Sequencing and analysis of the gastrula transcriptome of the brittle star Ophiocoma wendtii

EvoDevo

Volumn 3, Issue 1, 2012, Pages

  Vaughn, Roy ^a   Garnhart, Nancy ^b   Garey, James R ^a   Thomas, W K ^b   Livingston, Brian T ^c  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF NEW HAMPSHIRE   (United States)

^c CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Brittle star; Evolution; Gene regulatory networks; Transcriptome

Indexed keywords

ECHINODERMATA; ECHINOIDEA; OPHIOCOMA WENDTII; OPHIUROIDEA; PLUTEUS; STRONGYLOCENTROTUS PURPURATUS;

EID: 84868703951     PISSN: None     EISSN: 20419139     Source Type: Journal    
DOI: 10.1186/2041-9139-3-19     Document Type: Article

References (65)

1. Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C, Yuh CH, Minokawa T, Amore G, Hinman V, Arenas-Mena C, Otim O, Brown CT, Livi CB, Lee PY, Revilla R, Rust AG, Pan Z, Schilstra MJ, Clarke PJ, Arnone MI, Rowen L, Cameron RA, McClay DR, Hood L, Bolouri H. A genomic regulatory network for development. Science 2002, 295:1669-1678. 10.1126/science.1069883, 11872831.
2. Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C, Yuh CH, Minokawa T, Amore G, Hinman V, Arenas-Mena C, Otim O, Brown CT, Livi CB, Lee PY, Revilla R, Schilstra MJ, Clarke PJ, Rust AG, Pan Z, Arnone MI, Rowen L, Cameron RA, McClay DR, Hood L, Bolouri H. A provisional regulatory gene network for specification of endomesoderm in the sea urchin embryo. Dev Biol 2002, 246:162-190. 10.1006/dbio.2002.0635, 12027441.
3. Oliveri P, Davidson EH. Gene regulatory network controlling embryonic specification in the sea urchin. Curr Opin Genet Dev 2004, 204:351-380.
4. Su YH. Gene regulatory networks for ectoderm specification in sea urchin embryos. Biochim Biophys Acta 2009, 1789:261-267. 10.1016/j.bbagrm.2009.02.002, 19429544.
5. Peter IS, Davidson EH. The endoderm gene regulatory network in sea urchin embryos up to mid-blastula stage. Dev Biol 2010, 340:188-199. 10.1016/j.ydbio.2009.10.037, 19895806.
6. Cameron RA, Samanta M, Yuan A, He D, Davidson E. SpBase: the sea urchin genome database and web site. Nucleic Acids Res 2009, 37:D750-D754. http://spbase.org, 10.1093/nar/gkn887, 2686435, 19010966.
7. Sea Urchin Genome Sequencing Consortium The genome of the sea urchin Strongylocentrotus purpuratus. Science 2006, 314:941-952. 3159423, 17095691, Sea Urchin Genome Sequencing Consortium.
8. Poustka AJ, Herwig R, Krause A, Hennig S, Meier-Ewert S, Lehrach H. Toward the gene catalogue of sea urchin development: the construction and analysis of an unfertilized egg cDNA library highly normalized by oligonucleotide fingerprinting. Genomics 1999, 59:122-133. 10.1006/geno.1999.5852, 10409423.
9. Lee YH, Huang GM, Cameron RA, Graham G, Davidson EH, Hood L, Britten RJ. EST analysis of gene expression in early cleavage-stage sea urchin embryos. Development 1999, 126:3857-3867.
10. Zhu X, Mahairas G, Illies M, Cameron RA, Davidson EH, Ettensohn CA. A large-scale analysis of mRNAs expressed by primary mesenchyme cells of the sea urchin embryo. Development 2001, 128:2615-2627.
11. Poustka AJ, Groth D, Hennig S, Thamm S, Cameron A, Beck A, Reinhardt R, Herwig R, Panopoulou G, Lehrach H. Generation, annotation, evolutionary analysis, and database integration of 20,000 unique sea urchin EST clusters. Genome Res 2003, 13:2736-2746. 10.1101/gr.1674103, 403816, 14656975.
