BMP gradients: A paradigm for morphogen-mediated developmental patterning

Science

Volumn 348, Issue 6242, 2015, Pages

  Bier, Ethan ^a   De Robertis, Edward M ^b,c  

^a SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; MORPHOGEN;

CELL ORGANELLE; DEVELOPMENTAL BIOLOGY; EMBRYO; INVERTEBRATE; MORPHOGENESIS; NERVOUS SYSTEM; PARADIGM SHIFT; PHYSIOLOGICAL RESPONSE; PROTEIN; VERTEBRATE;

CELL FATE; CENTRAL NERVOUS SYSTEM; EMBRYO DEVELOPMENT; EXOSOME; EXTRACELLULAR SPACE; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; REACTION ANALYSIS; REVIEW; VERTEBRATE; ANIMAL; DROSOPHILA MELANOGASTER; ECTODERM; EMBRYOLOGY; EPIDERMIS; FEEDBACK SYSTEM; METABOLISM; MORPHOGENESIS; NEURAL TUBE; XENOPUS;

INVERTEBRATA; VERTEBRATA;

ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; DROSOPHILA MELANOGASTER; ECTODERM; EPIDERMIS; FEEDBACK, PHYSIOLOGICAL; NEURAL TUBE; XENOPUS;

EID: 84933544655     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aaa5838     Document Type: Review

References (119)

1. V. Hamburger, The Heritage of Experimental Embryology: Hans Spemann and the Organizer (Oxford Univ. Press, Oxford, 1988).
2. H. M. Spemann, H. Mangold, Uber induction von embryonanlagen durch implantation artfremder organis atoren. W. Roux' Arch. Ent. Org. 100, 599-638 (1924)
3. [translated and reprinted in Int. J. Dev. Biol. 45, 15(2001)].
4. E. M. De Robertis, Evo-devo: Variations on ancestral themes. Cell 132, 185-195 (2008). doi: 10.1016/j.cell.2008.01.003; pmid: 18243095
5. C. M. Mizutani, E. Bier, EvoD/Vo: The origins of BMP signalling in the neuroectoderm. Nat. Rev. Genet. 9, 663-677 (2008). doi: 10.1038/nrg2417; pmid:18679435
6. A. Turing, The chemical basis of morphogenesis. Philos. Trans. R. Soc. London Ser. B 237, 37-72 (1952). doi: 10.1098/rstb.1952.0012
7. F. Crick, Diffusion in embryogenesis. Nature 225, 420-422 (1970). doi: 10.1038/225420a0; pmid: 5411117
8. A. Gierer, H. Meinhardt, A theory of biological pattern formation. Kybernetik 12, 30-39 (1972). doi: 10.1007/BF00289234; pmid: 4663624
9. L. Wolpert, Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25, 1-47 (1969). doi: 10.1016/S0022-5193(69)80016-0; pmid: 4390734
