barsacchi,et al.  Specification of the vertebrate eye by a network of eye field transcription factors , 2003, Development.

[132]  W. Gehring,et al.  DNA-binding characteristics of cnidarian Pax-C and Pax-B proteins in vivo and in vitro: no simple relationship with the Pax-6 and Pax-2/5/8 classes. , 2003, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[133]  J. Piatigorsky,et al.  Gene Sharing, Lens Crystallins and Speculations on an Eye/Ear Evolutionary Relationship1 , 2003, Integrative and comparative biology.

[134]  G. Dressler,et al.  Mapping of Pax-2 Transcription Activation Domains* , 1996, The Journal of Biological Chemistry.

[135]  G. D'alessio.  The evolution of monomeric and oligomeric betagamma-type crystallins. Facts and hypotheses. , 2002, European journal of biochemistry.

[136]  G. Halder,et al.  twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development. , 1999, Molecular cell.