Evolution of OTP-Independent Larval Skeleton Patterning in the Direct-Developing Sea Urchin, Heliocidaris erythrogramma

Journal of Experimental Zoology Part B: Molecular and Developmental Evolution

Volumn 300, Issue 1, 2003, Pages 58-71

  Zhou, Na ^a   Wilson, Keen A ^a,b   Andrews, Mary E ^a   Kauffman, Jeffery S ^a   Raff, Rudolf A ^a,c  

^a INDIANA UNIVERSITY   (United States)

^b University of Georgia ^*  (United States)

^c 150 Myers Hall ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECHINOIDEA; HELIOCIDARIS ERYTHROGRAMMA; HELIOCIDARIS TUBERCULATA;

EID: 0346344053     PISSN: 0022104X     EISSN: None     Source Type: Journal    
DOI: 10.1002/jez.b.46     Document Type: Article

References (63)

1. Angerer LM, Angerer RC. 1991. Localization of mRNAs by in situ hybridization. Methods Cell Biol 35: 37-71.
2. Armstrong N, McClay DR. 1994. Skeletal pattern is specified autonomously by the primary mesenchyme cells in sea urchin embryos. Dev Biol 162: 329-338.
3. Armstrong N, Hardin J, McClay DR. 1993. Cell-cell interactions regulate skeleton formation in the sea urchin embryo. Development 119: 883-840.
4. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K, editors. 1988. Current Protocols in Molecular Biology. New York: Greene Publishing Associates and Wiley-Interscience.
5. Badiani P, Corbella P, Kioussis D, Marvel J, Weston K. 1994. Dominant interfering alleles define a role for c-Myb in T-cell development. Genes Dev 8: 770-782.
6. Bisgrove BW, Raff RA. 1993. The SpEGF III gene encodes a member of the fibropellins: EGF repeat-containing proteins that form the apical lamina of the sea urchin embryo. Dev Biol 157: 526-538.
7. Cameron RA, Zeller RW, Coffman JA, Davidson EH. 1996. Microinjection of sea urchin eggs. In: Ferraris JD, Palumbi SR, editors. Molecular Zoology Advances, Strategies, and Protocols. Hoboken, New Jersey: John Wiley and Sons, Inc. p 441-442.
8. Celi FS, Zenilman ME, Shuldiner AR. 1993. A rapid and versatile method to synthesize internal standards for competitive PCR. Nucleic Acids Res 21: 1047.
9. Chapman DM. 1977. Eriochrome Cyanin as a Substitute for Haematoxylin and Eosin. Canad J Med Tech 39: 65-66.
10. Chomcynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159.
11. Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C, Yuh C-H, Minokawa T, Amore G, Hinman V, Arenas-Mena C, Otim O, Brown CT, Livi CB, Lee PY, Revilla R, Schilstra MJ, Clarke PJC, Rust AG, Pan Z, Arnone MI, Rowen L, Cameron RA, McClay DR, Hood L, Bolouri H. 2002. A Provisional Regulatory Gene Network for Specification of Endomesoderm in the Sea Urchin Embryo. Dev Biol 246: 162-190.
12. Di Bernardo M, Castagnetti S, Bellomonte D, Oliveri P, Melfi R, Palla F, Spinelli G. 1999. Spatially restricted expression of PlOtp, a Paracentrotus lividus Orthopedia related homeobox gene, is correlated with oral ectodermal patterning and skeletal morphogenesis in late-cleavage sea urchin embryos. Development 126: 2171-2179.
13. Dobias SL, Ma L, Wu H, Bell JR, Maxon R. 1997. The evolution of Msx gene function: expression and regulation of a sea urchin Msx class homeobox gene. Mech Dev 61: 37-48.
14. Emlet RB. 1995. Larval spicules, cilia, and symmetry as remnants of indirect development in the direct developing sea urchin Heliocidaris erythrogramma. Dev Biol 167: 405-415.
15. Emlet RB, McEdward LR, Strathmann RR. 1987. Echinoderm larval ecology viewed from the egg. In: Jangoux M, Lawrence JM, editors. Echinoderm Studies, Vol 2. Rotterdam: Balkema. p 55-136.
16. Ettensohn CA. 1990. The regulation of primary mesenchyme cell patterning. Dev Biol 140: 261-271.
17. Ettensohn CA, Malinda KM. 1993. Size regulation and morphogenesis: a cellular analysis of skeletogenesis in the sea urchin embryo. Development 119: 155-167.
