Unfolding a chordate developmental program, one cell at a time: Invariant cell lineages, short-range inductions and evolutionary plasticity in ascidians

Developmental Biology

Volumn 332, Issue 1, 2009, Pages 48-60

  Lemaire, Patrick ^a  

^a CNRS   (France)

Author keywords

ADMP; Ascidian; BMP; Ciona; Embryo; Ephrin; Evolution; FGF; Halocynthia; Induction; Lineage; Nodal

Indexed keywords

EPHRIN; FIBROBLAST GROWTH FACTOR; PROTEIN NODAL;

ASCIDIACEA; CELL DIFFERENTIATION; CELL DIVISION; CELL FATE; CELL INTERACTION; CELL LINEAGE; EMBRYO AXIS; EMBRYO DEVELOPMENT; ENDODERM; EVOLUTIONARY ADAPTATION; GASTRULATION; GENE REGULATORY NETWORK; GENOME; GERM LAYER; MESENCHYME; MOLECULAR EVOLUTION; MORPHOLOGICAL ADAPTATION; MUSCLE DEVELOPMENT; NERVOUS SYSTEM DEVELOPMENT; NEUROECTODERM; NONHUMAN; NOTOCHORD; PRIORITY JOURNAL; REVIEW;

ANIMALIA; ASCIDIA; ASCIDIACEA; CIONA; CIONA INTESTINALIS; HALOCYNTHIA; HALOCYNTHIA RORETZI; METAZOA;

EID: 67650088455     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.05.540     Document Type: Review

References (73)

