The evolutionary history of placodes: A molecular genetic investigation of the larvacean urochordate Oikopleura dioica

Development

Volumn 132, Issue 19, 2005, Pages 4259-4272

  Bassham, Susan ^a   Postlethwait, John H ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

Appendicularia; Chordate evolution; Larvacean; Tunicate

Indexed keywords

ADENOHYPOPHYSIS; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EVOLUTION; GENE EXPRESSION; IN SITU HYBRIDIZATION; LARVAL STAGE; MOLECULAR CLONING; MOLECULAR GENETICS; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY SYSTEM; ORGANOGENESIS; ORTHOLOGY; PLESIOMORPHY; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; UROCHORDATA; VERTEBRATE;

ANIMALS; EMBRYO, NONMAMMALIAN; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MECHANORECEPTORS; MICROSCOPY, ELECTRON, SCANNING; MORPHOGENESIS; NEURAL CREST; NOTOCHORD; PROTEINS; UROCHORDATA;

APPENDICULARIA (CLASS); CHORDATA; OIKOPLEURA DIOICA; UROCHORDATA; VERTEBRATA;

EID: 27644458291     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01973     Document Type: Article

References (96)

1. Baker, C. V. and Bronner-Fraser, M. (1997). The origins of the neural crest. Part II: an evolutionary perspective. Mech. Dev. 69, 13-29.
2. Baker, C. V. H. and Bronner-Fraser, M. (2001). Vertebrate cranial placodes. I. Embryonic induction. Dev. Biol. 232, 1-61.
3. Bassham, S. and Postlethwait, J. (2000). Brachyury (T) expression in embryos of a larvacean urochordate, Oikopleura dioica, and the ancestral role of brachyury. Dev. Biol. 220, 322-333.
4. Begbie, J. and Graham, A. (2001). The ectodermal placodes: a dysfunctional family. Phil. Trans. R. Soc. Lond. B. 356, 1655-1660.
5. Bessarab, D. A., Chong, S. W. and Korzh, V. (2004). Expression of zebrafish six1 during sensory organ development and myogenesis. Dev. Dyn. 230, 781-786.
6. Bollner, T., Holmberg, K. and Olsson, R. (1986). A rostral sensory mechanism in Oikopleura dioica (Appendicularia). Acta Zool. (Stockholm) 67, 235-241.
7. Bollner, T., Storm-Mathiesen, J. and Ottersen, O. P. (1991). GABA-like immunoreactivity in the nervous system of Oikopleura dioica (Appendicularia). Biol. Bull. 180, 119-124.
8. Bone, Q. (1998). Nervous system, sense organs, and excitable epithelia. In The Biology of Pelagic Tunicates (ed. Q. Bone), pp. 55-80. New York: Oxford University Press.
9. Bone, Q. and Ryan, K. P. (1978). Cupular sense organs in Ciona (Tunicata: Ascidiacea). J. Zool. (Lond.) 186, 417-429.
10. Bone, Q. and Ryan, K. P. (1979). The Langerhans receptor of Oikopleura (Tunicata: Larvacea). J. Mar. Biol. Assoc. UK 59, 69-75.
11. Boorman, C. J. and Shimeld, S. M. (2002). Pitx homeobox genes in Ciona and amphioxus show left-right asymmetry is a conserved chordate character and define the ascidian adenohypophysis. Evol. Dev. 4, 354-365.
12. Burighel, P., Lane, N. J., Zaniolo, G. and Manni, L. (1998). Neurogenic role of the neural gland in the development of the ascidian, Botryllus schlosseri (Tunicata, Urochordata). J. Comp. Neurol. 394, 230-241.
13. Burighel, P., Lane, N. J., Fabio, G., Stefano, T., Zaniolo, G., Carnevali, M. D. and Manni, L. (2003). Novel, secondary sensory cell organ in ascidians: in search of the ancestor of the vertebrate lateral line. J. Comp. Neurol. 461, 236-249.
14. Cañestro, C., Bassham, S. and Postlethwait, J. H. (2005). Development of the Central Nervous System in the larvacean Oikopleura dioica and the evolution of the chordate brain. Dev. Biol. (in press).
15. Christiaen, L., Burighel, P., Smith, W. C., Vernier, P., Bourrat, F. and Joly, J.-S. (2002). Pitx genes in Tunicates provide new molecular insight into the evolutionary origin of pituitary. Gene 287, 107-113.
