Cleavage pattern and fate map of the mesentoblast, 4d, in the gastropod Crepidula: a hallmark of spiralian development

EvoDevo

Volumn 3, Issue 1, 2012, Pages

  Lyons, Deirdre C ^a   Perry, Kimberly J ^b   Lesoway, Maryna P ^c,d   Henry, Jonathan Q ^b  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; ANNELIDA; BILATERIA; CLITELLATA; CREPIDULA; CREPIDULA CONVEXA; CREPIDULA FORNICATA; DIPLOMONADIDA GROUP; GASTROPODA; GLOSSIPHONIIDAE; HIRUDINIDA; LOPHOTROCHOZOA; MOLLUSCA; PROTOSTOMIA; SPIRALIA; TUBIFEX; TUBIFICIDAE;

EID: 84870492475     PISSN: None     EISSN: 20419139     Source Type: Journal    
DOI: 10.1186/2041-9139-3-21     Document Type: Article

References (115)

1. Hinman VF, Yankura KA, McCauley BS. Evolution of gene regulatory network architectures: examples of subcircuit conservation and plasticity between classes of echinoderms. Biochim Biophys Acta 2009, 1789:326-332.
2. Maduro MF. Structure and evolution of the C. elegans embryonic endomesoderm network. Biochim Biophys Acta 2009, 1789:250-260.
3. Martindale MQ, Hejnol A. A developmental perspective: changes in the position of the blastopore during bilaterian evolution. Dev Cell 2009, 17:162-174.
4. Hejnol A. A twist in time - the evolution of spiral cleavage in the light of animal phylogeny. Integr Comp Biol 2010, 50:695-706.
5. Wilson EB. Considerations on cell-lineage and ancestral reminiscence. Ann N Y Acad Sci 1898, 11:1-27.
6. Verdonk NH, van den Biggelaar JAM. Early development and the formation of the germ layers. The Mollusca 1983, 91-122. Academic, San Diego, CA, 3.
7. Freeman G, Lundelius JW. Evolutionary implications of the mode of D quadrant specification in coelomates with spiral cleavage. J Evol Biol 1992, 5:205-247.
8. Henry J, Martindale M. Conservation and innovation in spiralian development. Hydrobiologia 1999, 402:255-265.
9. Dohle W. The ancestral cleavage pattern of the clitellates and its phylogenetic deviations. Hydrobiologia 1999, 402:267-283.
10. Lambert JD. Mesoderm in spiralians: the organizer and the 4d cell. J Exp Zool (Mol Dev Evol) 2008, 308B:15-23.
11. Lambert JD. Developmental patterns in spiralian embryos. Curr Biol 2010, 20:R72-R77.
12. Boyer BC, Henry JJ, Martindale MQ. The cell lineage of a polyclad turbellarian embryo reveals close similarity to coelomate spiralians. Dev Biol 1998, 204:111-123.
13. 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.
14. Lambert JD, Nagy LM. The MAPK cascade in equally cleaving spiralian embryos. Dev Biol 2003, 263:231-241.
15. Henry JQ, Perry KJ, Martindale MQ. Cell specification and the role of the polar lobe in the gastropod mollusc Crepidula fornicata. Dev Biol 2006, 297:295-307.
16. Weisblat DA, Kim SY, Stent GS. Embryonic origins of cells in the leech Helobdella triserialis. Dev Biol 1984, 104:65-85.
17. Weisblat DA, Huang FZ. An overview of glossiphoniid leech development. Can J Zool 2001, 79:218-232.
18. Gline SE, Nakamoto A, Cho SJ, Chi C, Weisblat DA. Lineage analysis of micromere 4d, a super-phylotypic cell for Lophotrochozoa, in the leech Helobdella and the sludgeworm Tubifex. Dev Biol 2011, 353:120-133.
19. Goto A, Kitamura K, Shimizu T. Cell lineage analysis of pattern formation in theTubifexembryo I. Segmentation in the mesoderm. Int J Dev Biol 1999, 43:317-327.
20. Goulding MB. Comparative and experimental analysis of precocious cell-lineage diversification in the embryonic dorsoventral axis of the gastropod Ilyanassa 2001, University of Texas, Austin, PhD thesis.
21. Rabinowitz JS, Chan XY, Kingsley EP, Duan Y, Lambert JD. Nanos is required in somatic blast cell lineages in the posterior of a mollusc embryo. Curr Biol 2008, 18:331-336.