12. Wei Z, Angerer RC, Angerer LM. A database of mRNA expression patterns for the sea urchin embryo. Dev Biol 2006, 300:476-484. 10.1016/j.ydbio.2006.08.034, 1762123, 17007833.
13. Materna SC, Nam J, Davidson EH. High accuracy, high-resolution prevalence measurement for the majority of locally expressed regulatory genes in early sea urchin development. Gene Expr Patterns 2010, 10:177-184. 10.1016/j.gep.2010.04.002, 2902461, 20398801.
14. Paul CRC, Smith AB. The early radiation and phylogeny of echinoderms. Biol Rev 1984, 59:443-481.
15. Littlewood DTJ, Smith AB, Clough KA, Emson RH. The interrelationships of the echinoderm classes: morphological and molecular evidence. Biol J Linnean Soc 1997, 61:409-438.
16. Harmon MC. The position of the ophiuroidea within the phylum echinodermata 2005, University of South Florida, Biology Department.
17. Davidson EH, Erwin DH. Gene regulatory networks and the evolution of animal body plans. Science 2006, 311:796-800. 10.1126/science.1113832, 16469913.
18. Hinman VF, Davidson EH. Evolutionary plasticity of developmental gene regulatory network architecture. Proc Natl Acad Sci USA 2007, 104:19404-19409. 10.1073/pnas.0709994104, 2148302, 18042699.
19. Gao F, Davidson EH. Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution. Proc Natl Acad Sci USA 2008, 105:6091-6096. 10.1073/pnas.0801201105, 2329712, 18413604.
20. Wilt FH, Ettensohn CA. Handbook of Biomineralization. The morphogenesis and biomineralization of the sea urchin larval skeleton 2007, 183-210. Weinheim Germany: Wiley-VCH, Bauerlin E.
21. Ettensohn CA. Lessons from a gene regulatory network: echinoderm skeletogenesis provides insights into evolution, plasticity and morphogenesis. Development 2009, 136:11-21. 10.1242/dev.023564, 19060330.
22. Wray GA, McClay DR. The origin of spicule-forming cells in a " primitive" sea urchin (Eucidares tribloides) which appears to lack primary mesenchyme cells. Development 1988, 103:305-315.
23. Meyer E, Aglyamova GV, Wang S, Buchanan-Carter J, Abrego D, Colbourne JK, Willis BL, Matz MV. Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx. BMC Genomics 2009, 10:219. 10.1186/1471-2164-10-219, 2689275, 19435504.
24. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
25. Lerat E, Daubin V, Ochman H, Moran NA. Evolutionary origins of genomic repertoires in bacteria. PLoS Biol 2005, 3:e130. 10.1371/journal.pbio.0030130, 1073693, 15799709.
26. Cooper VS, Vohr SH, Wrocklage SC, Hatcher PJ. Why genes evolve faster on secondary chromosomes in bacteria. PLoS Comput Biol 2010, 6:e1000732. 10.1371/journal.pcbi.1000732, 2848543, 20369015.
27. Flynn KM, Vohr SH, Hatcher PJ, Cooper VS. Evolutionary rates and gene dispensability associate with replication timing in the archaeon Sulfolobus islandicus. Genome Biol Evol 2010, 2:859-869. 10.1093/gbe/evq068, 3000693, 20978102.
28. Garnhart N, Bergeron RD. Homology Inspector (HomIn): A Tool for Exploring Homology http://www.cs.unh.edu/~rdb/reports/homin.pdf.
29. Kanehisam K, Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 2000, 28:27-30. 10.1093/nar/28.1.27, 102409, 10592173.
30. Tatusov RL, Koonin EV, Lipman DJ. A genomic perspective on protein families. Science 1997, 278:631-637. 10.1126/science.278.5338.631, 9381173.
31. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA. The COG database: an updated version includes eukaryotes. BMC Bioinforma 2003, 4:41.
32. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet 2000, 25:25-29. 10.1038/75556, 3037419, 10802651.
