Expression of FoxA and GATA transcription factors correlates with regionalized gut development in two lophotrochozoan marine worms: Chaetopterus (Annelida) and Themiste lageniformis (Sipuncula)

EvoDevo

Volumn 1, Issue 1, 2010, Pages

  Boyle, Michael J ^a   Seaver, Elaine C ^a  

^a UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; ANNELIDA; BILATERIA; CHAETOPTERUS; LOPHOTROCHOZOA; METAZOA; POLYCHAETA; SIPUNCULA; SIPUNCULUS NUDUS; SPIRALIA; THEMISTE; THEMISTE LAGENIFORMIS;

EID: 78651289619     PISSN: None     EISSN: 20419139     Source Type: Journal    
DOI: 10.1186/2041-9139-1-2     Document Type: Article

References (83)

1. Roberts DJ. Molecular mechanisms of development of the gastrointestinal tract. Dev Dyn 2000, 219:109-120. 10.1002/1097-0177(2000)9999:9999<::AID-DVDY1047>3.3.CO;2-Y, 11002332.
2. Maderspacher F. Breakthroughs and blind ends. Curr Biol 2009, 19:272-274.
3. Stainier DY. A glimpse into the molecular entrails of endoderm formation. Genes Dev 2002, 16:893-907. 10.1101/gad.974902, 11959838.
4. Davidson EH, Erwin DH. Gene regulatory networks and the evolution of animal body plans. Science 2006, 311:796-800. 10.1126/science.1113832, 16469913.
5. Zaret KS. Developmental competence of the gut endoderm: genetic potentiation by GATA and HNF3/fork head proteins. Dev Biol 1999, 209:1-10. 10.1006/dbio.1999.9228, 10208738.
6. Kiefer JC. Molecular mechanisms of early gut organogenesis: a primer on development of the digestive tract. Dev Dyn 2003, 228:287-291. 10.1002/dvdy.10382, 14518001.
7. Stainier DY. No organ left behind: tales of gut development and evolution. Science 2005, 307:1902-1904. 10.1126/science.1108709, 15790841.
8. Erwin DH. The developmental origins of animal body plans. Neoproterozoic Geobiology and Paleobiology; Dordrecht 2006, Chapter XXI:300. Netherlands: Springer, Xiao S, Kaufman AJ.
9. Schmidt-Rhaesa A. The evolution of organ systems 2007, Oxford; New York: Oxford University Press.
10. 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.
11. Halanych KM, Bacheller JD, Aguinaldo AM, Liva SM, Hillis DM, Lake JA. Evidence from 18 S ribosomal DNA that the lophophorates are protostome animals. Science 1995, 267:1641-1643. 10.1126/science.7886451, 7886451.
12. Mead AD. The early development of marine annelids. J Morphol 1897, XIII:227-327.
13. Lillie FR. Observations and experiments concerning the elementary phenomena of embryonic development in Chaetopterus. J Exp Zool 1906, 3:153-268.
14. Enders HE. A study of the life-history and habits of Chaetopterus variopedatus, Renier et Claparede. J Morphol 1909, 20:479-531.
15. Henry JJ. The role of unequal cleavage and the polar lobe in the segregation of developmental potential during first cleavage in the embryo of Chaetopterus variopedatus. Roux's Arch Dev Biol 1986, 195.
16. Henry JJ, Martindale MQ. The organizing role of the D quadrant as revealed through the phenomenon of twinning in the polychaete Chaetopterus variopedatus. Roux's Arch Dev Biol 1987, 196:499-510.
17. Irvine SQ, Martindale MQ. Expression patterns of anterior Hox genes in the polychaete Chaetopterus: correlation with morphological boundaries. Dev Biol 2000, 217:333-351. 10.1006/dbio.1999.9541, 10625558.
18. Seaver EC, Paulson DA, Irvine SQ, Martindale MQ. The spatial and temporal expression of Ch-en, the engrailed gene in the polychaete Chaetopterus, does not support a role in body axis segmentation. Dev Biol 2001, 236:195-209. 10.1006/dbio.2001.0309, 11456454.
19. Rouse GW, Pleijel F. Polychaetes 2001, Oxford; New York: Oxford University Press.
20. Struck T, Schult N, Kusen T, Hickman E, Bleidorn C, McHugh D, Halanych KM. Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evol Biol 2007, 7:57. 10.1186/1471-2148-7-57, 1855331, 17411434.
21. Pilger JF. Reproductive biology and development of Themiste lageniformis, a parthenogenic sipunculan. Bull Mar Sci 1987, 41:59-67.
22. Pilger JF. A cytophotometric study of parthenogenesis in Themiste lageniformis (Sipuncula). Bull Mar Sci 1989, 45:415-424.
23. Williams JA. Functional development in four species of the sipuncula. Doctoral Dissertation 1977, University of Hawaii, Department of Zoology.
24. Pilger JF. Reproduction of a parthenogenetic sipunculan. Annual Meeting of the American Society of Zoologists. American Zoologist 1978, 663.