22. Henry JJ, Collin R, Perry KJ. The slipper snail, Crepidula: an emerging lophotrochozoan model system. Biol Bull 2010, 218:211-229.
23. Conklin EG. The embryology of Crepidula, a contribution to the cell lineage and early development of some marine gastropods. J Morphol 1897, 13:1-226.
24. Hejnol A, Martindale MQ, Henry JQ. High-resolution fate map of the snail Crepidula fornicata: the origins of ciliary bands, nervous system, and muscular elements. Dev Biol 2007, 305:63-76.
25. Henry JQ, Perry KJ, Martindale MQ. beta-catenin and early development in the gastropod, Crepidula fornicata. Integr Comp Biol 2010, 50:707-719.
26. Henry Lab Home Page Crepidula Methods http://www.life.illinois.edu/henry/crepidula_methods.html, Henry Lab Home Page.
27. Henry JJ, Martindale MQ. Conservation of the spiralian developmental program: cell lineage of the nemertean, Cerebratulus lacteus. Dev Biol 1998, 201:253-269.
28. Henry JQ, Martindale MQ, Boyer BC. Axial specification in a basal member of the spiralian clade: lineage relationships of the first four cells to the larval body plan in the polyclad turbellarian Hoploplana inquilina. Biol Bull 1995, 189:194-195.
29. Martindale MQ, Henry JQ. Diagonal development: establishment of the anal axis in the ctenophore Mnemiopsis leidyi. Biol Bull 1995, 189:190-192.
30. Tadir Y, Douglas-Hamilton DH. Laser effects in the manipulation of human eggs and embryos for in vitro fertilization. Methods Cell Biol 2007, 82:409-431.
31. Douglas-Hamilton DH. Laser Heating of Embryos and Cells in the ZILOS/ZYclone system 2008, Hamilton Thorne Biosciences, Bererly, MA.
32. Henry JJ. The role of unequal cleavage and the polar lobe in the segregation of developmental potential during first cleavage in the embryo of Chætopterus variopedatus. Roux's Arch Dev Biol 1986, 195:103-116.
33. Crampton HE. Experimental studies on gastropod development. Wilhelm Roux Arch Entwickl Mech Org 1896, 3:1-19.
34. Novikoff AB. Embryonic determination in the annelid, Sabellaria vulgaris. II. Transplantation of polar lobes and blastomeres as a test of their inducing capacities. Biol Bull 1938, 74:211-234.
35. Clement AC. Experimental studies on germinal localization in Ilyanassa. I. the role of the polar lobe in determination of the cleavage pattern and its influence in later development. J Exp Zool 1952, 121:593-626.
36. Rattenbury JC, Berg WE. Embryonic segregation during early development of Mytilus edulis. J Morphol 1954, 95:393-414.
37. Atkinson JW. Organogenesis in normal and lobeless embryos of the marine prosobranch gastropod Ilyanassa obsoleta. J Morphol 1971, 133:339-352.
38. Cather JN, Verdonk NH. The development of Bithynia tentaculata (Prosobranchia, Gastropoda) after removal of the polar lobe. J Embryol Exp Morphol 1974, 31:415-422.
39. van Dongen CAM, Geilenkirchen WLM. The development of Dentalium with special reference to the significance to the significance of the polar lobe. 3. Division chronology and development of cell pattern in Dentalium dentale (Scaphopoda). Proc Koninklijke Nederlandse Akademie van Wetenschappen Series C Biol Med Sci 1974, 77:85-100.
40. van Dongen CAM, Geilenkirchen WLM. The development of Dentalium with special reference to the significance to the significance of the polar lobe. 1. Division chronology and development of cell pattern in Dentalium dentale (Scaphopoda). Proc Koninklijke Nederlandse Akademie van Wetenschappen Series C Biol Med Sci 1974, 77:57-70.
41. van Dongen CAM, Geilenkirchen WLM. The development of Dentalium with special reference to the significance to the significance of the polar lobe. 2. Division chronology and development of cell pattern in Dentalium dentale (Scaphopoda). Proc Koninklijke Nederlandse Akademie van Wetenschappen Series C Biol Med Sci 1974, 77:71-84.