16. Christiaen, L., Bourrat, E. and Joly, J. S. (2005). A modular cis-regulatory system controls isoform-specific pitx expression in ascidian stomodaeum. Dev. Biol. 277, 557-566.
17. Couly, G. F. and Le Douarin, N. M. (1985). Mapping of the early neural primordium in quail-chick chimeras. I. Developmental relationships between placodes, facial ectoderm, and prosencephalon. Dev. Biol. 110, 422-439.
18. Cox, C. J., Espinoza, H. M., McWilliams, B., Chappell, K., Morton, L., Hjalt, T. A., Semina, E. V. and Amendt, B. A. (2002). Differential regulation of gene expression by PITX2 isoforms. J. Biol. Chem. 277, 25001-25010.
19. David, R., Ahrens, K., Wedlich, D. and Schlosser, G. (2001). Xenopus Eya1 demarcates all neurogenic placodes as well as migrating hypaxial muscle precursors. Mech. Dev. 103, 189-192.
20. Delsman, H. C. (1912). Weitere beobachtungen über die entwicklung von Oikopleura dioica. Tijdschr. ned dierk. Ver. 12, 199-206.
21. Drouin, J., Lamolet, B., Lamonerie, T., Lanctot, C. and Tremblay, J. J. (1998). The PTX family of homeodomain transcription factors during pituitary developments. Mol. Cell Endocrinol. 140, 31-36.
22. Dutta, S., Dietrich, J.-E., Aspöck, G., Burdine, R. D., Schier, A., Westerfield, M. and Varga, Z. M. (2005). pitx3 defines an equivalence domain for lens and anterior pituitary placode. Development 132, 1579-1590.
23. Edvardsen, R. B., Seo, H. C., Jensen, M. F., Mialon, A., Mikhaleva, J., Bjordal, M., Cartry, J., Reinhardt, R., Weissenbach, J., Wincker, P. et al. (2005). Remodelling of the homeobox gene complement in the tunicate Oikopleura dioica. Curr. Biol. 15, R12-R13.
24. Essner, J. J., Branford, W. W., Zhang, J. and Yost, H. J. (2000). Mesendoderm and left-right brain, heart and gut development are differentially regulated by pitx2 isoforms. Development 127, 1081-1093.
25. Farbman, A. (1992). Cell Biology of Olfaction. Cambridge, UK: Cambridge University Press.
26. Farbman, A. I. (2000). Cell biology of olfactory epithelium. In The Neurobiology of Taste and Smell (ed. R. E. Finger, W. L. Silver and D. Restrepo), pp. 131-158. New York: Wiley-Liss.
27. Furukawa, T., Kozak, C. A. and Cepko, C. L. (1997). rax, a novel paired-type homeobox gene, shows expression in the anterior neural fold and developing retina. Proc. Natl. Acad. Sci. USA 94, 3088-3093.
28. Gage, P. J. and Camper, S. A. (1997). Pituitary homeobox 2, a novel member of the bicoid-related family of homeobox genes, is a potential regulator of anterior structure formation. Hum. Mol. Genet. 6, 457-464.
29. Gage, P. J., Suh, H. and Camper, S. A. (1999). The bicoid-related Pitx gene family in development. Mamm. Genome 10, 197-200.
30. Gallardo, M. E., Lopez-Rios, J., Fernaud-Espinosa, I., Granadino, B., Sanz, R., Ramos, C., Ayuso, C., Seller, M. J., Brunner, H. G., Bovolenta, P. et al. (1999). Genomic cloning and characterization of the human homeobox gene SIX6 reveals a cluster of SIX genes in chromosome 14 and associates SIX6 hemizygosity with bilateral anophthalmia and pituitary anomalies. Genomics 61, 82-91.
31. Galt, C. P. and Mackie, G. O. (1971). Electrical correlates of ciliary reversal in Oikopleura. J. Exp. Biol. 55, 205-212.
32. Ganot, P., Kallesoe, T., Reinhardt, R., Chourrout, D. and Thompson, E. M. (2004). Spliced-leader RNA trans splicing in a chordate, Oikopleura dioica, with a compact genome. Mol. Cell. Biol. 24, 7795-7805.
33. Gans, C. and Northcutt, R. G. (1983). Neural crest and the origin of vertebrates: a new head. Science 220, 268-274.
34. Georges, D., Holmberg, K. and Olsson, R. (1988). The ventral midbrain cells in Oikopleura dioica (Appendicularia). Acta Embryol. Morphol. Exp. 9, 39-47.
35. Ghanbari, H., Seo, H.-C., Fjose, A. and Brandli, A. W. (2001). Molecular cloning and embryonic expression of Xenopus Six homeobox genes. Mech. Dev. 101, 271-277.
