The evolution of dorsal-ventral patterning mechanisms in insects

Genes and Development

Volumn 25, Issue 2, 2011, Pages 107-118

  Lynch, Jeremy A ^a   Roth, Siegfried ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

BMP signaling; Dorsal; Drosophila; Nasonia; Toll signaling; Tribolium

Indexed keywords

BONE MORPHOGENETIC PROTEIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; STAT PROTEIN; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST;

DROSOPHILA; EMBRYO DEVELOPMENT; EMBRYOLOGY; GASTRULATION; GENE EXPRESSION; GENE REGULATORY NETWORK; INSECT; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; RNA INTERFERENCE; TRIBOLIUM;

ANIMALS; BIOLOGICAL EVOLUTION; BODY PATTERNING; DROSOPHILA MELANOGASTER; EMBRYONIC DEVELOPMENT; INSECTS; OOGENESIS;

HEXAPODA; NASONIA;

EID: 78651503848     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.2010711     Document Type: Review

References (82)

1. Akiyama-Oda Y, Oda H. 2006. Axis specification in the spider embryo: dpp is required for radial-to-axial symmetry transformation and sog for ventral patterning. Development 133: 2347-2357.
2. Araujo H, Bier E. 2000. sog and dpp exert opposing maternal functions to modify Toll signaling and pattern the dorsoventral axis of the Drosophila embryo. Development 127: 3631-3644.
3. Berghammer AJ, Klingler M, Wimmer EA. 1999. A universal marker for transgenic insects. Nature 402: 370-371.
4. Brent AE, Yucel G, Small S, Desplan C. 2007. Permissive and instructive anterior patterning rely on mRNA localization in the wasp embryo. Science 315: 1841-1843.
5. Bucher G, Scholten J, Klingler M. 2002. Parental RNAi in Tribolium (Coleoptera). Curr Biol 12: R85-R86. doi: 10.1016/S0960-9822(02)00666-8.
6. Büning J. 1994. The insect ovary. Chapman & Hall, London. Cande
7. J, Goltsev Y, Levine MS. 2009. Conservation of enhancer location in divergent insects. Proc Natl Acad Sci 106: 14414-14419.
8. Chen G, Handel K, Roth S. 2000. The maternal NF-κB/Dorsal gradient of Tribolium castaneum: Dynamics of early dorsoventral patterning in a short-germ beetle. Development 127: 5145-5156.
9. Cho YS, Stevens LM, Stein D. 2010. Pipe-dependent ventral processing of easter by snake is the defining step in Drosophila embryo DV axis formation. Curr Biol 20: 1133-1137.
10. Crocker J, Tamori Y, Erives A. 2008. Evolution acts on enhancer organization to fine-tune gradient threshold readouts. PLoS Biol 6: 2576-2587.
11. da Fonseca RN, von Levetzow C, Kaischeuer P, Basal A, van der Zee M, Roth S. 2008. Self-regulatory circuits in dorsoventral axis formation of the short-germ beetle Tribolium castaneum. Dev Cell 14: 605-615.
12. da Fonseca RN, van der Zee M, Roth S. 2010. Evolution of extracellular Dpp modulators in insects: The roles of tolloid and twisted-gastrulation in dorsoventral patterning of the Tribolium embryo. Dev Biol 345: 80-93.
13. Davis GK, Patel NH. 2002. Short, long, and beyond: Molecular and embryological approaches to insect segmentation. Annu Rev Entomol 47: 669-699.
14. Dearden PK, Akam M. 2001. Early embryo patterning in the grasshopper, Schistocerca gregaria: Wingless, decapentaplegic and caudal expression. Development 128: 3435-3444.
15. De Robertis EM. 2008. Evo-Devo: Variations on ancestral themes. Cell 132: 185-195.
16. De Robertis EM. 2009. Spemann's organizer and the self-regulation of embryonic fields. Mech Dev 126: 925-941.
17. Erives A, Levine M. 2004. Coordinate enhancers share common organizational features in the Drosophila genome. Proc Natl Acad Sci 101: 3851-3856. (Pubitemid 38381066)
18. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531-1545.
19. Gabay L, Scholz H, Golembo M, Klaes A, Shilo BZ, Klämbt C. 1996. EGF receptor signaling induces pointed P1 transcription and inactivates Yan protein in the Drosophila embryonic ventral ectoderm. Development 122: 3355-3362. (Pubitemid 26395978)
