Molecular conservation of metazoan gut formation: Evidence from expression of endomesoderm genes in Capitella teleta (Annelida)

EvoDevo

Volumn 5, Issue 1, 2014, Pages

  Boyle, Michael J ^a   Yamaguchi, Emi ^b   Seaver, Elaine C ^c  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^b UNIVERSITY OF HAWAII   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

Digestive system; Endoderm; Gut development; Hybridization; Kernel; Spiralian

Indexed keywords

ANNELIDA; BILATERIA; CAPITELLA; ECHINOIDEA; METAZOA; SPIRALIA;

EID: 84925314856     PISSN: None     EISSN: 20419139     Source Type: Journal    
DOI: 10.1186/2041-9139-5-39     Document Type: Article

References (112)

1. Wilson DB: Considerations of cell-lineage and ancestral reminiscence. Ann NY Acad Sci 1898, 11:1-27. 10.1111/j.1749-6632.1898.tb54960.x
2. Henry JQ, Martindale MQ: Conservation and innovation in spiralian development. Hydrobiologia 1999, 402:255-265.
3. Henry JJ, Martindale MQ, Boyer BC: The unique developmental program of the flatworm, Neochildia fusca. Dev Biol 2000, 220:285-295. 10.1006/dbio.2000.9628
4. Maduro MF, Rothman JH: Making worm guts: the gene regulatory network of the Caenorhabditis elegans endoderm. Dev Biol 2002, 246:68-85. 10.1006/dbio.2002.0655
5. Martindale MQ: The evolution of metazoan axial properties. Nat Rev Genet 2005, 6:917-927. 10.1038/nrg1725
6. Rodaway A, Takeda H, Koshida S, Broadbent J, Price B, Smith JC, Patient R, Holder N: Induction of the mesendoderm in the zebrafish germ ring by yolk cell-derived TGF-beta family signals and discrimination of mesoderm and endoderm by FGF. Development 1999, 126:3067-3078.
7. Stainier DY: A glimpse into the molecular entrails of endoderm formation. Genes Dev 2002, 16:893-907. 10.1101/gad.974902
8. 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
9. Loose M, Patient R: A genetic regulatory network for mesendoderm formation. Dev Biol 2004, 271:467-478. 10.1016/j.ydbio.2004.04.014
10. Davidson EH, Erwin DH: Gene regulatory networks and the evolution of animal body plans. Science 2006, 311:796-800. 10.1126/science.1113832
11. 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
12. Rodaway A, Patient R: Mesendoderm. an ancient germ layer? Cell 2001, 105:169-172. 10.1016/S0092-8674(01)00307-5
13. Peter IS, Davidson EH: A gene regulatory network controlling the embryonic specification of endoderm. Nature 2011, 474:635-639. 10.1038/nature10100
14. Röttinger E, Dahlin P, Martindale MQ: A framework for the establishment of a cnidarian gene regulatory network for "endomesoderm" specification: the inputs of β-catenin/TCF signaling. PLoS Genet 2012, 8:e1003164. 10.1371/journal.pgen.1003164
15. Hinman VF, Nguyen AT, Cameron RA, Davidson EH: Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proc Natl Acad Sci U S A 2003, 100:13356-13361. 10.1073/pnas.2235868100
16. Hinman VF, Davidson EH: Evolutionary plasticity of developmental gene regulatory network architecture. Proc Natl Acad Sci U S A 2007, 104:19404-19409. 10.1073/pnas.0709994104
17. Pires-daSilva A, Sommer RJ: The evolution of signalling pathways in animal development. Nat Rev Genet 2003, 4:39-49. 10.1038/nrg977
18. Nichols SA, Dirks W, Pearse JS, King N: Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci U S A 2006, 103:12451-12456. 10.1073/pnas.0604065103
19. Murakami R, Okumura T, Uchiyama H: GATA factors as key regulatory molecules in the development of Drosophila endoderm. Dev Growth Differ 2005, 47:581-589. 10.1111/j.1440-169X.2005.00836.x
20. Maduro MF: Structure and evolution of the C. elegans embryonic endomesoderm network. Biochim Biophys Acta 2009, 1789:250-260. 10.1016/j.bbagrm.2008.07.013
21. Kirschner M, Gerhart J: Evolvability. Proc Natl Acad Sci U S A 1998, 95:8420-8427. 10.1073/pnas.95.15.8420
22. 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
23. Carroll SB: Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 2008, 134:25-36. 10.1016/j.cell.2008.06.030
24. Sethi AJ, Angerer RC, Angerer LM: Gene regulatory network interactions in sea urchin endomesoderm induction. PLoS Biol 2009, 7:e1000029.