36. Glardon, S., Callaerts, P., Halder, G. and Gehring, W. J. (1997). Conservation of Pax-6 in a lower chordate, the ascidian Phallusia mammillata. Development 124, 817-825.
37. Gompel, N., Dambly-Chaudiere, C. and Ghysen, A. (2001). Neuronal differences prefigure somatotopy in the zebrafish lateral line. Development 128, 387-393.
38. Gorbman, A. (1983). Early development of the hagfish pituitary gland: evidence for the endodermal origin of the adenohypophysis. Am. Zool. 23, 639-654.
39. Gorbman, A. (1995). Olfactory origins and evolution of the brain-pituitary endocrine system: facts and speculation. Gen. Comp. Endocrinol. 97, 171-178.
40. Gorbman, A., Nozaki, M. and Kubokawa, K. (1999). A brain-Hatschek's pit connection in amphioxus. Gen. Comp. Endocrinol. 113, 251-254.
41. Hanson, I. M. (2001). Mammalian homologues of the Drosophila eye specification genes. Semin. Cell Dev. Biol. 12, 475-484.
42. Holland, L. Z. and Holland, N. D. (2001). Evolution of neural crest and placodes: amphioxus as a model for the ancestral vertebrate? J. Anat. 199, 85-98.
43. Holland, N. D. and Yu, J. K. (2002). Epidermal receptor development and sensory pathways in vitally stained amphioxus (Branchiostoma floridae). Acta Zool. (Stockholm) 83, 309-319.
44. Holmberg, K. (1982). The ciliated brain duct of Oikopleura dioica (Tunicata, Appendicularia). Acta Zool. (Stockholm) 63, 101-109.
45. Holmberg, K. (1986). The neural connection between the Langerhans receptor cells and the central nervous system in Oikopleura dioica (Appendicularia). Zoomorphology 106, 31-34.
46. Hoppe, R., Frank, H., Breer, H. and Strotmann, J. (2003). The clustered olfactory receptor gene family genomic organization, promoter elements, and interacting transcription factors. Genome Res. 13, 2674-2685.
47. Jean, D., Bernier, G. and Gruss, P. (1999). Six6 (Optx2) is a novel murine Six3-related homeobox gene that demarates the presumptive pituitary/hypothalamic axis and the ventral optic stalk. Mech. Dev. 84, 31-40.
48. Kawakami, K., Sato, S., Ozaki, H. and Ikeda, K. (2000). Six family genes - structure and function as transcription factors and their roles in development. BioEssays 22, 616-626.
49. Kawamura, K. and Kikuyama, S. (1992). Evidence that hypophysis and hypothalamus constitute a single entity from the primary stage of histogenesis. Development 115, 1-9.
50. Kobayashi, M., Toyama, R., Takeda, H., Dawid, I. B. and Kawakami, K. (1998). Overexpression of the forebrain-specific homeobox gene six3 induces rostral forebrain enlargement in zebrafish. Development 125, 2973-2982.
51. Kozlowski, D. J., Whitfield, T. T., Hukriede, N. A., Lam, W. K. and Weinberg, E. S. (2005). The zebrafish dog-eared mutation disrupts eya1, a gene required for cell survival and differentiation in the inner ear and lateral line. Dev. Biol. 277, 27-41.
52. Kozmik, Z., Holland, N. D., Kalousova, A., Paces, J., Schubert, N. and Holland, L. (1999). Characterization of an amphioxus paried box gene, AmphiPax2/5/8: developmental expression patterns in optic support cells, nephridium, thyroid-like structures and pharyngeal gill slits, but not in the midbrain boundary region. Development 126, 1295-1304.
53. Lacalli, T. C. and Hou, S. (1999). A reexamination of the epithelial sensory cells of amphioxus (Branchiostoma). Acta Zool. (Stockholm) 80, 125-134.
54. Lanctot, C., Lamolet, B. and Drouin, J. (1997). The bicoid-related homeoprotein Ptx1 defines the most anterior domain of the embryo and differentiates posterior from anterior lateral mesoderm. Development 124, 2807-2817.
55. Li, X., Oghi, K. A., Zhang, J., Krones, A., Bush, K. T., Glass, C. K., Nigam, S. K., Aggarwal, A. K., Maas, R., Rose, D. W. et al. (2003). Eya protein phosphatase activity regulates Six1-Dach-Eya transcriptional effects in mammalian organogenesis. Nature 426, 247-254.