20. Handel K, Basal A, Fan X, Roth S. 2005. Tribolium castaneum twist: Gastrulation and mesoderm formation in a short-germ beetle. Dev Genes Evol 215: 13-31.
21. Hong JW, Hendrix DA, Papatsenko D, Levine MS. 2008. How the Dorsal gradient works: Insights from postgenome technologies. Proc Natl Acad Sci 105: 20072-20076.
22. Hughes CL, Kaufman TC. 2000. RNAi analysis of Deformed, proboscipedia and Sex combs reduced in the milkweed bug Oncopeltus fasciatus: Novel roles for Hox genes in the Hemipteran head. Development 127: 3683-3694.
23. The International Aphid Genomics Consortium. 2010. Genome sequence of the pea aphid Acyrthosiphon pisum. Plos Biology 8: e1000313. doi: 10.1371/journal.pbio.1000313.
24. Kanodia JS, Rikhy R, Kim Y, Lund VK, DeLotto R, Lippincott-Schwartz J, Shvartsman SY. 2009. Dynamics of the Dorsal morphogen gradient. Proc Natl Acad Sci 106: 21707-21712.
25. Krause G. 1953. Die Aktionsfolge zur Gestaltung des Keimstreifs von Tachycines (Saltatoria), insbesondere das morphogenetische Konstruktionsbild bei Duplicitas parallela. Dev Genes Evol 146: 275-370.
26. Krause G, Krause J. 1965. Über das Vermögen median durchschnittener Keimanlagen von Bombyx mori L. sich. in ovo und sich ohne Dottersystem in vitro zwillingsartig zu entwickeln. Z Naturforsch B 20: 334-339.
27. Kuethe H-W. 1966. Das Differenzierungszentrum als selbstregulierendes Faktorensystem für den Aufbau der Keimanlage im Ei von Dermestes frischi (Coleoptera). Roux'. Archiv fûr Entwicklungsmechanik 157: 212-302.
28. Liberman LM, Stathopoulos A. 2009. Design flexibility in cisregulatory control of gene expression: Synthetic and comparative evidence. Dev Biol 327: 578-589.
29. Liberman LM, Reeves GT, Stathopoulos A. 2009. Quantitative imaging of the Dorsal nuclear gradient reveals limitations to threshold-dependent patterning in Drosophila. Proc Natl Acad Sci 106: 22317-22322.
30. Lynch JA, Desplan C. 2006. A method for parental RNA interference in the wasp Nasonia vitripennis. Nat Protoc 1: 486-494.
31. Lynch JA, Brent AE, Leaf DS, Pultz MA, Desplan C. 2006. Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature 439: 728-732.
32. Lynch JA, Peel AD, Drechsler A, Averof M, Roth S. 2010. EGF signaling and the origin of axial polarity among the insects. Curr Biol 20: 1042-1047.
33. Markstein M, Zinzen R, Markstein P, Yee KP, Erives A, Stathopoulos A, Levine M. 2004. A regulatory code for neurogenic gene expression in the Drosophila embryo. Development 131: 2387-2394.
34. Meinhardt H. 1989. Models for positional signalling with application to the dorsoventral patterning of insects and segregation into different cell types. Development 107: 169-180.
35. Meinhardt H. 2004. Different strategies for midline formation in bilaterians. Nat Rev Neurosci 5: 502-510.
36. Miya K and Kobayashi K. 1974. The embryonic development of Atrachya menetriesi. Faldermann (Coleoptera, Chrysomelidae). II. Analyses of early development by ligation and low temperature treatment. J Fac Agric Iwate Univ 12: 39-55.
37. Miyawaki K, Mito T, Sarashina I, Zhang HJ, Shinmyo Y, Ohuchi H, Noji S. 2004. Involvement of Wingless/Armadillo signaling in the posterior sequential segmentation in the cricket, Gryllus bimaculatus (Orthoptera), as revealed by RNAi analysis. Mech Dev 121: 119-130.
38. Mizutani CM, Bier E. 2008. EvoD/Vo: The origins of BMP signalling in the neuroectoderm. Nat Rev Genet 9: 663-677.
39. Mizutani CM, Meyer N, Roelink H, Bier E. 2006. Threshold-dependent BMP-mediated repression: A model for a conserved mechanism that patterns the neuroectoderm. PLoS Biol 4: 1777-1788.
40. Morisato D. 2001. Spatzle regulates the shape of the Dorsal gradient in the Drosophila embryo. Development 128: 2309-2319.