25. Blake JA, Grassle JP, Eckelbarger KJ: Capitella teleta , a new species designation for the opportunistic and experimental Capitella sp. I, with a review of the literature for confirmed records. In Proceedings of the Ninth International Polychaete Conference: 12-18 August 2007; Portland Edited by: Maciolek NJ, Blake JA. 2009. Zoosymposia 2009, 2:25-53
26. Costello DP, Henley C: Spiralian Development: A Perspective. Am Zool 1976, 16:277-291.
27. Meyer NP, Boyle MJ, Martindale MQ, Seaver EC: A comprehensive fate map by intracellular injection of identified blastomeres in the marine polychaete Capitella teleta. EvoDevo 2010, 1:8. 10.1186/2041-9139-1-8
28. Eisig H: Zur Entwicklungsgeschichte der Capitelliden. Mittheilungen Aus Der Zoologischen Station Zu Neapel 1899, 13:1-292.
29. Seaver EC, Thamm K, Hill SD: Growth patterns during segmentation in the two polychaete annelids, Capitella sp. I and Hydroides elegans: comparisons at distinct life history stages. Evol Dev 2005, 7:312-326. 10.1111/j.1525-142X.2005.05037.x
30. Meyer NP, Seaver EC: Neurogenesis in an annelid: characterization of brain neural precursors in the polychaete Capitella sp. I. Dev Biol 2009, 335:237-252. 10.1016/j.ydbio.2009.06.017
31. Boyle MJ, Seaver EC: Evidence of a dorsal pharynx in the marine polychaete Capitella teleta. In Proceedings of the Ninth International Polychaete Conference: 12-18 August 2007; Portland Edited by: Maciolek NJ, Blake JA. Zoosymposia 2009, 2:317-328
32. Meyer NP, Seaver EC: Cell Lineage and Fate Map of the Primary Somatoblast of the Polychaete Annelid Capitella teleta. Integr Comp Biol 2010, 50:756-767. 10.1093/icb/icq120
33. Seaver EC, Kaneshige LM: Expression of 'segmentation' genes during larval and juvenile development in the polychaetes Capitella sp. I and H. elegans. Dev Biol 2006, 289:179-194. 10.1016/j.ydbio.2005.10.025
34. Fröbius AC, Seaver EC: ParaHox gene expression in the polychaete annelid Capitella sp. I. Dev Genes Evol 2006, 216:81-88. 10.1007/s00427-005-0049-0
35. Dill KK, Thamm K, Seaver EC: Characterization of twist and snail gene expression during mesoderm and nervous system development in the polychaete annelid Capitella sp. I. Dev Genes Evol 2007, 217:435-447. 10.1007/s00427-007-0153-4
36. Fröbius AC, Matus DQ, Seaver EC: Genomic organization and expression demonstrate spatial and temporal Hox gene colinearity in the lophotrochozoan Capitella sp. I. PloS One 2008, 3:e4004. 10.1371/journal.pone.0004004
37. Boyle MJ, Seaver EC: Developmental expression of foxA and gata genes during gut formation in the polychaete annelid, Capitella sp. I. Evol Dev 2008, 10:89-105. 10.1111/j.1525-142X.2007.00216.x
38. Dill KK, Seaver EC: Vasa and nanos are coexpressed in somatic and germ line tissue from early embryonic cleavage stages through adulthood in the polychaete Capitella sp. I. Dev Genes Evol 2008, 218:453-463. 10.1007/s00427-008-0236-x
39. Shimeld SM, Boyle MJ, Brunet T, Luke GN, Seaver EC: Clustered Fox genes in lophotrochozoans and the evolution of the bilaterian Fox gene cluster. Dev Biol 2010, 340:234-248. 10.1016/j.ydbio.2010.01.015
40. Giani VC Jr, Yamaguchi E, Boyle MJ, Seaver EC: Somatic and germline expression of piwi during development and regeneration in the marine polychaete annelid Capitella teleta. EvoDevo 2011, 2:10. 10.1186/2041-9139-2-10
41. Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D, Kuo A, Minovitsky S, Nikitin R, Ohm RA, Otillar R, Poliakov A, Ratnere I, Riley R, Smirnova T, Rokhsar D, Dubchak I: The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 2012, 40:D26-D32. 10.1093/nar/gkr947
