Sog/Chordin is required for ventral-to-dorsal Dpp/BMP transport and head formation in a short germ insect

Bone morphogenetic protein (BMP) signaling plays a major role in dorsoventral patterning in vertebrates and in Drosophila. Remarkably, in Tribolium, a beetle with an ancestral type of insect development, early BMP/dpp exhibits differential expression along the anteroposterior axis. However, the BMP/Dpp inhibitor Sog/chordin is expressed ventrally and establishes a dorsal domain of BMP/Dpp activity by transporting BMPs toward the dorsal side, like in Drosophila. Loss of Tribolium Sog not only abolishes dorsoventral polarity in the ectoderm, but also leads to the complete absence of the CNS. This phenotype suggests that sog is the main BMP antagonist in Tribolium, in contrast to vertebrates and Drosophila, which possess redundant antagonists. Surprisingly, Sog also is required for head formation in Tribolium, as are the BMP antagonists in vertebrates. Thus, in Tribolium, the system of BMP and its antagonists is less complex than in Drosophila or vertebrates and combines features from both, suggesting that it might represent an ancestral state.

[1]  T. Holstein,et al.  Asymmetric expression of the BMP antagonists chordin and gremlin in the sea anemone Nematostella vectensis: implications for the evolution of axial patterning. , 2006, Developmental biology.

[2]  D. Tautz,et al.  A Segmentation Gene in Tribolium Produces a Polycistronic mRNA that Codes for Multiple Conserved Peptides , 2006, Cell.

[3]  K. Ober,et al.  The roles of wingless and decapentaplegic in axis and appendage development in the red flour beetle, Tribolium castaneum. , 2006, Developmental biology.

[4]  H. Oda,et al.  Axis specification in the spider embryo: dpp is required for radial-to-axial symmetry transformation and sog for ventral patterning , 2006, Development.

[5]  M. Martindale,et al.  Dorso/Ventral Genes Are Asymmetrically Expressed and Involved in Germ-Layer Demarcation during Cnidarian Gastrulation , 2006, Current Biology.

[6]  M. Roossinck.  Symbiosis versus competition in plant virus evolution , 2005, Nature Reviews Microbiology.

[7]  M. Martindale.  The evolution of metazoan axial properties , 2005, Nature Reviews Genetics.

[8]  E. D. De Robertis,et al.  Depletion of Bmp2, Bmp4, Bmp7 and Spemann organizer signals induces massive brain formation in Xenopus embryos , 2005, Development.

[9]  Qing Nie,et al.  Formation of the BMP activity gradient in the Drosophila embryo. , 2005, Developmental cell.

[10]  S. Roth,et al.  Distinct Functions of the Tribolium zerknu¨llt Genes in Serosa Specification and Dorsal Closure , 2005, Current Biology.

[11]  H. Othmer,et al.  Facilitated Transport of a Dpp/Scw Heterodimer by Sog/Tsg Leads to Robust Patterning of the Drosophila Blastoderm Embryo , 2005, Cell.

[12]  Yu-Chiun Wang,et al.  Spatial bistability of Dpp–receptor interactions during Drosophila dorsal–ventral patterning , 2005, Nature.

[13]  E. D. De Robertis,et al.  Dorsal-ventral patterning and neural induction in Xenopus embryos. , 2004, Annual review of cell and developmental biology.

[14]  C. Stern.  Gastrulation : from cells to embryo , 2004 .

[15]  S. Roth,et al.  Tribolium castaneum twist: gastrulation and mesoderm formation in a short-germ beetle , 2004, Development Genes and Evolution.

[16]  Mingfa Li,et al.  Stepwise formation of a SMAD activity gradient during dorsal-ventral patterning of the Drosophila embryo , 2003, Development.

[17]  Susan J. Brown,et al.  The expression and function of the achaete-scute genes in Tribolium castaneum reveals conservation and variation in neural pattern formation and cell fate specification , 2003, Development.