10. P. W. Holland, Evolution of homeobox genes. WIREs Dev. Biol. 2, 31-45 (2013). doi: 10.1002/wdev.78
11. S. J. Gould, The Structure of Evolutionary Theory (Harvard Univ. Press, Cambridge, MA, 2002).
12. A. Stathopoulos, M. Levine, Dorsal gradient networks in the Drosophila embryo. Dev. Biol. 246, 57-67 (2002). doi: 10.1006/dbio.2002.0652; pmid: 12027434
13. S. Ross, C. S. Hill, How the Smads regulate transcription. Int. J. Biochem. Cell Biol. 40, 383-408 (2008). doi: 10.1016/j.biocel.2007.09.006; pmid: 18061509
14. A. Weiss et al., A conserved activation element in BMP signaling during Drosophila development. Nat. Struct. Mol. Biol. 17, 69-76 (2010). doi: 10.1038/nsmb.1715; pmid: 20010841
15. F. Hamaratoglu, M. Affolter, G. Pyrowolakis, Dpp/BMP signaling in flies: From molecules to biology. Semin. Cell Dev. Biol. 32, 128-136 (2014). doi: 10.1016/j.semcdb.2014.04.036; pmid: 24813173
16. H. Araujo, M. R. Fontenele, R. N. da Fonseca, Position matters: Variability in the spatial pattern of BMP modulators generates functional diversity. Genesis 49, 698-718 (2011). doi: 10.1002/dvg.20778; pmid: 21671348
17. L. Zakin, E. M. De Robertis, Extracellular regulation of BMP signaling. Curr. Biol. 20, R89-R92 (2010). doi: 10.1016/j.cub.2009.11.021; pmid: 20144774
18. D. Umulis, M. B. O'Connor, S. S. Blair, The extracellular regulation of bone morphogenetic protein signaling. Development 136, 3715-3728 (2009). doi: 10.1242/dev.031534; pmid: 19855014
19. V. Francois, M. Solloway, J. W. O'Neill, J. Emery, E. Bier, Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene. Genes Dev. 8, 2602-2616 (1994). doi: 10.1101/gad.8.21.2602; pmid: 7958919
20. B. Biehs, V. François, E. Bier, The Drosophila short gastrulation gene prevents Dpp from autoactivating and suppressing neurogenesis in the neuroectoderm. Genes Dev. 10, 2922-2934 (1996). doi: 10.1101/gad.10.22.2922; pmid: 8918893
21. A. Jaźwińska, C. Rushlow, S. Roth, The role of brinker in mediating the graded response to Dpp in early Drosophila embryos. Development 126, 3323-3334 (1999). pmid: 10393112
22. O. Shimmi, D. Umulis, H. Othmer, M. B. O'Connor, Facilitated transport of a Dpp/Scw heterodimer by Sog/Tsg leads to robust patterning of the Drosophila blastoderm embryo. Cell 120, 873-886 (2005). doi: 10.1016/j.cell.2005.02.009; pmid: 15797386
23. S. Srinivasan, K. E. Rashka, E. Bier, Creation of a Sog morphogen gradient in the Drosophila embryo. Dev. Cell 2, 91-101 (2002). doi: 10.1016/S1534-5807(01)00097-1; pmid: 11782317
24. G. Marqués et al., Production of a DPP activity gradient in the early Drosophila embryo through the opposing actions of the SOG and TLD proteins. Cell 91, 417-426 (1997). doi: 10.1016/S0092-8674(00)80425-0; pmid: 9363950
25. Y. C. Wang, E. L. Ferguson, Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning. Nature 434, 229-234 (2005). doi: 10.1038/nature03318; pmid: 15759004
26. E. Negreiros, M. Fontenele, A. R. Câmara, H. Araujo, αPS1βPS integrin receptors regulate the differential distribution of Sog fragments in polarized epithelia. Genesis 48, 31-43 (2010). pmid: 20017203
27. H. Araujo, E. Negreiros, E. Bier, Integrins modulate Sog activity in the Drosophila wing. Development 130, 3851-3864 (2003). doi: 10.1242/dev.00613; pmid: 12835400
28. A. Sawala, C. Sutcliffe, H. L. Ashe, Multistep molecular mechanism for bone morphogenetic protein extracellular transport in the Drosophila embryo. Proc. Natl. Acad. Sci. U.S.A. 109, 11222-11227 (2012). doi: 10.1073/pnas.1202781109; pmid: 22733779
29. A. Aleman et al., Mad linker phosphorylations control the intensity and range of the BMP-activity gradient in developing Drosophila tissues. Sci. Rep. 4, 6927 (2014). doi: 10.1038/srep06927; pmid: 25377173
30. D. M. Umulis, O. Shimmi, M. B. O'Connor, H. G. Othmer, Organism-scale modeling of early Drosophila patterning via bone morphogenetic proteins. Dev. Cell 18, 260-274 (2010). doi: 10.1016/j.devcel.2010.01.006; pmid: 20159596
31. J. Gavin-Smyth, Y. C. Wang, I. Butler, E. L. Ferguson, A genetic network conferring canalization to a bistable patterning system in Drosophila. Curr. Biol. 23, 2296-2302 (2013). doi: 10.1016/j.cub.2013.09.055; pmid: 24184102