42. Wilson EB: The cell-lineage of Nereis. J Morphol 1892, VI:361-478.
43. Boyer BC, Henry JJ, Martindale MQ: Dual Origins of Mesoderm in a Basal Spiralian: Cell Lineage Analyses in the Polyclad Turbellarian Hoploplana inquilina. Dev Biol 1996, 179:329-338. 10.1006/dbio.1996.0264
44. Oliveri P, Davidson EH: Gene regulatory network controlling embryonic specification in the sea urchin. Curr Opin Genet Dev 2004, 14:351-360. 10.1016/j.gde.2004.06.004
45. Venkatesh TV, Holland ND, Holland LZ, Su MT, Bodmer R: Sequence and developmental expression of amphioxus AmphiNk2-1: insights into the evolutionary origin of the vertebrate thyroid gland and forebrain. Dev Genes Evol 1999, 209:254-259. 10.1007/s004270050250
46. Ristoratore F, Spagnuolo A, Aniello F, Branno M, Fabbrini F, Di Lauro R: Expression and functional analysis of Cititf1 , an ascidian NK-2 class gene, suggest its role in endoderm development. Development 1999, 126:5149-5159.
47. Takacs CM, Moy VN, Peterson KJ: Testing putative hemichordate homologues of the chordate dorsal nervous system and endostyle: expression of NK2.1 (TTF-1 ) in the acorn worm Ptychodera flava (Hemichordata, Ptychoderidae). Evol Dev 2002, 4:405-417. 10.1046/j.1525-142X.2002.02029.x
48. Harfe BD, Fire A: Muscle and nerve-specific regulation of a novel NK-2 class homeodomain factor in Caenorhabditis elegans. Development 1998, 125:421-429.
49. Zaffran S, Das G, Frasch M: The NK-2 homeobox gene scarecrow (scro ) is expressed in pharynx, ventral nerve cord and brain of Drosophila embryos. Mech Dev 2000, 94:237-241. 10.1016/S0925-4773(00)00298-7
50. Dunn EF, Moy VN, Angerer LM, Angerer RC, Morris RL, Peterson KJ: Molecular paleoecology: using gene regulatory analysis to address the origins of complex life cycles in the late Precambrian. Evol Dev 2007, 9:10-24. 10.1111/j.1525-142X.2006.00134.x
51. Hejnol A, Martindale MQ: Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature 2008, 456:382-386. 10.1038/nature07309
52. Neidert AH, Panopoulou G, Langeland JA: Amphioxus goosecoid and the evolution of the head organizer and prechordal plate. Evol Dev 2000, 2:303-310. 10.1046/j.1525-142x.2000.00073.x
53. Goriely A, Stella M, Coffinier C, Kessler D, Mailhos C, Dessain S, Desplan C: A functional homologue of goosecoid in Drosophila. Development 1996, 122:1641-1650.
54. Angerer LM, Oleksyn DW, Levine AM, Xiaotao L, Klein WH, Angerer RC: Sea urchin goosecoid function links fate specification along the animal-vegetal and oral-aboral embryonic axes. Development 2001, 128:4393-4404.
