Skip to main content
SpringerLink
Log in

Evidence for the plasticity of arthropod signal transduction pathways

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

Metazoans are known to contain a limited, yet highly conserved, set of signal transduction pathways that instruct early developmental patterning mechanisms. Genomic surveys that have compared gene conservation in signal transduction pathways between various insects and Drosophila support the conclusion that these pathways are conserved in evolution. However, the degree to which individual components of signal transduction pathways vary among more divergent arthropods is not known. Here, we report our results of a survey of the genome of the two-spotted spider mite Tetranychus urticae, using a set of 294 Drosophila orthologs of genes that function in signal transduction. We find a third of all genes surveyed absent from the spider mite genome. We also identify several novel duplications that have not been previously reported for a chelicerate. In comparison with previous insect surveys, Tetranychus contains a decrease in overall gene conservation, as well as an unusual ratio of ligands to receptors and other modifiers. These findings suggest that gene loss and duplication among components of signal transduction pathways are common among arthropods and suggest that signal transduction pathways in arthropods are more evolutionarily labile than previously hypothesized.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alexandre C, Jacinto A, Ingham PW (1996) Transcriptional activation of hedgehog target genes in Drosophila is mediated directly by the cubitus interruptus protein, a member of the GLI family of zinc finger DNA-binding proteins. Genes Dev 10:2003–2013

    Article  CAS  PubMed  Google Scholar 

  • Alves G, Limbourg-Bouchon B, Tricoire H, Brissard-Zahraoui J, Lamour-Isnard C, Busson D (1998) Modulation of Hedgehog target gene expression by the Fused serine-threonine kinase in wing imaginal discs. Mech Develop 78:17–31

    Article  CAS  Google Scholar 

  • Aza-Blanc P, Ramírez-Weber FA, Laget MP, Schwartz C, Kornberg TB (1997) Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 89:1043–1053

    Article  CAS  PubMed  Google Scholar 

  • Bänziger C, Soldini D, Schütt C, Zipperlen P, Hausmann G, Basler K (2006) Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell 125:509–522

    Article  PubMed  Google Scholar 

  • Bartscherer K, Pelte N, Ingelfinger D, Boutros M (2006) Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell 125:523–533

    Article  CAS  PubMed  Google Scholar 

  • Behura SK, Haugen M, Flannery E, Sarro J, Tessier CR, Severson DW, Duman-Scheel M (2011) Comparative genomic analysis of Drosophila melanogaster and vector mosquito developmental genes. PLoS ONE 6:e21504

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bolognesi R, Farzana L, Fischer TD, Brown SJ (2008) Multiple Wnt genes are required for segmentation in the short-germ embryo of Tribolium castaneum. Curr Biol 18:1624–1629

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brody T (1999) The Interactive Fly: gene networks, development and the Internet. Trends Genet 15:333–334

    Article  CAS  PubMed  Google Scholar 

  • Brou C, Logeat F, Gupta N, Bessia C, LeBail O, Doedens JR, Cumano A, Roux P, Black RA, Israel A (2000) A novel proteolytic cleavage involved in Notch signaling—the role of the disintegrin-metalloprotease TACE. Mol Cell 5:10–10

    Article  Google Scholar 

  • Burke R, Nellen D, Bellotto M, Hafen E, Senti KA, Dickson BJ, Basler K (1999) Dispatched, a novel sterol-sensing domain protein dedicated to the release of cholesterol-modified hedgehog from signaling cells. Cell 99:803–815

    Article  CAS  PubMed  Google Scholar 

  • Carroll, S.B., Grenier, J.K., and Weatherbee, S.D. (2005). From DNA to diversity: molecular genetics and the evolution of animal design. Blackwell, London

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Chesebro JE, Pueyo JI, Couso JP (2013) Interplay between a Wnt-dependent organiser and the Notch segmentation clock regulates posterior development in Periplaneta americana. Biology Open 2:227–237

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ching W, Hang HC, Nusse R (2008) Lipid-independent secretion of a Drosophila Wnt protein. J Biol Chem 283:17092–17098

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chipman AD, Akam M (2008) The segmentation cascade in the centipede Strigamia maritima: involvement of the Notch pathway and pair-rule gene homologues. Dev Biol 319:160–169