32. H. L. Liang, M. Xu, Y. C. Chuang, C. Rushlow, Response to the BMP gradient requires highly combinatorial inputs from multiple patterning systems in the Drosophila embryo. Development 139, 1956-1964 (2012). doi: 10.1242/dev.079772; pmid: 22513375
33. K. Yu et al., Processing of the Drosophila Sog protein creates a novel BMP inhibitory activity. Development 127, 2143-2154 (2000). pmid: 10769238
34. K. Carneiro et al., Graded maternal short gastrulation protein contributes to embryonic dorsal-ventral patterning by delayed induction. Dev. Biol. 296, 203-218 (2006). doi: 10.1016/j.ydbio.2006.04.453; pmid: 16781701
35. K.-H. Kang, E. Bier, dHIP14-dependent palmitoylation promotes secretion of the BMP antagonist Sog. Dev. Biol. 346, 1-10 (2010). doi: 10.1016/j.ydbio.2010.06.024; pmid: 20599894
36. C. M. Mizutani, N. Meyer, H. Roelink, E. Bier, Threshold-dependent BMP-mediated repression: A model for a conserved mechanism that patterns the neuroectoderm. PLOS Biol. 4, e313 (2006). doi: 10.1371/journal.pbio.0040313; pmid: 16968133
37. J. Cowden, M. Levine, Ventral dominance governs sequential patterns of gene expression across the dorsal-ventral axis of the neuroectoderm in the Drosophila embryo. Dev. Biol. 262, 335-349 (2003). doi: 10.1016/S0012-1606(03)00395-6; pmid: 14550796
38. F. F. Esteves et al., BMPs regulate msx gene expression in the dorsal neuroectoderm of Drosophila and vertebrates by distinct mechanisms. PLOS Genet. 10, e1004625 (2014). doi: 10.1371/journal.pgen.1004625; pmid: 25210771
39. E. M. De Robertis, H. Kuroda, Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell Dev. Biol. 20, 285-308 (2004). doi: 10.1146/annurev.cellbio.20.011403.154124; pmid: 15473842
40. M. K. Khokha, J. Yeh, T. C. Grammer, R. M. Harland, Depletion of three BMP antagonists from Spemann's organizer leads to a catastrophic loss of dorsal structures. Dev. Cell 8, 401-411 (2005). doi: 10.1016/j.devcel.2005.01.013; pmid: 15737935
41. J. L. Plouhinec, L. Zakin, Y. Moriyama, E. M. De Robertis, Chordin forms a self-organizing morphogen gradient in the extracellular space between ectoderm and mesoderm in the Xenopus embryo. Proc. Natl. Acad. Sci. U.S.A. 110, 20372-20379 (2013). doi: 10.1073/pnas.1319745110; pmid: 24284174
42. S. C. Little, M. C. Mullins, Bone morphogenetic protein heterodimers assemble heteromeric type I receptor complexes to pattern the dorsoventral axis. Nat. Cell Biol. 11, 637-643 (2009). doi: 10.1038/ncb1870; pmid: 19377468
43. S. Piccolo et al., Cleavage of Chordin by Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity. Cell 91, 407-416 (1997). doi: 10.1016/S0092-8674(00)80424-9; pmid: 9363949
44. H. X. Lee, A. L. Ambrosio, B. Reversade, E. M. De Robertis, Embryonic dorsal-ventral signaling: Secreted frizzled-related proteins as inhibitors of tolloid proteinases. Cell 124, 147-159 (2006). doi: 10.1016/j.cell.2005.12.018; pmid: 16413488
45. H. X. Lee, F. A. Mendes, J. L. Plouhinec, E. M. De Robertis, Enzymatic regulation of pattern: BMP4 binds CUB domains of Tolloids and inhibits proteinase activity. Genes Dev. 23, 2551-2562 (2009). doi: 10.1101/gad.1839309; pmid: 19884260
46. H. Inomata, T. Haraguchi, Y. Sasai, Robust stability of the embryonic axial pattern requires a secreted scaffold for chordin degradation. Cell 134, 854-865 (2008). doi: 10.1016/j.cell.2008.07.008; pmid: 18775317
47. A. L. Ambrosio et al., Crossveinless-2 is a BMP feedback inhibitor that binds Chordin/BMP to regulate Xenopus embryonic patterning. Dev. Cell 15, 248-260 (2008). doi: 10.1016/j.devcel.2008.06.013; pmid: 18694564
48. A. Ralston, S. S. Blair, Long-range Dpp signaling is regulated to restrict BMP signaling to a crossvein competent zone. Dev. Biol. 280, 187-200 (2005). doi: 10.1016/j.ydbio.2005.01.018; pmid: 15766758
49. P. F. Xu, N. Houssin, K. F. Ferri-Lagneau, B. Thisse, C. Thisse, Construction of a vertebrate embryo from two opposing morphogen gradients. Science 344, 87-89 (2014). doi: 10.1126/science.1248252; pmid: 24700857
50. T. A. Appel, The Cuvier-Geoffroy Debate: French Biology in the Decades Before Darwin (Oxford Univ. Press, Oxford, 1987).