33. EcoSim: null models software for ecology Version 7. 2011 http://garyentsminger.com/ecosim.htm, EcoSim: null models software for ecology.
34. UniGene sea urchin embryo cDNA libraries http://www.ncbi.nlm.nih.gov/UniGene/lbrowse2.cgi?TAXID=7668&CUTOF F=1000.
35. KEGG Orthology Database http://www.genome.jp/kegg/ko.html.
36. Whittaker CA, Bergeron KF, Whittle J, Brandhorst BP, Burke RD, Hynes RO. The echinoderm adhesome. Dev Biol 2006, 300:252-266. 10.1016/j.ydbio.2006.07.044, 16950242.
37. Smith J, Theodoris C, Davidson EH. A gene regulatory network subcircuit drives a dynamic pattern of gene expression. Science 2007, 318:794-797. 10.1126/science.1146524, 17975065.
38. Smith J, Kraemer E, Liu H, Theodoris C, Davidson E. A spatially dynamic cohort of regulatory genes in the endomesodermal gene network of the sea urchin embryo. Dev Biol 2008, 313:863-875. 10.1016/j.ydbio.2007.10.042, 18061160.
39. Hinman VF, Nguyen AT, Cameron A, Davidson EH. Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proc Natl Acad Sci USA 2003, 100:13356-13361. 10.1073/pnas.2235868100, 263818, 14595011.
40. Maruyama YK. A sea cucumber homolog of the mouse T-Brain-1 is expressed in the invaginated cells of the early gastrula in Holothuria leucospilota. Zoolog Sci 2000, 17:383-387.
41. Tagawa K, Humphreys T, Satoh N. T-Brain expression in the apical organ of hemichordate tornaria larvae suggests its evolutionary link to the vertebrate forebrain. J Exp Zool B Mol Dev Evol 2000, 288:23-31.
42. Hinman VF, Nguyen A, Davidson EH. Caught in the evolutionary act: precise cis-regulatory basis of difference in the organization of gene networks of sea stars and sea urchins. Dev Biol 2007, 312:584-595. 10.1016/j.ydbio.2007.09.006, 17956756.
43. Minemura K, Yamaguchi M, Minokawa T. Evolutionary modification of T- brain (tbr) expression patterns in sand dollar. Gene Expr Patterns 2009, 9:468-474. 10.1016/j.gep.2009.07.008, 19635588.
44. Patient RK, McGhee JD. The GATA family (vertebrates and invertebrates). Curr Opin Genet Dev 2002, 12:416-422. 10.1016/S0959-437X(02)00319-2, 12100886.
45. Yuh CW, Dorman ER, Howard ML, Davidson EH. An otx cis-regulatory module: a key node in the sea urchin endomesoderm gene regulatory network. Dev Biol 2004, 269:536-551. 10.1016/j.ydbio.2004.02.025, 15110718.
46. Howard EW, Newman LA, Oleksyn DW, Angerer RC, Angerer LM. SpKrl: a direct target of β-catenin regulation required for endoderm differentiation in sea urchin embryos. Development 2001, 128:365-375.
47. Peter IS, Davidson EH. A gene regulatory network controlling the embryonic specification of endoderm. Nature 2011, 474:635-639. 10.1038/nature10100, 21623371.
48. Peterson KJ, Harada Y, Cameron RA, Davidson EH. Expression Pattern of Brachyury and Not in the Sea Urchin: Comparative Implications for the Origins of Mesoderm in the Basal Deuterostomes. Dev Biol 1999, 207:419-431. 10.1006/dbio.1998.9177, 10068473.
49. Shoguchi E, Satoh N, Maruyama YK. Pattern of Brachyury gene expression in starfish embryos resembles that of hemichordate embryos but not of sea urchin embryos. Mech Dev 1999, 82:185-189. 10.1016/S0925-4773(99)00008-8, 10354483.
50. Mitsunaga-Nakatsubo K, Harada Y, Satoh N, Shimada H, Akasaka K. Brachyury homolog (HpTa) is involved in the formation of archenteron and secondary mesenchyme cell differentiation in the sea urchin embryo. Zoology 2001, 104:99-102. 10.1078/0944-2006-2410018, 16351823.