    Article  CAS  PubMed  Google Scholar 

  • Cohen B, Simcox AA, Cohen SM (1993) Allocation of the thoracic imaginal primordia in the Drosophila embryo. Development 117:597–608

    CAS  PubMed  Google Scholar 

  • Darnell JE Jr (1997) STATs and gene regulation. Science 277:1630–1635

    Article  CAS  PubMed  Google Scholar 

  • Dearden PK, Duncan EJ (2010) Evolution of a genomic regulatory domain: the role of gene co-option and gene duplication in the Enhancer of split complex. Genome Res 20:917–928

    Article  PubMed Central  PubMed  Google Scholar 

  • Dearden PK, Grbić M, Donly C (2003) Vasa expression and germ-cell specification in the spider mite Tetranychus urticae. Dev Genes Evol 212:599–603

    CAS  PubMed  Google Scholar 

  • Dearden PK, Wilson MJ, Sablan L, Osborne PW, Havler M, McNaughton E, Kimura K, Milshina NV, Hasselmann M, Gempe T et al (2006) Patterns of conservation and change in honey bee developmental genes. Genome Res 16:1376–1384

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dequeant ML, Glynn E, Gaudenz K, Wahl M, Chen J, Mushegian A, Pourquie O (2006) A complex oscillating network of signaling genes underlies the mouse segmentation clock. Science 314:1595–1598

    Article  CAS  PubMed  Google Scholar 

  • Farzana L, Brown SJ (2008) Hedgehog signaling pathway function conserved in Tribolium segmentation. Dev Genes Evol 218:181–192

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • García-Bellido A, de Celis JF (2009) The complex tale of the achaete-scute complex: a paradigmatic case in the analysis of gene organization and function during development. Genetics 182:631–639

    Article  PubMed Central  PubMed  Google Scholar 

  • Gazave E, Lapébie P, Richards GS, Brunet F, Ereskovsky AV, Degnan BM, Borchiellini C, Vervoort M, Renard E (2009) Origin and evolution of the Notch signalling pathway: an overview from eukaryotic genomes. BMC Evol Biol 9:249

    Article  PubMed Central  PubMed  Google Scholar 

  • Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, Osborne EJ, Dermauw W, Ngoc PCT, Ortego F et al (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479:487–492

    Article  PubMed  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biol 59:307–321

    Article  CAS  Google Scholar 

  • Herr P, Basler K (2012) Developmental biology. Dev Biol 361:392–402

    Article  CAS  PubMed  Google Scholar 

  • Holley SA, Neul JL, Attisano L, Wrana JL, Sasai Y, O'Connor MB, De Robertis EM, Ferguson EL (1996) The Xenopus dorsalizing factor noggin ventralizes Drosophila embryos by preventing DPP from activating its receptor. Cell 86:11–11

    Article  Google Scholar 

  • Janssen R, Brown SJ, Le Gouar M, Pechmann M, Poulin F, Bolognesi R, Schwager EE, Hopfen C, Colbourne JK, Budd GE et al (2010) Conservation, loss, and redeployment of Wnt ligands in protostomes: implications for understanding the evolution of segment formation. BMC Evol Biol 10:374

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kanehisa M, Goto S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28:27–30

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Khila A, Grbić M (2007) Gene silencing in the spider mite Tetranychus urticae: dsRNA and siRNA parental silencing of the Distal-less gene. Dev Genes Evol 217:241–251

    Article  CAS  PubMed  Google Scholar 

  • Kraft R, Jäckle H (1994) Drosophila mode of metamerization in the embryogenesis of the lepidopteran insect Manduca sexta. Pnas 91(14):6634–6638

  • Krämer H, Cagan RL, Zipursky SL (1991) Interaction of bride of Sevenless membrane-bound ligand and the Sevenless tyrosine-kinase receptor. Nature 352:207–212

    Article  PubMed  Google Scholar 

  • Lieber T (2002) kuzbanian-mediated cleavage of Drosophila Notch. Genes Dev 16:209–221

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maier D (2006) Hairless: the ignored antagonist of the Notch signalling pathway. Hereditas 143:212–221