51. L. Marjoram, C. Wright, Rapid differential transport of Nodal and Lefty on sulfated proteoglycan-rich extracellular matrix regulates left-right asymmetry in Xenopus. Development 138, 475-485 (2011). doi: 10.1242/dev.056010; pmid: 21205792
52. K. J. Lee, T. M. Jessell, The specification of dorsal cell fates in the vertebrate central nervous system. Annu. Rev. Neurosci. 22, 261-294 (1999). doi: 10.1146/annurev.neuro.22.1.261; pmid: 10202540
53. I. Patten, M. Placzek, Opponent activities of Shh and BMP signaling during floor plate induction in vivo. Curr. Biol. 12, 47-52 (2002). doi: 10.1016/S0960-9822(01)00631-5; pmid: 11790302
54. A. S. Denes et al., Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129, 277-288 (2007). doi: 10.1016/j.cell.2007.02.040; pmid: 17448990
55. D. Arendt, A. S. Denes, G. Jékely, K. Tessmar-Raible, The evolution of nervous system centralization. Philos. Trans. R. Soc. London Ser. B 363, 1523-1528 (2008). doi: 10.1098/rstb.2007.2242; pmid: 18192182
56. D. Ben-Zvi, A. Fainsod, B. Z. Shilo, N. Barkai, Scaling of dorsal-ventral patterning in the Xenopus laevis embryo. BioEssays 36, 151-156 (2014). doi: 10.1002/bies.201300136; pmid: 24323952
57. Y. T. Zhang, A. D. Lander, Q. Nie, Computational analysis of BMP gradients in dorsal-ventral patterning of the zebrafish embryo. J. Theor. Biol. 248, 579-589 (2007). doi: 10.1016/j.jtbi.2007.05.026; pmid: 17673236
58. C. M. Mizutani et al., Formation of the BMP activity gradient in the Drosophila embryo. Dev. Cell 8, 915-924 (2005). doi: 10.1016/j.devcel.2005.04.009; pmid: 15935780
59. A. D. Lander, Pattern, growth, and control. Cell 144, 955-969 (2011). doi: 10.1016/j.cell.2011.03.009; pmid: 21414486
60. S. Restrepo, J. J. Zartman, K. Basler, Coordination of patterning and growth by the morphogen DPP. Curr. Biol. 24, R245-R255 (2014). doi: 10.1016/j.cub.2014.01.055; pmid: 24650915
61. D. Nellen, R. Burke, G. Struhl, K. Basler, Direct and long-range action of a DPP morphogen gradient. Cell 85, 357-368 (1996). doi: 10.1016/S0092-8674(00)81114-9; pmid: 8616891
62. S. Zhou et al., Free extracellular diffusion creates the Dpp morphogen gradient of the Drosophila wing disc. Curr. Biol. 22, 668-675 (2012). doi: 10.1016/j.cub.2012.02.065; pmid: 22445299
63. P. Müller, K. W. Rogers, S. R. Yu, M. Brand, A. F. Schier, Morphogen transport. Development 140, 1621-1638 (2013). doi: 10.1242/dev.083519; pmid: 23533171
64. J. L. Erickson, Formation and maintenance of morphogen gradients: An essential role for the endomembrane system in Drosophila melanogaster wing development. Fly 5, 266-271 (2011). doi: 10.4161/fly.5.3.16542; pmid: 21654212
65. V. Greco, M. Hannus, S. Eaton, Argosomes: A potential vehicle for the spread of morphogens through epithelia. Cell 106, 633-645 (2001). doi: 10.1016/S0092-8674(01)00484-6; pmid: 11551510
66. S. Pfeiffer, C. Alexandre, M. Calleja, J. P. Vincent, The progeny of wingless-expressing cells deliver the signal at a distance in Drosophila embryos. Curr. Biol. 10, 321-324 (2000). doi: 10.1016/S0960-9822(00)00381-X; pmid: 10744976
67. S. Roy, H. Huang, S. Liu, T. B. Kornberg, Cytoneme-mediated contact-dependent transport of the Drosophila decapentaplegic signaling protein. Science 343, 1244624 (2014). doi: 10.1126/science.1244624; pmid: 24385607