51. Gross JM, McClay DR. The role of Brachyury (T) during gastrulation movements in the sea urchin Lytechinus variegatus. Dev Biol 2001, 239:132-147. 10.1006/dbio.2001.0426, 11784024.
52. Ettensohn CA, Kitazawa C, Cheers MS, Leonard JD, Sharma T. Gene regulatory networks and developmental plasticity in the early sea urchin embryo: alternative deployment of the skeletogenic gene regulatory network. Development 2007, 134:3077-3087. 10.1242/dev.009092, 17670786.
53. McCauley BS, Weideman EP, Hinman VF. A conserved gene regulatory network subcircuit drives different developmental fates in the vegetal pole of highly divergent echinoderm embryos. Dev Biol 2010, 340:200-208. 10.1016/j.ydbio.2009.11.020, 19941847.
54. Livingston BT, Killian CE, Wilt F, Cameron A, Landrum MJ, Ermolaeva O, Sapojnikov V, Maglott DR, Buchanan AM, Ettensohn CA. A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purpuratus. Dev Biol 2006, 300:335-348. 10.1016/j.ydbio.2006.07.047, 16987510.
55. Mann K, Poustka AJ, Mann M. The sea urchin (Strongylocentrotus purpuratus) test and spine proteomes. Proteome Sci 2008, 6:22. 10.1186/1477-5956-6-22, 2527298, 18694502.
56. Mann K, Wilt FH, Poustka AJ. Proteomic analysis of sea urchin (Strongylocentrotus purpuratus) spicule matrix. Proteome Sci 2010, 8:33. 10.1186/1477-5956-8-33, 2909932, 20565753.
57. Ransick A, Davidson EH. cis-regulatory processing of Notch signaling input to the sea urchin glial cells missing gene during mesoderm specification. Dev Biol 2006, 297:587-602. 10.1016/j.ydbio.2006.05.037, 16925988.
58. Croce JC, McClay DR. Dynamics of Delta/Notch signaling on endomesoderm segregation in the sea urchin embryo. Development 2010, 137:83-91. 10.1242/dev.044149, 2796929, 20023163.
59. Duboc V, Lepage T. A conserved role for the nodal signaling pathway in the establishment of dorso-ventral and left-right axes in deuterostomes. J Exp Zool B Mol Dev Evol 2008, 310B:41-53.
60. Duboc V, Lapraz F, Besnardeau L, Lepage T. Lefty acts as an essential modulator of Nodal activity during sea urchin oral-aboral axis formation. Dev Biol 2008, 320:49-59. 10.1016/j.ydbio.2008.04.012, 18582858.
61. Saudemont A, Haillot E, Mekpoh F, Bessodes N, Quirin M, Lapraz F, Duboc V, Röttinger E, Range R, Oisel A, Besnardeau L, Wincker P, Lepage T. Ancestral regulatory circuits governing ectoderm patterning downstream of nodal and BMP2/4 revealed by gene regulatory network analysis in an Echinoderm. PLoS Genet 2010, 6(12):1-31.
62. Lapraz F, Besnardeau L, Lepage T. Patterning of the dorsal-ventral axis in echinoderms: insights into the evolution of the BMP-chordin signaling network. PLoS Biol 2009, 7:e1000248. 10.1371/journal.pbio.1000248, 2772021, 19956794.
63. Bradham CA, Oikonomou C, Kühn A, Core AB, Modell JW, McClay DR, Poustka AJ. Chordin is required for neural but not axial development in sea urchin embryos. Dev Biol 2009, 328:221-233. 10.1016/j.ydbio.2009.01.027, 2700341, 19389361.
64. Revilla-i-Domingo R, Oliveri P, Davidson EH. A missing link in the sea urchin embryo gene regulatory network: hesC and the double-negative specification of micromeres. Proc Natl Acad Sci USA 2007, 104:12383-12388. 10.1073/pnas.0705324104, 1941478, 17636127.
65. Sharma T, Ettensohn CA. Activation of the skeletogenic gene regulatory network in the early sea urchin embryo. Development 2010, 137:1149-1157. 10.1242/dev.048652, 20181745.