56. Liu, C., Liu, W., Lu, M. F., Brown, N. A. and Martin, J. F. (2001). Regulation of left-right asymmetry by thresholds of Pitx2c activity. Development 128, 2039-2048.
57. Liu, D., Chu, H., Maves, L., Yan, Y. L., Morcos, P. A., Postlethwait, J. H. and Westerfield, M. (2003). Fgf3 and Fgf8 dependent and independent transcription factors are required for otic placode specification. Development 130, 2213-2224.
58. Lohmann, H. (1933). Erste Klasse der Tunicaten: Appendiculariae. In Handbuch der Zoologie, Vol. 5 (ed. W. Kükenthal and T. Krumbach). Berlin and Leipzig: Walter De Gruyter and Company.
59. Manni, L., Caicci, F., Gasparini, F., Zaniolo, G. and Burighel, P. (2004a). Hair cells in ascidians and the evolution of lateral line placodes. Evol. Dev. 6, 379-381.
60. Manni, L., Lane, N. J., Joly, J. S., Gasparini, F., Tiozzo, S., Caicci, F., Zaniolo, G. and Burighel, P. (2004b). Neurogenic and non-neurogenic placodes in ascidians. J. Exp. Zoolog. B Mol. Dev. Evol. 302, 483-504.
61. Manni, L., Lane, N. J., Sorrentino, M., Zaniolo, G. and Burighel, P. (1999). Mechanism of neurogenesis during the embryonic development of a tunicate. J. Comp. Neurol. 412, 527-541.
62. Maroney, P. A., Denker, J. A., Darzynkiewicz, E., Laneve, R. and Nilsen, T. W. (1995). Most mRNAs in the nematode Ascaris lumbricoides are trans-spliced: a role for spliced leader addition in translational efficiency. RNA 1, 714-723.
63. Martini, E. (1909). Studien uber die Konstanz histologischer Elemente, I. Oikopleura longicauda. Z. Wiss. Zool. 92, 563-626.
64. Mazet, F., Hutt, J. A., Milloz, J., Millard, J., Graham, A. and Shimeld, S. M. (2005). Molecular evidence from Ciona intestinalis for the evolutionary origin of vertebrate sensory placodes. Dev. Biol. 282, 494-508.
65. Meijlink, F., Beverdam, A., Brouwer, A., Oosterveen, T. C. and ten Berge, D. (1999). Vertebrate aristaless-related genes. Int. J. Dev. Biol. 43, 651-663.
66. Muske, L. E. (1993). Evolution of gonadotropin-releasing hormone (GnRH) neuronal systems. Brain Behav. Evol. 42, 215-230.
67. Northcutt, R. G. (1996). The origin of craniates: neural crest, neurogenic placodes, and homeobox genes. Israel J. Zool. 42, S273-S313.
68. Northcutt, R. G. and Gans, C. (1983). The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. Quart. Rev. Biol. 58, 1-28.
69. Nozaki, M. and Gorbman, A. (1992). The question of functional homology of Hatschek's pit of amphioxus (Branchiostoma belcheri) and the vertebrate adenohypophysis. Zool. Sci. 9, 387-395.
70. Ohto, H., Kamada, S., Tago, K., Tominaga, S. I., Ozaki, H., Sato, S. and Kawakami, K. (1999). Cooperation of Six and Eya in activation of their target genes through nuclear translocation of Eya. Mol. Cell. Biol. 19, 6815-6834.
71. Oliver, G., Mailhos, A., Wehr, R., Copeland, N. G., Jenkins, N. A. and Gruss, P. (1995). Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 121, 4045-4055.
72. Olsson, R. (1969). General review of the endocrinology of the protochordata and myxinoidea. Gen. Comp. Endocrinol. 2, 485-499.
73. Olsson, R. (1990). Evolution of chordate endocrine organs. Prog. Comp. Endocrinol. 342, 272-281.
74. Olsson, R., Holmberg, K. and Lilliemark, Y. (1990). Fine structure of the brain and brain nerves of Oikopleura dioica (Urochordata, Appendicularia). Zool. Morphol. 110, 1-7.
75. Pandur, P. D. and Moody, S. A. (2000). Xenopus Six1 gene is expressed in neurogenic cranial placodes and maintained in the differentiating lateral lines. Mech. Dev. 96, 253-257.
76. Pignoni, F., Hu, B., Zavitz, K. H., Xiao, J., Garrity, P. A. and Zipursky, S. L. (1997). The eye-specification proteins So and Eya form a complex and regulate multiple steps in Drosophila eye development. Cell 91, 881-891.
