Dynamic BMP Signaling Polarized by Toll Patterns the Dorsoventral Axis in a Hemimetabolous Insect

Overview

Journal Elife

Specialty Biology

Date 2015 May 13

PMID 25962855

Citations 19

Authors

Lena Sachs

Yen-Ta Chen

Axel Drechsler

Jeremy A Lynch

Kristen A Panfilio

Michael Lassig

Johannes Berg

Siegfried Roth

Affiliations

Soon will be listed here.

Abstract

Toll-dependent patterning of the dorsoventral axis in Drosophila represents one of the best understood gene regulatory networks. However, its evolutionary origin has remained elusive. Outside the insects Toll is not known for a patterning function, but rather for a role in pathogen defense. Here, we show that in the milkweed bug Oncopeltus fasciatus, whose lineage split from Drosophila's more than 350 million years ago, Toll is only required to polarize a dynamic BMP signaling network. A theoretical model reveals that this network has self-regulatory properties and that shallow Toll signaling gradients are sufficient to initiate axis formation. Such gradients can account for the experimentally observed twinning of insect embryos upon egg fragmentation and might have evolved from a state of uniform Toll activity associated with protecting insect eggs against pathogens.

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References

Liu P, Kaufman T . Morphology and husbandry of the large milkweed bug, Oncopeltus fasciatus. Cold Spring Harb Protoc. 2010; 2009(8):pdb.emo127. DOI: 10.1101/pdb.emo127. View

Hong J, Hendrix D, Papatsenko D, Levine M . How the Dorsal gradient works: insights from postgenome technologies. Proc Natl Acad Sci U S A. 2008; 105(51):20072-6. PMC: 2629255. DOI: 10.1073/pnas.0806476105. View

Umulis D, Shimmi O, OConnor M, Othmer H . Organism-scale modeling of early Drosophila patterning via bone morphogenetic proteins. Dev Cell. 2010; 18(2):260-74. PMC: 2848394. DOI: 10.1016/j.devcel.2010.01.006. View

Xue Y, Zheng X, Huang L, Xu P, Ma Y, Min Z . Organizer-derived Bmp2 is required for the formation of a correct Bmp activity gradient during embryonic development. Nat Commun. 2014; 5:3766. PMC: 4071459. DOI: 10.1038/ncomms4766. View

OConnor M, Umulis D, Othmer H, Blair S . Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development. 2005; 133(2):183-93. PMC: 6469686. DOI: 10.1242/dev.02214. View

Akiyama-Oda Y, Oda H . Axis specification in the spider embryo: dpp is required for radial-to-axial symmetry transformation and sog for ventral patterning. Development. 2006; 133(12):2347-57. DOI: 10.1242/dev.02400. View

Roth S, Hiromi Y, Godt D, Nusslein-Volhard C . cactus, a maternal gene required for proper formation of the dorsoventral morphogen gradient in Drosophila embryos. Development. 1991; 112(2):371-88. DOI: 10.1242/dev.112.2.371. View

Langdon Y, Mullins M . Maternal and zygotic control of zebrafish dorsoventral axial patterning. Annu Rev Genet. 2011; 45:357-77. DOI: 10.1146/annurev-genet-110410-132517. View

Gierer A, Meinhardt H . A theory of biological pattern formation. Kybernetik. 1972; 12(1):30-9. DOI: 10.1007/BF00289234. View

10.

Jacobs C, van der Zee M . Immune competence in insect eggs depends on the extraembryonic serosa. Dev Comp Immunol. 2013; 41(2):263-9. DOI: 10.1016/j.dci.2013.05.017. View

11.

Berni M, Fontenele M, Tobias-Santos V, Caceres-Rodrigues A, Mury F, Vionette-do-Amaral R . Toll signals regulate dorsal-ventral patterning and anterior-posterior placement of the embryo in the hemipteran Rhodnius prolixus. Evodevo. 2015; 5:38. PMC: 4407881. DOI: 10.1186/2041-9139-5-38. View

12.

Saina M, Genikhovich G, Renfer E, Technau U . BMPs and chordin regulate patterning of the directive axis in a sea anemone. Proc Natl Acad Sci U S A. 2009; 106(44):18592-7. PMC: 2773963. DOI: 10.1073/pnas.0900151106. View

13.

Schulte-Merker S, Lee K, McMahon A, Hammerschmidt M . The zebrafish organizer requires chordino. Nature. 1997; 387(6636):862-3. DOI: 10.1038/43092. View

14.

Inomata H, Shibata T, Haraguchi T, Sasai Y . Scaling of dorsal-ventral patterning by embryo size-dependent degradation of Spemann's organizer signals. Cell. 2013; 153(6):1296-311. DOI: 10.1016/j.cell.2013.05.004. View

15.

Von Ohlen T, Doe C . Convergence of dorsal, dpp, and egfr signaling pathways subdivides the drosophila neuroectoderm into three dorsal-ventral columns. Dev Biol. 2000; 224(2):362-72. DOI: 10.1006/dbio.2000.9789. View

16.

Ben-Zvi D, Shilo B, Fainsod A, Barkai N . Scaling of the BMP activation gradient in Xenopus embryos. Nature. 2008; 453(7199):1205-11. DOI: 10.1038/nature07059. View

17.

Liberman L, Stathopoulos A . Design flexibility in cis-regulatory control of gene expression: synthetic and comparative evidence. Dev Biol. 2009; 327(2):578-89. PMC: 2746413. DOI: 10.1016/j.ydbio.2008.12.020. View

18.

Eldar A, Dorfman R, Weiss D, Ashe H, Shilo B, Barkai N . Robustness of the BMP morphogen gradient in Drosophila embryonic patterning. Nature. 2002; 419(6904):304-8. DOI: 10.1038/nature01061. View

19.

De Robertis E . Evo-devo: variations on ancestral themes. Cell. 2008; 132(2):185-95. PMC: 2280037. DOI: 10.1016/j.cell.2008.01.003. View

20.

Lynch J, Roth S . The evolution of dorsal-ventral patterning mechanisms in insects. Genes Dev. 2011; 25(2):107-18. PMC: 3022256. DOI: 10.1101/gad.2010711. View