42. van Dongen CAM, Geilenkirchen WLM. The development of Dentalium with special reference to the significance to the significance of the polar lobe. 4. Division chronology and development of cell pattern in Dentalium dentale after removal of polar lobe at 1st cleavage. Proc Koninklijke Nederlandse Akademie van Wetenschappen Series C Biol Med Sci 1975, 78:358-375.
43. van Dongen CAM. The development of Dentalium with special reference to the significance to the significance of the polar lobe. 7. Organogenesis and hostogenesis in lobeless embryos of Dentalium vulgare (Da Costa) as compared to normal development. Proc Koninklijke Nederlandse Akademie van Wetenschappen Series C Biol Med Sci 1976, 79:454-465.
44. van Dongen CAM. The development of Dentalium with special reference to the significance to the significance of the polar lobe. 6. Differentiation of cell pattern in lobeless embryos of Dentalium vulgare (Da Costa) during late larval development. Proc Koninklijke Nederlandse Akademie van Wetenschappen Series C Biol Med Sci 1976, 79:256-266.
45. van Dongen CAM. The development of Dentalium with special reference to the significance to the significance of the polar lobe. 5. Differentiation of cell pattern in lobeless embryos of Dentalium vulgare (Da Costa) during late larval development. Proc Koninklijke Nederlandse Akademie van Wetenschappen Series C Biol Med Sci 1976, 79:245-255.
46. Cather JN, Verdonk NH, Dohmen MR. Role of the vegetal body in the regulation of development in Bithynia tentaculata (Prosobranchia, Gastropoda). Am Zool 1976, 16:455-468.
47. Render JA. The second polar lobe of Sabellaria cementarium plays an inhibitory role in apical tuft formation. Roux's Arch Dev Biol 1983, 192:120-129.
48. Wilson EB. Experimental studies on germinal localization. I. The germ-regions in the egg of Dentalium. J Exp Zool 1904, 1:1-72.
49. Wilson EB. Experimental studies in germinal localization. II. Experiments on the cleavage-mosaic in Patella and Dentalium. J Exp Zool 1904, 1(Wilson EB):197-268.
50. Hatt P. Essais expérimentaux sur les localizations germinales dans l'oeuf d'un annelide (Sabellaria alveolata L.). Arch D'anat Micros 1932, 28:81-98.
51. Swartz SZ, Chan XY, Lambert JD. Localization of Vasa mRNA during early cleavage of the snail Ilyanassa. Dev Genes Evol 2008, 218:107-113.
52. Woods FH. History of the germ cells in Sphaerium striatinum (Lam.). J Morphol 1931, 51:545.
53. Woods FH. Keimbahn determinants and continuity of the germ cells in Sphaerium striatinum (Lam.). J Morphol 1932, 53:345-365.
54. Ruthensteiner B, Schaefer K. On the protonephridia and 'larval kidneys' of Nassarius (Hinia) reticulatus (Linnaeus) (Caenogastropoda). J Molluscan Stud 1991, 57:323-329.
55. Rivest BR. Studies on the structure and function of the larval kidney complex of prosobranch gastropods. Biol Bull 1992, 182:305-323.
56. Collin R. Worldwide patterns in mode of development in calyptraeid gastropods. Mar Ecol Prog Ser 2003, 247:103-122.
57. Pechenik J. The relationship between temperature, growth rate, and duration of planktonic life for larvae of the gastropod Crepidula fornicata (L.). J ExpMar Biol Ecol 1984, 74:241-257.
58. Wilson EB. A cell-lineage of Nereis. A contribution to the cytogeny of the annelid body. J Morphol 1892, 6:361-481.
59. Render JA. Cell fate maps in the Ilyanassa obsoleta embryo beyond the third division. Dev Biol 1997, 189:301-310.
60. Hendler G, Franz DR. Population dynamics and life history of Crepidula convexa Say (Gastropoda: Prosobranchia) in Delaware Bay. Biol Bull 1971, 141:514-526.
61. Hoagland KE. Patterns of encapsulation and brooding in the calyptraeidae (Prosobranchia: Mesogastropoda). Am Malacol Bull 1986, 4:173-183.
62. Whitman CO. The embryology of Clepsine. Q J Microsc Sci 1878, 18:213-315.
63. Wilson EB. Cell-lineage and ancestral reminiscence. Biological Lectures from the Marine Biological Laboratory, Woods Hole, Massachusetts 1898, 21-42. Ginn & Co, Boston.
64. Tannreuther GW. The embryology of Bdellodrilus philadelphicus. J Morphol 1915, 26:143-216.
65. 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.