25. Huang DY, Chen JY, Vannier J, Saiz Salinas JI. Early Cambrian sipunculan worms from southwest China. Proc Biol Sci 2004, 271:1671-1676. 10.1098/rspb.2004.2774, 1691784, 15306286.
26. Sperling EA, Vinther J, Moy VN, Wheeler BM, Semon M, Briggs DE, Peterson KJ. MicroRNAs resolve an apparent conflict between annelid systematics and their fossil record. Proc Biol Sci 2009, 276:4315-22. 10.1098/rspb.2009.1340, 19755470.
27. Purschke G. On the ground pattern of Annelida. Org Divers Evol 2002, 2:181-196.
28. Bartolomaeus T. Structure and development of nephridia in Annelida and related taxa. Hydrobiologia 2005, 535/536:139-165.
29. Tzetlin A, Purschke G. Fine structure of the pharyngeal apparatus of the pelagosphera larva in phascolosoma agassizii (Sipuncula) and its phyolgenetic significance. Zoomorphology 2006, 125:109-117.
30. Kristof A, Wollesen T, Wanninger A. Segmental mode of neural patterning in sipuncula. Curr Biol 2008, 18:1129-1132. 10.1016/j.cub.2008.06.066, 18656359.
31. Boore JL, Staton JL. The mitochondrial genome of the Sipunculid Phascolopsis gouldii supports its association with Annelida rather than Mollusca. Mol Biol Evol 2002, 19:127-137.
32. Mwinyi A, Meyer A, Bleidorn C, Lieb B, Bartolomaeus T, Podsiadlowski L. Mitochondrial genome sequence and gene order of Sipunculus nudus give additional support for an inclusion of Sipuncula into Annelida. BMC Genomics 2009, 10:27. 10.1186/1471-2164-10-27, 2639372, 19149868.
33. Colgan DJ, Hutchings PA, Beacham E. Multi-gene analyses of the phylogenetic relationships among the Mollusca, Annelida, and Arthropoda. Zool Stud 2008, 47:338-351.
34. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV, Haddock SH, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008, 452:745-749. 10.1038/nature06614, 18322464.
35. Zrzavý J, Riha P, Pialek L, Janouskovec J. Phylogeny of Annelida (Lophotrochozoa): total-evidence analysis of morphology and six genes. BMC Evol Biol 2009, 9:189. 10.1186/1471-2148-9-189, 2732625, 19660115.
36. Schulze A, Cutler EB, Giribet G. Phylogeny of sipunculan worms: A combined analysis of four gene regions and morphology. Mol Phylogenet Evol 2007, 42:171-192. 10.1016/j.ympev.2006.06.012, 16919974.
37. Cazaux C. Developpement larvaire de Chaetopterus variopedatus (Renier). Actes Soc Linneénne de Bordeaux 1965, 102:1-16.
38. Bonch-Bruevich EV, Malakhov VV. Organization of early larvae of the polychaete worm Chaetopterus variopedatus (Spiomorpha, Chaetopteridae). Dokl Akad Nauk SSSR 1987, 292:107-109.
39. Malakhov VV. Embryogenesis of Chaetopterus variopedatus (Spiomorpha, Chaetopteridae). Zool Zh 1984, 63:656-661.
40. Irvine SQ, Chaga O, Martindale MQ. Larval ontogenetic stages of Chaetopterus: developmental heterochrony in the evolution of Chaetopterid polychaetes. Biol Bull 1999, 197:319-331. 10.2307/1542786, 10630333.
41. Williams JA. Development of a rock burrowing sipunculid inhabiting stony coral. Winter Meeting of the American Society of Zoologists. Am Zool 1972, 723.
42. Kaufmann E, Knochel W. Five years on the wings of fork head. Mech Dev 1996, 57:3-20. 10.1016/0925-4773(96)00539-4, 8817449.
43. Carlsson P, Mahlapuu M. Forkhead transcription factors: key players in development and metabolism. Dev Biol 2002, 250:1-23. 10.1006/dbio.2002.0780, 12297093.
44. Lowry JA, Atchley WR. Molecular evolution of the GATA family of transcription factors: conservation within the DNA-binding domain. J Mol Evol 2000, 50:103-115.
45. 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, 2383905, 18412965.
46. 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, 12027435.
47. Nakagoshi H. Functional specification in the Drosophila endoderm. Dev Growth Differ 2005, 47:383-392. 10.1111/j.1440-169X.2005.00811.x, 16109036.
48. 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.
49. Hinman VF, Nguyen AT, Cameron RA, 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.
50. 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, 15261650.
51. D'Souza A, Lee M, Taverner N, Mason J, Carruthers S, Smith JC, Amaya E, Papalopulu N, Zorn AM. Molecular components of the endoderm specification pathway in Xenopus tropicalis. Dev Dyn 2003, 226:118-127. 10.1002/dvdy.10201, 12508233.
52. 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, 17031669.