18. Ettensohn CA, Guss KA, Hodor PG, Malinda KM. 1997. The morphogenesis of the skeletal system of the sea urchin embryo. In: Collier JR, editors. Reproductive Biology of Invertebrates, Vol. VII. New Delhi: Oxford and IBH Publishing Co. Pvt. Ltd. p 225-265.
19. Galliot B, de Vargas C, Miller D. 1999. Evolution of homeobox genes: Q50 Paired-like genes founded the Paired class. Dev Genes Evol 209: 186-197.
20. Gilliland G, Perrin S, Blanchard K, Bunn HF. 1990. Analysis of cytokine mRNA and DNA: detection and quantitation by competitive polymerase chain reaction. Proc Natl Acad Sci USA 87: 2725-2729.
21. Guss KA, Ettensohn CA. 1997. Skeletal morphogenesis in the sea urchin embryo: regulation of primary mesenchyme gene expression and skeletal rod growth by ectoderm derived cues. Development 124: 1899-1908.
22. Haag ES, Raff RA. 1998. Isolation and characterization of three mRNAs enriched in embryos of the direct-developing sea urchin Heliocidaris erythrogramma: evolution of larval ectoderm. Dev Genes Evol 208: 188-204.
23. Han K, Manley JL. 1993. Functional domains of the Drosophila engrailed protein. EMBO J 12: 2723-2733.
24. 2. Development 116: 671-685.
25. Harkey MA, Whiteley AH. 1980. Isolation, culture, and differentiation of echinoid primary mesenchyme cells. Wilhelm Roux's Arch 189: 111-122.
26. Hodor PG, Ettensohn CA. 1998. The dynamics and regulation of mesenchymal cell fusion in the sea urchin embryo. Dev Biol 199: 111-124.
27. Jungblut B, Pires-daSilva A, Sommer RJ. 2001. Formation of the egg-laying system in Pristionchus pacificus requires complex interactions between gonadal, mesodermal, and epidermal tissues and does not rely on single cell inductions. Development 128: 3395-3404.
28. Kauffman JS, Raff RA. 2003. Patterning mechanisms in the evolution of derived developmental life histories: the role of Wnt signaling in axis formation of the direct developing sea urchin Heliocidaris erythrogramma. Dev Genes Evo. in press.
29. Kessler DS. 1997. Siamois is required for formation of Spemann's organizer. Proc Natl Acad Sci USA 94: 13017-13022.
30. Kissinger JC, Raff RA. 1998. Evolutionary changes in sites and timing of actin gene expression in embryos of the direct-and indirect-developing sea urchins, Heliocidaris erythrogramma and H. tuberculata. Dev Genes Evol 208: 82-93.
31. Kissinger JC, Hahn JH, Raff RA. 1997. Rapid evolution in a conserved gene family. Evolution of the actin gene family in the sea urchin genus Heliocidaris and related genera. Mol Biol Evol 14:654-665.
32. Klueg KM, Harkey MA, Raff RA. 1997. Mechanisms of evolutionary changes in timing, spatial expression, and mRNA processing in the msp130 gene in a direct-developing sea urchin, Heliocidaris erythrogramma. Dev Biol 182: 121-133.
33. Leaf DS, Anstrom JA, Chin JE, Harkey MA, Showman RM, Raff RA. 1987. Antibodies to a fusion protein identify a cDNA clone encoding msp 130, a primary mesenchyme specific cell surface protein of the sea urchin embryo. Dev Biol 121: 29-40.
34. Li X, Wikramanayake AH, Klein WH. 1999. Requirement of SpOtx in cell fate decisions in the sea urchin embryo and possible role as a mediator of beta-catenin signaling. Dev Biol 212: 425-439.
35. Lin X, State MW, Vaccarino FM, Greally J, Hass M, Leckman JF. 1999. Identification, chromosomal assignment, and expression analysis of the human homeodomain containing gene Orthopedia (OTP). Genomics 60: 96-104.
36. Malinda KM, Ettensohn CA. 1994. Primary mesenchyme cell migration in the sea urchin embryo: distribution of directional cues. Dev Biol 164: 562-578.
37. Nedelman J, Heagerty P, Lawrence C. 1992. Quantitative PCR with internal controls. Comput Appl Biosci 8: 65-70.
38. Nederbragt AJ, de Welscher P, van den Driesche S, van Loon AE, Dictus WJ. 2002. Novel and conserved roles for orthodenticle/ otx and orthopedia/ otp orthologs in the gastropod mollusc Patella vulgata. Dev Genes Evol 212: 330-337.