41. Moussian B, Roth S. 2005. Dorsoventral axis formation in the Drosophila embryo - Shaping and transducing a morphogen gradient. Curr Biol 15: R887-R899. doi: 10.1016/j.cub.2005.10.026.
42. Nakamura T, Yoshizaki M, Ogawa S, Okamoto H, Shinmyo Y, Bando T, Ohuchi H, Noji S, Mito T. 2010. Imaging of transgenic cricket embryos reveals cell movements consistent with a syncytial patterning mechanism. Curr Biol 20: 1641-1647.
43. Netzel H. 1965. Über die Übereinstimmung von Polarität und Bilateralsymmetrie in Embryo, Ei, Oocyte, und Oocytenkern bei Gryllus domesticus L. Roux' Archiv für Entwicklungsmechanik 156: 88-95.
44. Netzel H. 1968. Die ausprägung von Polarität und Bilateralsymmetrie in den Oocyten von Gryllus domesticus L. Roux' Archiv für Entwicklungsmechanik 160: 119-166.
45. Neuman-Silberberg FS, Schuepbach T. 1993. The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGF-α-like protein. Cell 75: 165-174.
46. O'Connor MB, Umulis D, Othmer HG, Blair SS. 2006. Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 133: 183-193.
47. Ohde T, Masumota M, Yaginuma T, Niimi T. 2009. Embryonic RNAi analysis in the firebrat, Thermobia domestica: Distalless is required to form caudal filament. J Insect Biotechnol Sericology 78: 99-105.
48. Olesnicky EC, Desplan C. 2007. Distinct mechanisms for mRNA localization during embryonic axis specification in the wasp Nasonia. Dev Biol 306: 134-142.
49. Papatsenko D. 2007. ClusterDraw web server: A tool to identify and visualize clusters of binding motifs for transcription factors. Bioinformatics 23: 1032-1034.
50. Pavlopoulos A, Berghammer AJ, Averof M, Klingler M. 2004. Efficient transformation of the beetle Tribolium castaneum using the Minos transposable element: Quantitative and qualitative analysis of genomic integration events. Genetics 167: 737-746.
51. Peloquin JJ, Thibault ST, Staten R, Miller TA. 2000. Germ-line transformation of pink bollworm (Lepidoptera: gelechiidae) mediated by the piggyBac transposable element. Insect Mol Biol 9: 323-333.
52. Petersen CP, Reddien PW. 2009. Wnt signaling and the polarity of the primary body axis. Cell 139: 1056-1068.
53. Price AL, Modrell MS, Hannibal RL, Patel NH. 2010. Mesoderm and ectoderm lineages in the crustacean Parhyale hawaiensis display intra-germ layer compensation. Dev Biol 341: 256-266.
54. Reversade B, De Robertis EM. 2005. Regulation of ADMP and BMP2/4/7 at opposite embryonic poles generates a self-regulating morphogenetic field. Cell 123: 1147-1160.
55. Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, Beeman RW, Gibbs R, Bucher G, Friedrich M, Grimmelikhuijzen CJP, et al. 2008. The genome of the model beetle and pest Tribolium castaneum. Nature 452: 949-955.
56. Roth S. 2003. The origin of dorsoventral polarity in Drosophila. Philos Trans R Soc Lond B Biol Sci 358: 1317-1329.
57. Roth S. 2004. Gastrulation in other insects. In Gastrulation (ed. C. Stern), pp. 105-121. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
58. Roth S, Lynch JA. 2009. Symmetry breaking during Drosophila oogenesis. Cold Spring Harb Perspect Biol 1: a001891. doi: 10.1101/cshperspect.a001891.
59. Roth S, Schupbach T. 1994. The relationship between ovarian and embryonic dorsoventral patterning in Drosophila. Development 120: 2245-2257.
60. Rousso T, Lynch J, Yogev S, Roth S, Schejter ED, Shilo BZ. 2010. Generation of distinct signaling modes via diversification of the Egfr ligand-processing cassette. Development 137: 3427-3437.
61. Sander K. 1971. Pattern formation in longitudinal halves of leaf hopper eggs (Homoptera) and some remarks on definition of embryonic regulation. Wilhelm Roux' Arch Entwickl Mech Org 167: 336.