66. Giani VC, 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.
67. Desjeux I, Price DJ. The production and elimination of supernumerary blast cells in the leech embryo. Dev Genes Evol 1999, 209:284-293.
68. Liu N-JL, Isaksen DE, Smith CM, Weisblat DA. Movements and stepwise fusion of endodermal precursor cells in leech. Dev Genes Evol 1998, 208:117-127.
69. Nardelli-Haefliger D, Shankland M. Lox10, a member of the NK-2 homeobox gene class, is expressed in a segmental pattern in the endoderm and in the cephalic nervous system of the leech Helobdella. Development 1993, 118:877-892.
70. Gline SE, Kuo DH, Stolfi A, Weisblat DA. High resolution cell lineage tracing reveals developmental variability in leech. Dev Dyn 2009, 238:3139-3151.
71. Weisblat DA, Shankland M. Cell lineage and segmentation in the leech. Philos Trans R Soc Lond B Biol Sci 1985, 312:39-56.
72. Rebscher N, Zelada-González F, Banisch TU, Raible F, Arendt D. Vasa unveils a common origin of germ cells and of somatic stem cells from the posterior growth zone in the polychaete Platynereis dumerilii. Dev Biol 2007, 306:599-611.
73. Rebscher N, Lidke AK, Ackermann CF. Hidden in the crowd: primordial germ cells and somatic stem cells in the mesodermal posterior growth zone of the polychaete Platynereis dumerillii are two distinct cell populations. EvoDevo 2012, 3:9.
74. Ackermann C, Dorresteijn A, Fischer A. Clonal domains in postlarval Platynereis dumerilii (Annelida: Polychaeta). J Morphol 2005, 266:258-280.
75. Kitamura K, Shimizu T. Analyses of segment-specific expression of alkaline phosphatase activity in the mesoderm of the oligochaete annelid Tubifex: implications for specification of segmental identity. Dev Biol 2000, 219:214-223.
76. Clement AC. The embryonic value of the micromeres in Ilyanassa obsoleta, as determined by deletion experiments. III. The third quartet cells and the mesentoblast cell, 4d. Int J Invertebr Reprod Dev 1986, 9:155-168.
77. Okada K, . Sci Rep Tohoku Imp Univ Ser The development of the primary mesoderm in Sphaerium japonicum biwaense Mori. Sci Rep Tohoku Imp Univ Ser 4 1939, 14:25-47. Sci Rep Tohoku Imp Univ Ser.
78. Zeigler HE. Die Entwicklung von Cyclas cornea Lam 1885, 41. Zeit f wiss Zool, Bd.
79. Boyer BC, Henry JQ, 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.
80. Goulding MQ. Cell lineage of the Ilyanassa embryo: evolutionary acceleration of regional differentiation during early development. PLoS One 2009, 4:e5506.
81. Shimizu T, Nakamoto A. Segmentation in annelids: cellular and molecular basis for metameric body plan. Zoolog Sci 2001, 18:285-298.
82. Weisblat DA. Leeches. Curr Biol 2003, 13:R752.
83. Brusca RC, Brusca GJ. Invertebrates 1990, Sinauer, Sunderland, MA.
84. Tzetlin A. G P: Pharynx and intestine. Hydrobioilogia 2005, 535/536:199-225.
85. Michel C. The ultrastructure of Polychaeta. Microfauna Marina 1988, 5-175. Gustav Fischer Verlag, Stuttgart, Westheide W, Hermans CO, 4.
86. Verdonk NH, Cather JN. Morphogenetic determination and differentiation. The Mollusca 1983, 215-252. Academic, San Diego, CA, 3.
87. Demian ES, Yousif F. Embryonic development and organogenesis in the snail Marisa cornuarietis. III. Development of the circulatory and renal systems. Malacologia 1973, 12:175-194.
88. Okada K. Some notes on Sphaerium japonicum biwaense Mori, a freshwater bivalve. IV. Gastrula and fetal larva. Sci Rep Tohoku Imp Univ Ser 4 1936, 11:49-68.
89. Clement AC. The embryonic value of the micromeres in Ilyanassa obsoleta, as determined by deletion experiments. II. The second quartet cells. Int J Invertebr Reprod Dev 1986, 9:139-153.