39. Nielsen MG, Wilson KA, Raff EC, Raff RA. 2000. Novel gene expression patterns in hybrid embryos between species with different modes of development. Evol Dev 2: 133-144.
40. Okazaki K. 1975a. Normal development to metamorphosis. In: Czihak G, editor. The Sea Embryo: Biochemistry and Morphogenesis. New York: Springer-Verlag, p 177-232.
41. Okazaki K. 1975b. Spicule formation by isolated micromeres of the sea urchin embryo. Am Zool 15: 567-581.
42. Parks AL, Parr BA, Chin J-E, Leaf DS, Raff RA. 1988. Molecular analysis of heterochronic changes in the evolution of direct developing sea urchins. J Evol Biol 1: 27-44.
43. Pires-da Silva A, Sommer RJ. 2003. The evolution of signaling pathways in animal development. Nature Rev Gen 4: 39-49.
44. Raff RA. 1987. Constraint, flexibility, and phylogenetic change in the evolution of direct development in sea urchins. Dev Biol 119: 6-19.
45. Raff RA. 1996. The Shape of Life: Genes, Development, and the Evolution of Animal Form. Chicago: University of Chicago Press.
46. Raff RA, Sly BJ. 2000. Modularity and dissociation in the evolution of gene expression territories in development. Evol Dev 2: 102-113.
47. Raff EC, Popodi EM, Sly BJ, Turner FR, Villinski JT, Raff RA. 1999. A novel ontogenetic pathway in hybrid embryos between species with different modes of development. Development 126: 1937-1945.
48. Raff EC, Popodi EM, Kauffman JS, Sly BJ, Turner FR, Morris VB, Raff RA. 2003. Regulatory punctuated equilibrium and convergence in the evolution of developmental pathways in direct-developing sea urchins. Evo Dev 5: 478-493.
49. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
50. Schneeberger C, Speiser P, Kury F, Zeillinger R. 1995. Quantitative detection of reverse transcriptase-PCR products by means of a novel and sensitive DNA stain. PCR Methods Appl 4: 234-238.
51. Siebert PD, Larrick JW. 1992. Competitive PCR. Nature 359: 557-558.
52. Simeone A, D'Apice MR, Nigro V, Casanova J, Graziani F, Acampora D, Avantaggiato V. 1994. Orthopedia, a novel homeobox-containing gene expressed in the developing CNS of both mouse and Drosophila. Neuron 13: 83-101.
53. Stander MC. 1999. Regulation and evolution of skeletogenesis in sea urchin development. Masters Thesis, Indiana University.
54. Stauber M, Prell A, Schmidt-Ott U. 2002. A single Hox3 gene with composite bicoid and zerknult expression characteristics in non-Cyclorrhaphan flies. Proc Natl Acad Sci USA 99: 274-279.
55. Strathmann RR. 1978. The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32: 894-906.
56. Tan H, Ransick A, Wu H, Dobias S, Liu YH, Maxson R. 1998. Disruption of primary mesenchyme cell patterning by misregulated ectodermal expression of SpMsx in sea urchin embryos. Dev Biol 201: 230-246.
57. Taylor RC, Shi SR, Chen C, Young L, Yang C, Cote RJ. 1996. Comparative study of antigen retrieval heating methods: microwave, microwave and pressure cooker, autoclave, and steamer. Biotech Histochem 71: 263-270.
58. Triezenberg SJ, Kingsbury RC, McKnight SL. 1988. Functional dissection of VP16, the trans-activator of herpes simplex virus immediate early gene expression. Genes Dev 2: 718-729.
59. Umesono Y, Watanabe K, Agata K. 1999. Distinct structural domains in the planarian brain defined by the expression of evolutionarily conserved homeobox genes. Dev Genes Evol 209: 31-39.
60. Wagner GP. 1996. Homologies, natural kinds and the evolution of modularity. Amer Zool 36: 36-43.
61. Wang W, Lufkin T. 2000. The murine Otp homeobox gene plays an essential role in the specification of neuronal cell lineages in the developing hypothalamus. Dev Biol 227: 432-449.
62. Wray GA. 1999. Evolutionary dissociations between homologous genes and homologous structures. Novartis Found Symp 222:189-203; discussion 203-206.
63. Zigler KS, Raff EC, Popodi E, Raff RA, Lessios HE. 2003. Adaptive evolution of binding in the genus Heliocidaris is correlated with the shift to direct development. Evolution 57: 2293-2302.