62. Sandmann T, Girardot C, Brehme M, Tongprasit W, Stolc V, Furlong EE. 2007. A core transcriptional network for early mesoderm development in Drosophila melanogaster. Genes & Dev 21: 436-449.
63. Schupbach T, Roth S. 1994. Dorsoventral patterning in Drosophila oogenesis. Curr Opin Genet Dev 4: 502-507.
64. Schweitzer R, Shaharabany M, Seger R, Shilo BZ. 1995. Secreted Spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination. Genes Dev 9: 1518-1529.
65. Sen J, Goltz JS, Stevens L, Stein D. 1998. Spatially restricted expression of pipe in the Drosophila egg chamber defines embryonic dorsal-ventral polarity. Cell 95: 471-481.
66. Shigenobu S, Bickel RD, Brisson JA, Butts T, Chang CC, Christiaens O, Davis GK, Duncan EJ, Ferrier DEK, Iga M, et al. 2010. Comprehensive survey of developmental genes in the pea aphid, Acyrthosiphon pisum: Frequent lineage-specific duplications and losses of developmental genes. Insect Mol Biol 19: 47-62.
67. Stathopoulos A, Levine M. 2004. Whole-genome analysis of Drosophila gastrulation. Curr Opin Genet Dev 14: 477-484.
68. Stathopoulos A, Levine M. 2005. Genomic regulatory networks and animal development. Dev Cell 9: 449-462. (Pubitemid 41430729)
69. Tamura T, Thibert C, Royer C, Kanda T, Abraham E, Kamba M, Komoto N, Thomas JL, Mauchamp B, Chavancy G, et al. 2000. Germline transformation of the silkworm Bombyx mori L. using a piggyBac transposon-derived vector. Nat Biotechnol 18: 81-84.
70. van der Zee M, Stockhammer O, von Levetzow C, da Fonseca RN, Roth S. 2006. Sog/Chordin is required for ventral-todorsal Dpp/BMP transport and head formation in a short germ insect. Proc Natl Acad Sci 103: 16307-16312.
71. Van der Zee M, da Fonseca RN, Roth S. 2008. TGF β signaling in Tribolium: Vertebrate-like components in a beetle. Dev Genes Evol 218: 203-213.
72. Vargas-Vila MA, Hannibal RL, Parchem RJ, Liu PZ, Patel NH. 2010. A prominent requirement for single-minded and the ventral midline in patterning the dorsoventral axis of the crustacean Parhyale hawaiensis. Development 137: 3469-3476.
73. Von Ohlen T, Doe CQ. 2000. Convergence of dorsal, Dpp, and Egfr signaling pathways subdivides the Drosophila neuroectoderm into three dorsal-ventral columns. Dev Biol 224: 362-372.
74. Wang YC, Ferguson EL. 2005. Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning. Nature 434: 229-234.
75. Weinstock GM, Robinson GE, Gibbs RA, Worley KC, Evans JD, Maleszka R, Robertson HM, Weaver DB, Beye M, Bork P, et al. 2006. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443: 931-949.
76. Werren JH, Richards S, Desjardins CA, Niehuis O, Gadau J, Colbourne JK, Beukeboom LW, Desplan C, Elsik CG, Grimmelikhuijzen CJP, et al. 2010. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327: 343-348.
77. Wheeler SR, Carrico ML, Wilson BA, Skeath JB. 2005. The Tribolium columnar genes reveal conservation and plasticity in neural precursor patterning along the embryonic dorsal-ventral axis. Dev Biol 279: 491-500.
78. Wiegmann BM, Trautwein MD, Kim JW, Cassel BK, Bertone MA, Winterton SL, Yeates DK. 2009. Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biol 7: 34. doi: 10.1186/1741-7007-7-34.
79. Zeitlinger J, Zinzen RP, Stark A, Kellis M, Zhang H, Young RA, Levine M. 2007. Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. Genes Dev 21: 385-390.
80. Zhang ZY, Stevens LM, Stein D. 2009a. Sulfation of eggshell components by pipe defines dorsal-ventral polarity in the Drosophila embryo. Curr Biol 19: 1200-1205.
81. Zhang ZY, Zhu XJ, Stevens LM, Stein D. 2009b. Distinct functional specificities are associated with protein isoforms encoded by the Drosophila dorsal-ventral patterning gene pipe. Development 136: 2779-2789.
82. Zinzen RP, Cande J, Ronshaugen M, Papatsenko D, Levine M. 2006. Evolution of the ventral midline in insect embryos. Dev Cell 11: 895-902.