55. Arendt D, Technau U, Wittbrodt J: Evolution of the bilaterian larval foregut. Nature 2001, 409:81-85. 10.1038/35051075
56. Lartillot N, Le Gouar M, Adoutte A: Expression patterns of fork head and goosecoid homologues in the mollusc Patella vulgata supports the ancestry of the anterior mesendoderm across Bilateria. Dev Genes Evol 2002, 212:551-561. 10.1007/s00427-002-0274-8
57. Martin-Duran JM, Janssen R, Wennberg S, Budd GE, Hejnol A: Deuterostomic development in the protostome Priapulus caudatus. Curr Biol 2012, 22:2161-2166. 10.1016/j.cub.2012.09.037
58. Tu Q, Brown CT, Davidson EH, Oliveri P: Sea urchin Forkhead gene family: phylogeny and embryonic expression. Dev Biol 2006, 300:49-62. 10.1016/j.ydbio.2006.09.031
59. Yu JK, Mazet F, Chen YT, Huang SW, Jung KC, Shimeld SM: The Fox genes of Branchiostoma floridae. Dev Genes Evol 2008, 218:629-638. 10.1007/s00427-008-0229-9
60. Fuchs J, Martindale MQ, Hejnol A: Gene expression in bryozoan larvae suggest a fundamental importance of pre-patterned blastemic cells in the bryozoan life-cycle. EvoDevo 2011, 2:13. 10.1186/2041-9139-2-13
61. Grassle JP, Grassle JF: Sibling species in the marine pollution indicator Capitella (polychaeta). Science 1976, 192:567-569. 10.1126/science.1257794
62. Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW: GenBank. Nucleic Acids Res 2013, 41:D36-D42. 10.1093/nar/gks1195
63. Abascal F, Zardoya R, Posada D: ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105. 10.1093/bioinformatics/bti263
64. Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755. 10.1093/bioinformatics/17.8.754
65. Stamatakis A: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690. 10.1093/bioinformatics/btl446
66. Boyle MJ, Seaver EC: Expression of FoxA and GATA transcription factors correlates with regionalized gut development in two lophotrochozoan marine worms: Chaetopterus (Annelida) and Themiste lageniformis (Sipuncula). EvoDevo 2010, 1:2. 10.1186/2041-9139-1-2
67. Lartillot N, Lespinet O, Vervoort M, Adoutte A: Expression pattern of Brachyury in the mollusc Patella vulgata suggests a conserved role in the establishment of the AP axis in Bilateria. Development 2002, 129:1411-1421.
68. Nederbragt AJ, te Welscher P, van den Driesche S, van Loon AE, Dictus WJ: Novel and conserved roles for orthodenticle / otx and orthopedia / otp orthologs in the gastropod mollusc Patella vulgata. Dev Genes Evol 2002, 212:330-337. 10.1007/s00427-002-0246-z
69. Arenas-Mena C: Embryonic expression of HeFoxA1 and HeFoxA2 in an indirectly developing polychaete. Dev Genes Evol 2006, 216:727-736. 10.1007/s00427-006-0099-y
70. Arenas-Mena C, Wong KS: HeOtx expression in an indirectly developing polychaete correlates with gastrulation by invagination. Dev Genes Evol 2007, 217:373-384. 10.1007/s00427-007-0150-7
71. Gillis WJ, Bowerman B, Schneider SQ: Ectoderm- and endomesoderm-specific GATA transcription factors in the marine annelid Platynereis dumerilli. Evol Dev 2007, 9:39-50. 10.1111/j.1525-142X.2006.00136.x
72. Arenas-Mena C: The transcription factors HeBlimp and HeT-brain of an indirectly developing polychaete suggest ancestral endodermal, gastrulation, and sensory cell-type specification roles. J Exp Zool B 2008, 310:567-576.
73. Christodoulou F, Raible F, Tomer R, Simakov O, Trachana K, Klaus S, Snyman H, Hannon GJ, Bork P, Arendt D: Ancient animal microRNAs and the evolution of tissue identity. Nature 2010, 463:1084-1088. 10.1038/nature08744
74. Martin-Duran JM, Romero R: Evolutionary implications of morphogenesis and molecular patterning of the blind gut in the planarian Schmidtea polychroa. Dev Biol 2011, 352:164-176. 10.1016/j.ydbio.2011.01.032
75. Arenas-Mena C: Brachyury , Tbx2/3 and sall expression during embryogenesis of the indirectly developing polychaete Hydroides elegans. Int J Dev Biol 2013, 57:73-83. 10.1387/ijdb.120056ca
76. Martindale MQ, Hejnol A: A developmental perspective: changes in the position of the blastopore during bilaterian evolution. Dev Cell 2009, 17:162-174. 10.1016/j.devcel.2009.07.024
77. Hejnol A: Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc R Soc Lond B Biol 2009, 276:4261-4270. 10.1098/rspb.2009.0896
78. Mazza ME, Pang K, Martindale MQ, Finnerty JR: Genomic organization, gene structure, and developmental expression of three clustered otx genes in the sea anemone Nematostella vectensis. J Exp Zool B 2007, 308:494-506.