1. Bertrand V., Hudson C., Caillol D., Popovici C., and Lemaire P. Neural tissue in ascidian embryos is induced by FGF9/16/20, acting via a combination of maternal GATA and Ets transcription factors. Cell 115 (2003) 615-627
2. Bourlat S.J., et al. Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444 (2006) 85-88
3. Chabry L. Embryologie normale et tératologique des Ascidie (1887), Felix Alcan Editeur, Paris
4. Christiaen L., Stolfi A., Davidson B., and Levine M. Spatio-temporal intersection of Lhx3 and Tbx6 defines the cardiac field through synergistic activation of Mesp. Dev. Biol. 328 (2009) 552-560
5. Christiaen L., Davidson B., Kawashima T., Powell W., Nolla H., Vranizan K., and Levine M. The transcription/migration interface in heart precursors of Ciona intestinalis. Science 320 (2008) 1349-1352
6. Conklin E. The organization and cell lineage of the ascidian egg. J. Acad., Nat. Sci. Phila 13 (1905) 1
7. Darras S., and Nishida H. The BMP signaling pathway is required together with the FGF pathway for notochord induction in the ascidian embryo. Development 128 (2001) 2629-2638
8. Davidson B. Ciona intestinalis as a model for cardiac development. Semin. Cell Dev. Biol. 18 (2007) 16-26
9. Davidson B., Shi W., Beh J., Christiaen L., and Levine M. FGF signaling delineates the cardiac progenitor field in the simple chordate, Ciona intestinalis. Genes Dev. 20 (2006) 2728-2738
10. Davidson B., Shi W., and Levine M. Uncoupling heart cell specification and migration in the simple chordate Ciona intestinalis. Development 132 (2005) 4811-4818
11. Dehal P., et al. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298 (2002) 2157-2167
12. Delsuc F., Brinkmann H., Chourrout D., and Philippe H. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439 (2006) 965-968
13. Félix M. An inversion in the wiring of an intercellular signal: evolution of Wnt signaling in the nematode vulva. BioEssays 27 (2005) 765-769
14. Hill M.M., Broman K.W., Stupka E., Smith W.C., Jiang D., and Sidow A. The C. savignyi genetic map and its integration with the reference sequence facilitates insights into chordate genome evolution. Genome Res. 18 (2008) 1369-1379
15. Holland L.Z., and Gibson-Brown J.J. The Ciona intestinalis genome: when the constraints are off. BioEssays 25 (2003) 529-532
16. Hotta K., Mitsuhara K., Takahashi H., Inaba K., Oka K., Gojobori T., and Ikeo K. A web-based interactive developmental table for the ascidian Ciona intestinalis, including 3D real-image embryo reconstructions: I. From fertilized egg to hatching larva. Dev. Dyn. 236 (2007) 1790-1805
17. Hudson C., and Lemaire P. Induction of anterior neural fates in the ascidian Ciona intestinalis. Mech. Dev. 100 (2001) 189-203
18. Hudson C., Darras S., Caillol D., Yasuo H., and Lemaire P. A conserved role for the MEK signalling pathway in neural tissue specification and posteriorisation in the invertebrate chordate, the ascidian Ciona intestinalis. Development 130 (2003) 147-159
19. Hudson C., Lotito S., and Yasuo H. Sequential and combinatorial inputs from Nodal, Delta2/Notch and FGF/MEK/ERK signalling pathways establish a grid-like organisation of distinct cell identities in the ascidian neural plate. Development 134 (2007) 3527-3537
20. Hudson C., and Yasuo H. A signalling relay involving Nodal and Delta ligands acts during secondary notochord induction in Ciona embryos. Development 133 (2006) 2855-2864
21. Hudson C., and Yasuo H. Patterning across the ascidian neural plate by lateral Nodal signalling sources. Development 132 (2005) 1199-1210
22. Hudson C., and Yasuo H. Similarity and diversity in mechanisms of muscle fate induction between ascidian species. Biol. Cell 100 (2008) 265-277
23. Imai K., Takada N., Satoh N., and Satou Y. (beta)-catenin mediates the specification of endoderm cells in ascidian embryos. Development 127 (2000) 3009-3020
24. Imai K.S., Hino K., Yagi K., Satoh N., and Satou Y. Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: towards a comprehensive understanding of gene networks. Development 131 (2004) 4047-4058
25. Imai K.S., Levine M., Satoh N., and Satou Y. Regulatory blueprint for a chordate embryo. Science 312 (2006) 1183-1187
26. Imai K.S., Satoh N., and Satou Y. An essential role of a FoxD gene in notochord induction in Ciona embryos. Development 129 (2002) 3441-3453