68. S. Roy, F. Hsiung, T. B. Kornberg, Specificity of Drosophila cytonemes for distinct signaling pathways. Science 332, 354-358 (2011). doi: 10.1126/science.1198949; pmid: 21493861
69. F. Hsiung, F.-A. Ramirez-Weber, D. D. Iwaki, T. B. Kornberg, Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic. Nature 437, 560-563 (2005). doi: 10.1038/nature03951; pmid: 16177792
70. M. Sato, T. B. Kornberg, FGF is an essential mitogen and chemoattractant for the air sacs of the Drosophila tracheal system. Dev. Cell 3, 195-207 (2002). doi: 10.1016/S1534-5807(02)00202-2; pmid: 12194851
71. F. A. Ramírez-Weber, T. B. Kornberg, Cytonemes: Cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 97, 599-607 (1999). doi: 10.1016/S0092-8674(00)80771-0; pmid: 10367889
72. T. A. Sanders, E. Llagostera, M. Barna, Specialized filopodia direct long-range transport of SHH during vertebrate tissue patterning. Nature 497, 628-632 (2013). doi: 10.1038/nature12157; pmid: 23624372
73. M. Nahmad, A. Stathopoulos, Dynamic interpretation of hedgehog signaling in the Drosophila wing disc. PLOS Biol. 7, e1000202 (2009). doi: 10.1371/journal.pbio.1000202; pmid: 19787036
74. C. Alexandre, A. Baena-Lopez, J. P. Vincent, Patterning and growth control by membrane-tethered Wingless. Nature 505, 180-185 (2014). doi: 10.1038/nature12879; pmid: 24390349
75. P. McHale et al., Gene length may contribute to graded transcriptional responses in the Drosophila embryo. Dev. Biol. 360, 230-240 (2011). doi: 10.1016/j.ydbio.2011.08.016; pmid: 21920356
76. E. Kutejova, J. Briscoe, A. Kicheva, Temporal dynamics of patterning by morphogen gradients. Curr. Opin. Genet. Dev. 19, 315-322 (2009). doi: 10.1016/j.gde.2009.05.004; pmid: 19596567
77. K. F. Liem Jr., G. Tremml, T. M. Jessell, A role for the roof plate and its resident TGFb-related proteins in neuronal patterning in the dorsal spinal cord. Cell 91, 127-138 (1997). doi: 10.1016/S0092-8674(01)80015-5; pmid: 9335341
78. M. Lek et al., A homeodomain feedback circuit underlies step-function interpretation of a Shh morphogen gradient during ventral neural patterning. Development 137, 4051-4060 (2010). doi: 10.1242/dev.054288; pmid: 21062862
79. A. D. Lander, W. C. Lo, Q. Nie, F. Y. Wan, The measure of success: Constraints, objectives, and tradeoffs in morphogen-mediated patterning. Cold Spring Harb. Perspect. Biol. 1, a002022 (2009). doi: 10.1101/cshperspect.a002022; pmid: 20066078
80. F. Hamaratoglu, A. M. de Lachapelle, G. Pyrowolakis, S. Bergmann, M. Affolter, Dpp signaling activity requires Pentagone to scale with tissue size in the growing Drosophila wing imaginal disc. PLOS Biol. 9, e1001182 (2011). doi: 10.1371/journal.pbio.1001182; pmid: 22039350
81. R. Vuilleumier et al., Control of Dpp morphogen signalling by a secreted feedback regulator. Nat. Cell Biol. 12, 611-617 (2010). doi: 10.1038/ncb2064; pmid: 20453847
82. L. A. Baena-Lopez, H. Nojima, J. P. Vincent, Integration of morphogen signalling within the growth regulatory network. Curr. Opin. Cell Biol. 24, 166-172 (2012). doi: 10.1016/j.ceb.2011.12.010; pmid: 22257639