[18]  E. Lander,et al.  Anteroposterior Patterning in Hemichordates and the Origins of the Chordate Nervous System , 2003, Cell.

[19]  Ryan M. Anderson,et al.  Chordin and noggin promote organizing centers of forebrain development in the mouse. , 2002, Development.

[20]  N. Barkai,et al.  Robustness of the BMP morphogen gradient in Drosophila embryonic patterning , 2022 .

[21]  Urs Schmidt-Ott,et al.  A single Hox3 gene with composite bicoid and zerknüllt expression characteristics in non-Cyclorrhaphan flies , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M. Mullins,et al.  Dorsoventral patterning in the zebrafish: bone morphogenetic proteins and beyond. , 2002, Results and problems in cell differentiation.

[23]  E. Bier,et al.  Creation of a Sog morphogen gradient in the Drosophila embryo. , 2002, Developmental cell.

[24]  R. Dorfman,et al.  Biphasic activation of the BMP pathway patterns the Drosophila embryonic dorsal region. , 2001, Development.

[25]  S. Roth,et al.  The maternal NF-kappaB/dorsal gradient of Tribolium castaneum: dynamics of early dorsoventral patterning in a short-germ beetle. , 2000, Development.

[26]  J. Gerhart.  Inversion of the chordate body axis: are there alternatives? , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Ryan M. Anderson,et al.  The organizer factors Chordin and Noggin are required for mouse forebrain development , 2000, Nature.

[28]  M. Saraste,et al.  FEBS Lett , 2000 .

[29]  T. Tabata,et al.  Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs. , 2000, Molecular cell.

[30]  S. Roth,et al.  The role of brinker in mediating the graded response to Dpp in early Drosophila embryos. , 1999, Development.

[31]  Michael Levine,et al.  Local inhibition and long-range enhancement of Dpp signal transduction by Sog , 1999, Nature.

[32]  C. Heldin,et al.  The L45 loop in type I receptors for TGF‐β family members is a critical determinant in specifying Smad isoform activation , 1998, FEBS letters.

[33]  Ken W. Y. Cho,et al.  Production of a DPP Activity Gradient in the Early Drosophila Embryo through the Opposing Actions of the SOG and TLD Proteins , 1997, Cell.

[34]  B. Biehs,et al.  The Drosophila short gastrulation gene prevents Dpp from autoactivating and suppressing neurogenesis in the neuroectoderm. , 1996, Genes & development.

[35]  Susan J. Brown,et al.  The Tribolium decapentaplegic gene is similar in sequence, structure, and expression to the Drosophila dpp gene , 1996, Development Genes and Evolution.

[36]  Susan J. Brown,et al.  Two orthodenticle-related genes in the short-germ beetle Tribolium castaneum , 1996, Development Genes and Evolution.

[37]  A. Mccarthy.  Development , 1996, Current Opinion in Neurobiology.

[38]  M. Levine,et al.  The screw gene encodes a ubiquitously expressed member of the TGF-beta family required for specification of dorsal cell fates in the Drosophila embryo. , 1994, Genes & development.

[39]  J. Emery,et al.  Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene. , 1994, Genes & development.

[40]  D. Arendt,et al.  Inversion of dorsoventral axis? , 1994, Nature.

[41]  R. Sommer,et al.  Expression patterns of twist and snail in Tribolium (Coleoptera) suggest a homologous formation of mesoderm in long and short germ band insects. , 1994, Developmental genetics.

[42]  W. Gelbart,et al.  An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. , 1993, Development.

[43]  K. Anderson,et al.  decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo , 1992, Cell.

[44]  C. Nüsslein-Volhard,et al.  The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. , 1991, Development.

[45]  C. Nüsslein-Volhard,et al.  A gradient of nuclear localization of the dorsal protein determines dorsoventral pattern in the Drosophila embryo , 1989, Cell.

[46]  W. Gelbart,et al.  Decapentaplegic transcripts are localized along the dorsal‐ventral axis of the Drosophila embryo. , 1987, The EMBO journal.