79. Li X, Chuang C-K, Mao C-A, Angerer LM, Klein WH: Two Otx Proteins Generated from Multiple Transcripts of a Single Gene in Strongylocentrotus purpuratus. Dev Biol 1997, 187:253-266. 10.1006/dbio.1997.8610
80. Hinman VF, Nguyen AT, Davidson EH: Expression and function of a starfish Otx ortholog, Am Otx: a conserved role for Otx proteins in endoderm development that predates divergence of the eleutherozoa. Mech Dev 2003, 120:1165-1176. 10.1016/j.mod.2003.08.002
81. Williams NA, Holland PW: Gene and domain duplication in the chordate Otx gene family: insights from Amphioxus Otx. Mol Biol Evol 1998, 15:600-607. 10.1093/oxfordjournals.molbev.a025961
82. Fumasoni I, Meani N, Rambaldi D, Scafetta G, Alcalay M, Ciccarelli FD: Family expansion and gene rearrangements contributed to the functional specialization of PRDM genes in vertebrates. BMC Evol Biol 2007, 7:187. 10.1186/1471-2148-7-187
83. Ruvinsky I, Silver LM, Gibson-Brown JJ: Phylogenetic analysis of T-Box genes demonstrates the importance of amphioxus for understanding evolution of the vertebrate genome. Genetics 2000, 156:1249-1257.
84. Carlsson P, Mahlapuu M: Forkhead transcription factors: key players in development and metabolism. Dev Biol 2002, 250:1-23. 10.1006/dbio.2002.0780
85. Gillis WQ, Bowerman BA, Schneider SQ: The evolution of protostome GATA factors: molecular phylogenetics, synteny, and intron/exon structure reveal orthologous relationships. BMC Evol Biol 2008, 8:112. 10.1186/1471-2148-8-112
86. Grens A, Gee L, Fisher DA, Bode HR: CnNK-2 , an NK-2 homeobox gene, has a role in patterning the basal end of the axis in Hydra. Dev Biol 1996, 180:473-488. 10.1006/dbio.1996.0321
87. Ryan JF, Burton PM, Mazza ME, Kwong GK, Mullikin JC, Finnerty JR: The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes: evidence from the starlet sea anemone, Nematostella vectensis. Genome Biol 2006, 7:R64. 10.1186/gb-2006-7-7-r64
88. Larroux C, Fahey B, Degnan SM, Adamski M, Rokhsar DS, Degnan BM: The NK homeobox gene cluster predates the origin of Hox genes. Curr Biol 2007, 17:706-710.
89. Fahey B, Larroux C, Woodcroft BJ, Degnan BM: Does the high gene density in the sponge NK homeobox gene cluster reflect limited regulatory capacity? Biol Bull 2008, 214:205-217. 10.2307/25470664
90. Matus DQ, Pang K, Marlow H, Dunn CW, Thomsen GH, Martindale MQ: Molecular evidence for deep evolutionary roots of bilaterality in animal development. Proc Natl Acad Sci U S A 2006, 103:11195-11200. 10.1073/pnas.0601257103
91. Lambert JD, Chan XY, Spiecker B, Sweet HC: Characterizing the embryonic transcriptome of the snail Ilyanassa. Integr Comp Biol 2010, 50:768-777. 10.1093/icb/icq121
92. Ruffins SW, Ettensohn CA: A fate map of the vegetal plate of the sea urchin (Lytechinus variegatus ) mesenchyme blastula. Development 1996, 122:253-263.
93. Sulston JE, Schierenberg E, White JG, Thomson JN: The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 1983, 100:64-119. 10.1016/0012-1606(83)90201-4
94. Davidson EH, Cameron RA, Ransick A: Specification of cell fate in the sea urchin embryo: summary and some proposed mechanisms. Development 1998, 125:3269-3290.