83. F. Galton, Vox populi. Nature 75, 450-451 (1907).
84. J. Surowiecki, The Wisdom of Crowds (Anchor Books/Random House, New York, 2004).
85. S. A. Holley et al., A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 376, 249-253 (1995). doi: 10.1038/376249a0; pmid: 7617035
86. J. Schmidt, V. Francois, E. Bier, D. Kimelman, Drosophila short gastrulation induces an ectopic axis in Xenopus: Evidence for conserved mechanisms of dorsal-ventral patterning. Development 121, 4319-4328 (1995). pmid: 8575332
87. R. W. Padgett, J. M. Wozney, W. M. Gelbart, Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc. Natl. Acad. Sci. U.S.A. 90, 2905-2909 (1993). doi: 10.1073/pnas.90.7.2905; pmid: 8464906
88. Y. Goltsev et al., Evolution of the dorsal-ventral patterning network in the mosquito, Anopheles gambiae. Development 134, 2415-2424 (2007). doi: 10.1242/dev.02863; pmid: 17522157
89. Y. Akiyama-Oda, H. Oda, Axis specification in the spider embryo: Dpp is required for radial-to-axial symmetry transformation and sog for ventral patterning. Development 133, 2347-2357 (2006). doi: 10.1242/dev.02400; pmid: 16720876
90. M. D. Molina et al., Noggin and noggin-like genes control dorsoventral axis regeneration in planarians. Curr. Biol. 21, 300-305 (2011). doi: 10.1016/j.cub.2011.01.016; pmid: 21295481
91. M. A. Gaviño, P. W. Reddien, A Bmp/Admp regulatory circuit controls maintenance and regeneration of dorsal-ventral polarity in planarians. Curr. Biol. 21, 294-299 (2011). doi: 10.1016/j.cub.2011.01.017; pmid: 21295483
92. P. W. Reddien, A. L. Bermange, A. M. Kicza, A. Sánchez Alvarado, BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration. Development 134, 4043-4051 (2007). doi: 10.1242/dev.007138; pmid: 17942485
93. F. Lapraz, L. Besnardeau, T. Lepage, Patterning of the dorsal-ventral axis in echinoderms: Insights into the evolution of the BMP-chordin signaling network. PLOS Biol. 7, e1000248 (2009). doi: 10.1371/journal.pbio.1000248; pmid: 19956794
94. J. K. Yu et al., Axial patterning in cephalochordates and the evolution of the organizer. Nature 445, 613-617 (2007). doi: 10.1038/nature05472; pmid: 17237766
95. E. Bier, Evolution of development: Diversified dorsoventral patterning. Curr. Biol. 21, R591-R594 (2011). doi: 10.1016/j.cub.2011.06.037; pmid: 21820625
96. G. Genikhovich et al., Axis patterning by BMPs: Cnidarian network reveals evolutionary constraints. Cell Rep. 10, 1646-1654 (2015). doi: 10.1016/j.celrep.2015.02.035
97. C. Niehrs, On growth and form: A Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 137, 845-857 (2010). doi: 10.1242/dev.039651; pmid: 20179091