90. Clement AC. Development of the Ilyanassa embryo after the removal of the mesentoblast cell. Biol Bull 1960, 119:310.
91. Lambert JD, Nagy LM. MAPK signaling by the D quadrant embryonic organizer of the mollusc Ilyanassa obsoleta. Development 2001, 128:45-56.
92. Henry JJ, Perry KJ. MAPK activation and the specification of the D quadrant in the gastropod mollusc, Crepidula fornicata. Dev Biol 2008, 313:181-195.
93. Kang D, Pilon M, Weisblat DA. Maternal and zygotic expression of a nanos-class gene in the leech Helobdella robusta: primordial germ cells arise from segmental mesoderm. Dev Biol 2002, 245:28-41.
94. Fabioux C, Huvet A, Lelong C, Robert R, Pouvreau S, Daniel JY, Minguant C, Le Pennec M. Oyster vasa-like gene as a marker of the germline cell development in Crassostrea gigas. Biochem Biophys Res Commun 2004, 320:592-598.
95. Oyama A, Shimizu T. Transient occurrence of vasa-expressing cells in nongenital segments during embryonic development in the oligochaete annelid Tubifex tubifex. Dev Genes Evol 2007, 217:675-690.
96. Kranz AM, Tollenaere A, Norris BJ, Degnan BM, Degnan SM. Identifying the germline in an equally cleaving mollusc: Vasa and Nanos expression during embryonic and larval development of the vetigastropod Haliotis asinina. J Exp Zool B Mol Dev Evol 2010, 314:267-279.
97. Griffond B. Individualization and organogenesis of embryonic gonad in gonochoric prosobranch mollusc Viviparus viviparus (L.). Roux Arch Dev Biol 1977, 183:131-147.
98. Richardson BE, Lehmann R. Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat Rev Mol Cell Biol 2010, 11:37-49.
99. Ikenishi K. Germ plasm in Caenorhabditis elegans, Drosophila and Xenopus. Dev Growth Differ 1998, 40:1-10.
100. Dohmen MR, Lok D. The ultrastructure of the polar lobe of Crepidula fornicata (Gastropoda, Prosobranchia). J Embryol Exp Morphol 1975, 34:419-428.
101. Dohmen MR, Verdonk NH. The ultrastructure and role of the polar lobe in development of molluscs. Determinants of Spatial Organization 1979, 3. Academic, New York, Subtelny S, Konigsberg IR.
102. Dohmen MR, Verdonk NH. Cytoplasmic localizations in mosaic eggs. Maternal Effects of Development 1979, 127-145. Cambridge University Press, Cambridge, Newth DR, Balls M.
103. Raven CP. Morphogenesis: the Analysis of Molluscan Development 1966, Pergamon, Oxford, 2.
104. Henry JJ, Perry KJ, Fukui L, Alvi N. Differential localization of mRNAs during early development in the mollusc, Crepidula fornicata. Integr Comp Biol 2010, 50:720-733.
105. Logan CY, Miller JR, Ferkowicz MJ, McClay DR. Nuclear β-catenin is required to specify vegetal cell fates in the sea urchin embryo. Development 1999, 126:345-357.
106. Yajima M, Wessel GM. Small micromeres contribute to the germline in the sea urchin. Development 2011, 138:237-243.
107. Martindale MQ, Shankland M. Intrinsic segmental identity of segmental founder cells of the leech embryo. Nature 1990, 347:672-674.
108. Gleizer L, Stent GS. Developmental origin of segmental identity in the leech mesoderm. Development 1993, 117:177-189.
109. Cather JN. Cellular interactions in the development of the shell gland of the gastropod, Ilyanassa. J Exp Zool 1967, 166:205-223.
110. Surface FM. The early development of a polyclad, Planocera inquilina Wh. Proc Acad Nat Sci Phila 1907, 59:514-559.
111. van den Biggelaar JAM. Cleavage pattern and mesentoblast formation in Acanthochiton crinitus (Polyplacophora, Mollusca). Dev Biol 1996, 174:423-430.
112. Fukuda K, Kikuchi Y. Endoderm development in vertebrates: fate mapping, induction and regional specification. Dev Growth Differ 2005, 47:343-355.
113. Kingsley EP, Chan XY, Duan Y, Lambert JD. Widespread RNA segregation in a spiralian embryo. Evol Dev 2007, 9:527-539.
114. Lambert JD, Nagy LM. Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages. Nature 2002, 420:682-686.
115. 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.