77. Pommereit, D., Pieler, T. and Hollemann, T. (2001). Xpitx3: a member of the Rieg/Pitx gene family expressed during pituitary and lens formation in Xenopus laevis. Mech. Dev. 102, 255-257.
78. Ruppert, E. E. (1990). Structure, ultrastructure and function of the neural gland complex of Ascidia interrupta (Chordata, Ascidiacea): clarification of hypotheses regarding the evolution of the vertebrate anterior pituitary. Acta Zool. (Stockholm) 71, 135-149.
79. Schlosser, G. and Ahrens, K. (2004). Molecular anatomy of placode development in Xenopus laevis. Dev. Biol. 271, 439-466.
80. Schweickert, A., Campione, M., Steinbeisser, H. and Blum, M. (2000). Pitx2 isoforms: involvement of Pitx2c but not Pitx2a or Pitx2b in vertebrate left-right asymmetry. Mech. Dev. 90, 41-51.
81. Schweickert, A., Steinbeisser, H. and Blum, M. (2001). Differential gene expression of Xenopus Pitx1, Pitx2b and Pitx2c during cement gland, stomodeum and pituitary development. Mech. Dev. 107, 191-194.
82. Seo, H.-C., Curtiss, J., Mlodzik, M. and Fjose, A. (1999). Six class homeobox genes in Drosophila belong to three distinct families and are involved in head development. Mech. Dev. 83, 127-139.
83. Seo, H. C., Edvardsen, R. B., Maeland, A. D., Bjordal, M., Jensen, M. F., Hansen, A., Flaat, M., Weissenbach, J., Lehrach, H., Wincker, P. et al. (2004). Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 431, 67-71.
84. Shimeld, S. M. and Holland, P. W. (2000). Vertebrate innovations. Proc. Natl. Acad. Sci. USA 97, 4449-4452.
85. Streit, A. (2004). Early development of the cranial sensory nervous system: from a common field to individual placodes. Dev. Biol. 276, 1-15.
86. Suh, H., Gage, P. J., Drouin, J. and Camper, S. A. (2002). Pitx2 is required at multiple stages of pituitary organogenesis: pituitary primordium formation and cell specification. Development 129, 329-337.
87. Takor, T. and Pearse, A. G. E. (1975). Neuroectodermal origin of avian hypothalamus-hypophyseal complex: the role of the ventral neural ridge. J. Embryol. Exp. Morphol. 34, 311-325.
88. Tremblay, J. J., Goodyer, C. G. and Drouin, J. (2000). Transcriptional properties of Ptx1 and Ptx2 isoforms. Neuroendocrinology 71, 277-286.
89. Wada, H., Saiga, H., Satoh, N. and Holland, P. W. H. (1998). Tripartite organization of the ancestral chordate brain and the antiquity of placodes: insights from ascidian Pax2/5/8, Hox and Otx genes. Development 125, 1113-1122.
90. Whitlock, K. E. and Westerfield, M. (2000). The olfactory placodes of the zebrafish form by convergence of cellular fields at the edge of the neural plate. Development 127, 3645-3653.
91. Whitlock, K. E., Wolf, C. D. and Boyce, M. L. (2003). Gonadotropin-releasing hormone (GnRH) cells arise from cranial neural crest and adenohypophyseal regions of the neural plate in the zebrafish, Danio rerio. Dev. Biol. 257, 140-152.
92. Wirsig-Wiechmann, C. R. (2001). Function of gonadotropin-releasing hormone in olfaction. Keio J. Med. 50, 81-85.
93. Xu, P.-X., Woo, I., Her, H., Beier, D. R. and Maas, R. L. (1997). Mouse Eya homologues of the Drosophila eyes absent gene require Pax-6 for expression in the lens and nasal placode. Development 124, 219-231.
94. Yasui, K., Zhang, S., Uemura, M. and Saiga, H. (2000). Left-right asymmetric expression of BpPtx, a Ptx-related gene, in a lancelet species and the developmental left-sidedness in deuterostomes. Development 127, 187-195.
95. Zeiner, G. M., Sturm, N. R. and Campbell, D. A. (2003). The Leishmania tarentolae spliced leader contains determinants for association with polysomes. J. Biol. Chem. 278, 38269-38275.
96. Zheng, W., Huang, L., Wei, Z. B., Silvius, D., Tang, B. and Xu, P. X. (2003). The role of Six1 in mammalian auditory system development. Development 130, 3989-4000.