    Article  PubMed  Google Scholar 

  • Massagué J, Chen Y-G (2000) Controlling TGF-β signaling. Genes Dev 14:627–644

    PubMed  Google Scholar 

  • Mathies LD, Kerridge S, Scott MP (1994) Role of the teashirt gene in Drosophila midgut morphogenesis: secreted proteins mediate the action of homeotic genes. Development 120:2799–2809

    CAS  PubMed  Google Scholar 

  • McGregor AP, Pechmann M, Schwager EE, Feitosa NM, Kruck S, Aranda M, Damen WGM (2008) Wnt8 is required for growth-zone establishment and development of opisthosomal segments in a spider. Curr Biol 18:1619–1623

    Article  CAS  PubMed  Google Scholar 

  • Miyawaki K, Mito T, Sarashina I, Zhang H, 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 Develop 121:119–130

    Article  CAS  Google Scholar 

  • Mumm JS, Schroeter EH, Saxena MT, Griesemer A, Tian X, Pan DJ, Ray WJ, Kopan R (2000) A ligand-induced extracellular cleavage regulates gamma-secretase-like proteolytic activation of Notch1. Mol Cell 5:197–206

    Article  CAS  PubMed  Google Scholar 

  • Nagy LM, Carroll S (1994) Conservation of wingless patterning functions in the short-germ embryos of Tribolium castaneum. Nature 367(6462):460–463

  • Nüsslein-Volhard C, Wieschaus E, Kluding H (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. 1. Zygotic loci on the 2nd chromosome. Wilhelm Rouxs Arch Dev Biol 193:267–282

    Article  Google Scholar 

  • Ober KA, Jockusch EL (2006) The roles of wingless and decapentaplegic in axis and appendage development in the red flour beetle, Tribolium castaneum. Dev Biol 294:391–405

    Article  CAS  PubMed  Google Scholar 

  • Palmeirim I, Henrique D, Ish-Horowicz D, Pourquie O (1997) Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91:639–648

    Article  CAS  PubMed  Google Scholar 

  • Pan DJ, Rubin GM (1997) Kuzbanian controls proteolytic processing of Notch and mediates lateral inhibition during Drosophila and vertebrate neurogenesis. Cell 90:271–280

    Article  CAS  PubMed  Google Scholar 

  • Pires-daSilva A, Sommer RJ (2003) The evolution of signalling pathways in animal development. Nat Rev Genet 4:39–49

    Article  CAS  PubMed  Google Scholar 

  • Pisani D, Poling LL, Lyons-Weiler M, Hedges S (2004) The colonization of land by animals: molecular phylogeny and divergence times among arthropods. BMC Biol 2:1. doi:10.1186/1741-7007-2-1

  • Pueyo JI, Lanfear R, Couso JP (2008) Ancestral Notch-mediated segmentation revealed in the cockroach Periplaneta americana. Proc Natl Acad Sci 105:16614–16619

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rawlings JS, Rosler KM, Harrison DA (2004) The JAK/STAT signaling pathway. J Cell Sci 117:1281–1283

    Article  CAS  PubMed  Google Scholar 

  • Rooke J, Pan D, Xu T, Rubin GM (1996) KUZ, a conserved metalloprotease-disintegrin protein with two roles in Drosophila neurogenesis. Science 273:1227–1231

    Article  CAS  PubMed  Google Scholar 

  • Schlatter R, Maier D (2005) The Enhancer of split and Achaete-Scute complexes of Drosophilids derived from simple ur-complexes preserved in mosquito and honeybee. BMC Evol Biol 5:67

    Article  PubMed Central  PubMed  Google Scholar 

  • Schoppmeier M, Damen WGM (2005) Suppressor of Hairless and Presenilin phenotypes imply involvement of canonical Notch-signalling in segmentation of the spider Cupiennius salei. Dev Biol 280:211–224

    Article  CAS  PubMed  Google Scholar 

  • Shigenobu S, Dearden PK, Bickel RD, Brisson JA, Butts T, Chang C-C, Christiaens O, Davis GK, Duncan EJ, Ferrier DEK 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(Suppl 2):47–62

    Article  CAS  PubMed  Google Scholar 

  • Simcox AA, Roberts IJ, Hersperger E, Gribbin MC, Shearn A, Whittle JR (1989) Imaginal discs can be recovered from cultured embryos mutant for the segment-polarity genes engrailed, naked and patched but not from wingless. Development 107:715–722