53. Gillis WJ, Bowerman B, Schneider SQ. Ectoderm- and endomesoderm-specific GATA transcription factors in the marine annelid Platynereis dumerilii. Evol Dev 2007, 9:39-50.
54. Gaudet J, Mango SE. Regulation of organogenesis by the Caenorhabditis elegans FoxA protein PHA-4. Science 2002, 295:821-825. 10.1126/science.1065175, 11823633.
55. 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, 17038513.
56. Rice ME. Sipuncula. Reproduction of Marine Invertebrates: Entoprocts and Lesser Coelomates 1975, II:67-127. New York: Academic Press, Giese AC, Pearse JS.
57. Cutler EB. The Sipuncula: their systematics, biology, and evolution 1994, Ithaca: Comstock Pub. Associates.
58. Michel C. Intestine and digestive glands. The Ultrastructure of Polychaeta 1988, 4:494. Stuttgart: Gustav Fischer Verlag, Westheide W, Hermans CO, [Ax P (Series Editor) Microfauna Marina].
59. Rice ME. Sipuncula. Microscopic Anatomy of Invertebrates. Onychophora, Chilopoda, and Lesser Protostomata 1993, 12:274-296. New York: Wiley-Liss, Harrison FW, Rice ME.
60. Schulze A, Cutler EB, Giribet G. Reconstructing the phylogeny of the Sipuncula. Hydrobiologia 2005, 535/536:277-296.
61. Costello DP, Henley C. Methods for Obtaining and Handling Marine Eggs and Embryos. 1971, City: Marine Biological Library; Wood Hole Oceanographic Institute., https://darchive.mblwhoilibrary.org/handle/1912/295
62. Hoch M, Pankratz MJ. Control of gut development by fork head and cell signaling molecules in Drosophila. Mech Dev 1996, 58:3-14. 10.1016/S0925-4773(96)00541-2, 8887312.
63. Wu LH, Lengyel JA. Role of caudal in hindgut specification and gastrulation suggests homology between Drosophila amnioproctodeal invagination and vertebrate blastopore. Development 1998, 125:2433-2442.
64. Takashima S, Murakami R. Regulation of pattern formation in the Drosophila hindgut by wg, hh, dpp, and en. Mech Dev 2001, 101:79-90. 10.1016/S0925-4773(00)00555-4, 11231061.
65. Lengyel JA, Iwaki DD. It takes guts: the Drosophila hindgut as a model system for organogenesis. Dev Biol 2002, 243:1-19. 10.1006/dbio.2002.0577, 11846473.
66. 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, 16416136.
67. 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, 16330020.
68. Conklin EG. The embryology of Crepidula. J Morphol 1897, 13:1-226.
69. Costello DP, Henley C. Spiralian development: a perspective. Am Zool 1976, 16:277-291.
70. Henry JQ, Martindale MQ. Conservation and innovation in spiralian development. Hydrobiologia 1999, 402:255-265.
71. Kalb JM, Lau KK, Goszczynski B, Fukushige T, Moons D, Okkema PG, McGhee JD. pha-4 is Ce-fkh-1, a fork head/HNF-3alpha, beta, gamma homolog that functions in organogenesis of the C. elegans pharynx. Development 1998, 125:2171-2180.
72. Weigel D, Jurgens G, Kuttner F, Seifert E, Jackle H. The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 1989, 57:645-658. 10.1016/0092-8674(89)90133-5, 2566386.
73. 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, 16316403.
74. Ang SL, Rossant J. HNF-3 beta is essential for node and notochord formation in mouse development. Cell 1994, 78:561-574. 10.1016/0092-8674(94)90522-3, 8069909.
75. Soudais C, Bielinska M, Heikinheimo M, MacArthur CA, Narita N, Saffitz JE, Simon MC, Leiden JM, Wilson DB. Targeted mutagenesis of the transcription factor GATA-4 gene in mouse embryonic stem cells disrupts visceral endoderm differentiation in vitro. Development 1995, 121:3877-3888.
76. Taguchi S, Tagawa K, Humphreys T, Nishino A, Satoh N, Harada Y. Characterization of a hemichordate fork head/HNF-3 gene expression. Dev Genes Evol 2000, 210:11-17. 10.1007/PL00008181, 10603081.
77. 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, 12459924.
78. 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.
79. Martindale MQ, Pang K, Finnerty JR. Investigating the origins of triploblasty: 'mesodermal' gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 2004, 131:2463-2474. 10.1242/dev.01119, 15128674.
80. Shubin N, Tabin C, Carroll S. Deep homology and the origins of evolutionary novelty. Nature 2009, 457:818-823. 10.1038/nature07891, 19212399.
81. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755. 10.1093/bioinformatics/17.8.754, 11524383.
82. NCBI GenBank. , http://www.ncbi.nlm.nih.gov/
83. DOE Joint Genome Institute. , http://www.jgi.doe.gov/