98. J. W. Valentine, On The Origin of Phyla (Univ. of Chicago Press, Chicago, ed. 1, 2004).
99. C. J. Lowe et al., Dorsoventral patterning in hemichordates: Insights into early chordate evolution. PLOS Biol. 4, e291 (2006). doi: 10.1371/journal.pbio.0040291; pmid: 16933975
100. M. van der Zee, O. Stockhammer, C. von Levetzow, R. Nunes da Fonseca, S. Roth, Sog/Chordin is required for ventral-to-dorsal Dpp/BMP transport and head formation in a short germ insect. Proc. Natl. Acad. Sci. U.S.A. 103, 16307-16312 (2006). doi: 10.1073/pnas.0605154103; pmid: 17050690
101. H. L. Ashe, M. Levine, Local inhibition and long-range enhancement of Dpp signal transduction by Sog. Nature 398, 427-431 (1999). doi: 10.1038/18892; pmid: 10201373
102. E. Bier, Developmental biology: A unity of opposites. Nature 398, 375-376 (1999). pmid: 10201364
103. K. Yu et al., Cysteine repeat domains and adjacent sequences determine distinct bone morphogenetic protein modulatory activities of the Drosophila Sog protein. Genetics 166, 1323-1336 (2004). doi: 10.1534/genetics.166.3.1323; pmid: 15082551
104. E. Decotto, E. L. Ferguson, A positive role for Short gastrulation in modulating BMP signaling during dorsoventral patterning in the Drosophila embryo. Development 128, 3831-3841 (2001). pmid: 11585808
105. E. L. Ferguson, K. V. Anderson, Localized enhancement and repression of the activity of the TGF-β family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development 114, 583-597 (1992). pmid: 1618130
106. E. L. Ferguson, Conservation of dorsal-ventral patterning in arthropods and chordates. Curr. Opin. Genet. Dev. 6, 424-431 (1996). doi: 10.1016/S0959-437X(96)80063-3; pmid: 8791529
107. D. M. Umulis, M. Serpe, M. B. O'Connor, H. G. Othmer, Robust, bistable patterning of the dorsal surface of the Drosophila embryo. Proc. Natl. Acad. Sci. U.S.A. 103, 11613-11618 (2006). doi: 10.1073/pnas.0510398103; pmid: 16864795
108. A. M. Rafiqi, C. H. Park, C. W. Kwan, S. Lemke, U. Schmidt-Ott, BMP-dependent serosa and amnion specification in the scuttle fly Megaselia abdita. Development 139, 3373-3382 (2012). doi: 10.1242/dev.083873; pmid: 22874914
109. Y. Akiyama-Oda, H. Oda, Early patterning of the spider embryo: A cluster of mesenchymal cells at the cumulus produces Dpp signals received by germ disc epithelial cells. Development 130, 1735-1747 (2003). doi: 10.1242/dev.00390; pmid: 12642480
110. D. Bachiller et al., The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature 403, 658-661 (2000). doi: 10.1038/35001072; pmid: 10688202
111. A. Lauri et al., Development of the annelid axochord: Insights into notochord evolution. Science 345, 1365-1368 (2014). pmid: 25214631
112. D. H. Kuo, D. A. Weisblat, A new molecular logic for BMP-mediated dorsoventral patterning in the leech Helobdella. Curr. Biol. 21, 1282-1288 (2011). doi: 10.1016/j.cub.2011.06.024; pmid: 21782437
113. S. V. Nuzhdin et al., Natural genetic variation in transcriptome reflects network structure inferred with major effect mutations: Insulin/TOR and associated phenotypes in Drosophila melanogaster. BMC Genomics 10, 124 (2009). doi: 10.1186/1471-2164-10-124; pmid: 19317915
114. I. Dworkin et al., The effects of weak genetic perturbations on the transcriptome of the wing imaginal disc and its association with wing shape in Drosophila melanogaster. Genetics 187, 1171-1184 (2011). doi: 10.1534/genetics.110.125922; pmid: 21288875
115. E. Bier, The Coiled Spring: How Life Begins (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, ed. 1, 2000).
116. D. Kosman et al., Multiplex detection of RNA expression in Drosophila embryos. Science 305, 846 (2004). doi: 10.1126/science.1099247; pmid: 15297669
117. J. C. Illes, E. Winterbottom, H. V. Isaacs, Cloning and expression analysis of the anterior parahox genes, Gsh1 and Gsh2 from Xenopus tropicalis. Dev. Dyn. 238, 194-203 (2009). doi: 10.1002/dvdy.21816; pmid: 19097192
118. T. B. Kornberg, S. Roy, Cytonemes as specialized signaling filopodia. Development 141, 729-736 (2014). doi: 10.1242/dev.086223; pmid: 24496611
119. E. Bier, Drawing lines in the Drosophila wing: Initiation of wing vein development. Curr. Opin. Genet. Dev. 10, 393-398 (2000). doi: 10.1016/S0959-437X(00)00102-7; pmid: 10889058