27. Imai K.S., Stolfi A., Levine M., and Satou Y. Gene regulatory networks underlying the compartmentalization of the Ciona central nervous system. Development 136 (2009) 285-293
28. Jeffery W.R. Chordate ancestry of the neural crest: new insights from ascidians. Semin. Cell Dev. Biol. 18 (2007) 481-491
29. Kawai N., Iida Y., Kumano G., and Nishida H. Nuclear accumulation of beta-catenin and transcription of downstream genes are regulated by zygotic Wnt5alpha and maternal Dsh in ascidian embryos. Dev. Dyn. 236 (2007) 1570-1582
30. Kim G.J., Yamada A., and Nishida H. An FGF signal from endoderm and localized factors in the posterior-vegetal egg cytoplasm pattern the mesodermal tissues in the ascidian embryo. Development 127 (2000) 2853-2862
31. Kim G.J., Kumano G., and Nishida H. Cell fate polarization in ascidian mesenchyme/muscle precursors by directed FGF signaling and role for an additional ectodermal FGF antagonizing signal in notochord/nerve cord precursors. Development 134 (2007) 1509-1518
32. Kobayashi K., Sawada K., Yamamoto H., Wada S., Saiga H., and Nishida H. Maternal macho-1 is an intrinsic factor that makes cell response to the same FGF signal differ between mesenchyme and notochord induction in ascidian embryos. Development 130 (2003) 5179-5190
33. Kondoh K., Kobayashi K., and Nishida H. Suppression of macho-1-directed muscle fate by FGF and BMP is required for formation of posterior endoderm in ascidian embryos. Development 130 (2003) 3205-3216
34. Kourakis M.J., and Smith W.C. Did the first chordates organize without the organizer?. Trends Genet. 21 (2005) 506-510
35. Kumano G., and Nishida H. Ascidian embryonic development: an emerging model system for the study of cell fate specification in chordates. Dev. Dyn. 236 (2007) 1732-1747
36. Kumano G., Yamaguchi S., and Nishida H. Overlapping expression of FoxA and Zic confers responsiveness to FGF signaling to specify notochord in ascidian embryos. Dev. Biol. 300 (2006) 770-784
37. Kuratani S., Wada H., Kusakabe R., and Agata K. Evolutionary embryology resurrected in Japan with a new molecular basis: Nori Satoh and the history of ascidian studies originating in Kyoto during the 20th century. Int. J. Dev. Biol. 50 (2006) 451-454
38. Lamy C., Rothbächer U., Caillol D., and Lemaire P. Ci-FoxA-a is the earliest zygotic determinant of the ascidian anterior ectoderm and directly activates Ci-sFRP1/5. Development 133 (2006) 2835-2844
39. Lemaire P. Developmental biology. How many ways to make a chordate?. Science 312 (2006) 1145-1146
40. Lemaire P., Smith W.C., and Nishida H. Ascidians and the plasticity of the chordate developmental program. Curr. Biol. 18 (2008) R620-R631
41. Meedel T.H., Farmer S.C., and Lee J.J. The single MyoD family gene of Ciona intestinalis encodes two differentially expressed proteins: implications for the evolution of chordate muscle gene regulation. Development 124 (1997) 1711-1721
42. Meedel T.H., Chang P., and Yasuo H. Muscle development in Ciona intestinalis requires the b-HLH myogenic regulatory factor gene Ci-MRF. Dev. Biol. 302 (2007) 333-344
43. Minokawa T., Yagi K., Makabe K.W., and Nishida H. Binary specification of nerve cord and notochord cell fates in ascidian embryos. Development 128 (2001) 2007-2017
44. Miwata K., Chiba T., Horii R., Yamada L., Kubo A., Miyamura D., Satoh N., and Satou Y. Systematic analysis of embryonic expression profiles of zinc finger genes in Ciona intestinalis. Dev. Biol. 292 (2006) 546-554
45. Morley R.H., Lachani K., Keefe D., Gilchrist M.J., Flicek P., Smith J.C., and Wardle F.C. A gene regulatory network directed by zebrafish No tail accounts for its roles in mesoderm formation. Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 3829-3834
46. Munro E. Asymmetric cell division: a CAB driver for spindle movements. Curr. Biol. 17 (2007) R639-R641
47. Nakamura Y., Makabe K.W., and Nishida H. POPK-1/Sad-1 kinase is required for the proper translocation of maternal mRNAs and putative germ plasm at the posterior pole of the ascidian embryo. Development 132 (2005) 4731-4742
48. Nakamura Y., Makabe K.W., and Nishida H. The functional analysis of Type I postplasmic/PEM mRNAs in embryos of the ascidian Halocynthia roretzi. Dev. Genes Evol. 216 (2006) 69-80
49. Negishi T., Takada T., Kawai N., and Nishida H. Localized PEM mRNA and protein are involved in cleavage-plane orientation and unequal cell divisions in ascidians. Curr. Biol. 17 (2007) 1014-1025