    CAS  PubMed  Google Scholar 

  • Sisson JC, Ho KS, Suyama K, Scott MP (1997) Costal2, a novel kinesin-related protein in the Hedgehog signaling pathway. Cell 90:235–245

    Article  CAS  PubMed  Google Scholar 

  • St Pierre SE, Ponting L, Stefancsik R, McQuilton P, FlyBase Consortium (2014) FlyBase 102–advanced approaches to interrogating FlyBase. Nucleic Acids Res 42:D780–D788

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sterck L, Billiau K, Abeel T, Rouze P, Van de Peer Y (2012) ORCAE: online resource for community annotation of eukaryotes. Nat Meth 9:1041–1041

    Article  CAS  Google Scholar 

  • Stollewerk A, Schoppmeier M, Damen WGM (2003) Involvement of Notch and Delta genes in spider segmentation. Nature 423:863–865

    Article  CAS  PubMed  Google Scholar 

  • Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biol 56:564–577

    Article  CAS  Google Scholar 

  • Van der Zee M, Fonseca RN, Roth S (2008) TGFβ signaling in Tribolium: vertebrate-like components in a beetle. Dev Genes Evol 218:203–213

    Article  PubMed  Google Scholar 

  • Wilkins AS (2002) The evolution of developmental pathways. Sinauer, MA

  • Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T, Yates JR, Nusse R (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423:448–452

    Article  CAS  PubMed  Google Scholar 

  • Zeidler MP, Bach EA, Perrimon N (2000) The roles of the Drosophila JAK/STAT pathway. Oncogene 19:2598–2606

    Article  CAS  PubMed  Google Scholar 

  • Zhai L (2004) Drosophila Wnt-1 undergoes a hydrophobic modification and is targeted to lipid rafts, a process that requires porcupine. J Biol Chem 279:33220–33227

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Matt Stansbury and two anonymous reviewers for careful reading and helpful comments on earlier drafts. This research was carried out while R.M.P. and P.C.E was supported through NSF-IGERT grant DGE-0114420. R.M.P. was also supported through NIH Training Grant T32GM008659.

Author contributions

R.M.P. designed the study, performed the data analyses, and wrote the first draft manuscript. M.G. and L.M.N. participated in study design and data discussion. L.M.N. and P.C.E contributed to data analyses and writing the final version of the manuscript. All authors approved the final version of the manuscript.

Conflict of interest

The authors declare that there are no conflicts of interest in this report.

Author information

Authors and Affiliations

  1. Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ, 85721, USA

    Ryan M. Pace & Lisa M. Nagy

  2. Department of Biology, University of Western Ontario, London, Ontario, N6A 5B7, Canada

    Miodrag Grbić

  3. Instituto de Ciencias de la Vid y del Vino CSIC, Universidad de la Rioja, Logroño, 26006, Spain

    Miodrag Grbić

  4. Graduate Interdisciplinary Program in Entomology and Insect Science, University of Arizona, Tucson, AZ, 85721, USA

    P. Cole Eskridge

Authors
  1. Ryan M. Pace
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Cole Eskridge
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Miodrag Grbić
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lisa M. Nagy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lisa M. Nagy.

Additional information

Communicated by: Siegfried Roth

Electronic supplementary material

Below is the link to the electronic supplementary material.

Figure S1

Maximum likelihood tree of Enhancer of Split (E(spl)-C) complex basic helix-loop-helix genes. (JPEG 28 kb)

Table S1

Tetranychus survey results containing gene name, accession, BLAST scores, and reciprocal BLAST scores. (XLSX 141 kb)

Table S2

List of 62 genes found to overlap within Tetranychus, Apis, and Acyrthosiphon surveys. (XLSX 10.6 kb)

Table S3

Genes surveyed in Ixodes that are absent in Tetranychus. (XLSX 58 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pace, R.M., Eskridge, P.C., Grbić, M. et al. Evidence for the plasticity of arthropod signal transduction pathways. Dev Genes Evol 224, 209–222 (2014). https://doi.org/10.1007/s00427-014-0479-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-014-0479-7

Keywords

Search

Navigation