95. Goldstein B: Induction of gut in Caenorhabditis elegans embryos. Nature 1992, 357:255-257. 10.1038/357255a0
96. De Robertis EM, Blum M, Niehrs C: Steinbeisser: goosecoid and the organizer. Development 1992, 116:167-171.
97. De Robertis EM: Goosecoid. In Gastrulation: From Cells to Embryo. 1st edition. Edited by: Stern CD. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2004:731.
98. Seaver EC, Yamaguchi E, Richards GS, Meyer NP: Expression of the pair-rule gene homologs runt , Pax3/7 , even-skipped-1 and even-skipped-2 during larval and juvenile development of the polychaete annelid Capitella teleta does not support a role in segmentation. EvoDevo 2012, 3:8. 10.1186/2041-9139-3-8
99. True JR, Carroll SB: Gene co-option in physiological and morphological evolution. Ann Rev Cell Dev Biol 2002, 18:53-80. 10.1146/annurev.cellbio.18.020402.140619
100. Sanetra M, Begemann G, Becker MB, Meyer A: Conservation and co-option in developmental programmes: the importance of homology relationships. Front Zool 2005, 2:15. 10.1186/1742-9994-2-15
101. Monteiro A, Podlaha O: Wings, horns, and butterfly eyespots: how do complex traits evolve? PLoS Biol 2009, 7:e37. 10.1371/journal.pbio.1000037
102. Oliveri P, Walton KD, Davidson EH, McClay DR: Repression of mesodermal fate by foxa , a key endoderm regulator of the sea urchin embryo. Development 2006, 133:4173-4181. 10.1242/dev.02577
103. Maduro MF: Endomesoderm specification in Caenorhabditis elegans and other nematodes. Bioessays 2006, 28:1010-1022. 10.1002/bies.20480
104. Maduro MF, Meneghini MD, Bowerman B, Broitman-Maduro G, Rothman JH: Restriction of mesendoderm to a single blastomere by the combined action of SKN-1 and a GSK-3beta homolog is mediated by MED-1 and -2 in C. elegans. Mol Cell 2001, 7:475-485. 10.1016/S1097-2765(01)00195-2
105. Horner MA, Quintin S, Domeier ME, Kimble J, Labouesse M, Mango SE: pha-4 , an HNF-3 homolog, specifies pharyngeal organ identity in Caenorhabditis elegans. Genes Dev 1998, 12:1947-1952. 10.1101/gad.12.13.1947
106. Kalb JM, Lau KK, Goszczynski B, Fukushige T, Moons D, Okkema PG, McGhee JD: pha-4 is Ce-fkh-1, a fork fork head/HNF-3α, β, γ homolog that functions in organogenesis of the C. elegans pharynx. Development 1998, 125:2171-2180.
107. Broitman-Maduro G, Lin KT, Hung WW, Maduro MF: Specification of the C. elegans MS blastomere by the T-box factor TBX-35. Development 2006, 133:3097-3106. 10.1242/dev.02475
108. Lambert JD: Mesoderm in spiralians: the organizer and the 4d cell. J Exp Zool B Mol Dev Evol 2007, 310:15-23.
109. Ackermann C, Dorresteijn A, Fischer A: Clonal domains in postlarval Platynereis dumerilii (Annelida: Polychaeta). J Morphol 2005, 266:258-280. 10.1002/jmor.10375
110. Koinuma S, Umesono Y, Watanabe K, Agata K: Planaria FoxA (HNF3 ) homologue is specifically expressed in the pharynx-forming cells. Gene 2000, 259:171-176. 10.1016/S0378-1119(00)00426-1
111. Cho SJ, Valles Y, Giani VC Jr, Seaver EC, Weisblat DA: Evolutionary dynamics of the wnt gene family: a lophotrochozoan perspective. Mol Biol Evol 2010, 27:1645-1658. 10.1093/molbev/msq052
112. Thamm K, Seaver EC: Notch signaling during larval and juvenile development in the polychaete annelid Capitella sp. I. Dev Biol 2008, 320:304-318. 10.1016/j.ydbio.2008.04.015