50. Nishida H. Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III. Up to the tissue restricted stage. Dev. Biol. 121 (1987) 526-541
51. Nishida H. Determinative mechanisms in secondary muscle lineages of ascidian embryos: development of muscle-specific features in isolated muscle progenitor cells. Development 108 (1990) 559-568
52. Nishida H., and Sawada K. macho-1 encodes a localized mRNA in ascidian eggs that specifies muscle fate during embryogenesis. Nature 409 (2001) 724-729
53. Nishida H. Spatio-temporal pattern of MAP kinase activation in embryos of the ascidian Halocynthia roretzi. Dev. Growth Differ. 45 (2003) 27-37
54. Nishida H. Specification of embryonic axis and mosaic development in ascidians. Dev. Dyn. 233 (2005) 1177-1193
55. Oda-Ishii I., Bertrand V., Matsuo I., Lemaire P., and Saiga H. Making very similar embryos with divergent genomes: conservation of regulatory mechanisms of Otx between the ascidians Halocynthia roretzi and Ciona intestinalis. Development 132 (2005) 1663-1674
56. Pasini A., Amiel A., Rothbächer U., Roure A., Lemaire P., and Darras S. Formation of the ascidian epidermal sensory neurons: insights into the origin of the chordate peripheral nervous system. PLoS Biol. 4 (2006) e225
57. Picco V., Hudson C., and Yasuo H. Ephrin-Eph signalling drives the asymmetric division of notochord/neural precursors in Ciona embryos. Development 134 (2007) 1491-1497
58. Putnam N.H., et al. The amphioxus genome and the evolution of the chordate karyotype. Nature 453 (2008) 1064-1071
59. Rothbächer U., Bertrand V., Lamy C., and Lemaire P. A combinatorial code of maternal GATA, Ets and beta-catenin-TCF transcription factors specifies and patterns the early ascidian ectoderm. Development 134 (2007) 4023-4032 (the first two authors contributed equally)
60. Roure A., Rothbächer U., Robin F., Kalmar E., Ferone G., Lamy C., Missero C., Mueller F., and Lemaire P. A multicassette Gateway vector set for high throughput and comparative analyses in Ciona and vertebrate embryos. PLoS ONE 2 (2007) e916
61. Sardet C., Paix A., Prodon F., Dru P., and Chenevert J. From oocyte to 16-cell stage: cytoplasmic and cortical reorganizations that pattern the ascidian embryo. Dev. Dyn. 236 (2007) 1716-1731
62. Satou Y., Satoh N., and Imai K.S. Gene Regulatory Networks in the Early Ascidian Embryo. Biochim. Biophys. Acta 1789 (2008) 268-273
63. Shi W., and Levine M. Ephrin signaling establishes asymmetric cell fates in an endomesoderm lineage of the Ciona embryo. Development 135 (2008) 931-940
64. Shirae-Kurabayashi M., Nishikata T., Takamura K., Tanaka K.J., Nakamoto C., and Nakamura A. Dynamic redistribution of vasa homolog and exclusion of somatic cell determinants during germ cell specification in Ciona intestinalis. Development 133 (2006) 2683-2693
65. Small K.S., Brudno M., Hill M.M., and Sidow A. A haplome alignment and reference sequence of the highly polymorphic Ciona savignyi genome. Genome Biol. 8 (2007) R41
66. Strähle U., Lam C.S., Ertzer R., and Rastegar S. Vertebrate floor-plate specification: variations on common themes. Trends Genet. 20 (2004) 155-162
67. Tassy O., Daian F., Hudson C., Bertrand V., and Lemaire P. A quantitative approach to the study of cell shapes and interactions during early chordate embryogenesis. Curr. Biol. 16 (2006) 345-358
68. Tokuoka M., Kumano G., and Nishida H. FGF9/16/20 and Wnt-5alpha signals are involved in specification of secondary muscle fate in embryos of the ascidian, Halocynthia roretzi. Dev. Genes Evol. 217 (2007) 515-527
69. Tomioka M., Miya T., and Nishida H. Repression of zygotic gene expression in the putative germline cells in ascidian embryos. Zoolog. Sci. 19 (2002) 49-55
70. Wada S., Hamada M., Kobayashi K., and Satoh N. Novel genes involved in canonical Wnt/beta-catenin signaling pathway in early Ciona intestinalis embryos. Dev Growth Differ. 50 (2008) 215-227
71. Wilson D., Charoensawan V., Kummerfeld S.K., and Teichmann S.A. DBD-taxonomically broad transcription factor predictions: new content and functionality. Nucleic Acids Res. 36 (2008) D88-D92
72. Yagi K., Satoh N., and Satou Y. Identification of downstream genes of the ascidian muscle determinant gene Ci-macho1. Dev. Biol. 274 (2004) 478-489
73. Yasuo H., and Hudson C. FGF8/17/18 functions together with FGF9/16/20 during formation of the notochord in Ciona embryos. Dev. Biol. 302 (2007) 92-103