期刊论文详细信息
EvoDevo
Analysis of the Wnt gene repertoire in an onychophoran provides new insights into the evolution of segmentation
Ralf Janssen2  Nico Posnien1  Alistair P McGregor3  Graham E Budd2  Anna Schönauer3  Mattias Hogvall2 
[1] Department of Developmental Biology, Georg-August-University Göttingen, Justus-von-Liebig-Weg 11, Göttingen, 37077, Germany;Department of Earth Sciences, Palaeobiology, Uppsala University, Villavägen 16, Uppsala, 75236, Sweden;Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, OX3 0BP, UK
关键词: Wnt signalling;    Segment polarity;    Segmentation;    Evolution;    Development;   
Others  :  801725
DOI  :  10.1186/2041-9139-5-14
 received in 2014-01-16, accepted in 2014-03-11,  发布年份 2014
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【 摘 要 】

Background

The Onychophora are a probable sister group to Arthropoda, one of the most intensively studied animal phyla from a developmental perspective. Pioneering work on the fruit fly Drosophila melanogaster and subsequent investigation of other arthropods has revealed important roles for Wnt genes during many developmental processes in these animals.

Results

We screened the embryonic transcriptome of the onychophoran Euperipatoides kanangrensis and found that at least 11 Wnt genes are expressed during embryogenesis. These genes represent 11 of the 13 known subfamilies of Wnt genes.

Conclusions

Many onychophoran Wnt genes are expressed in segment polarity gene-like patterns, suggesting a general role for these ligands during segment regionalization, as has been described in arthropods. During early stages of development, Wnt2, Wnt4, and Wnt5 are expressed in broad multiple segment-wide domains that are reminiscent of arthropod gap and Hox gene expression patterns, which suggests an early instructive role for Wnt genes during E. kanangrensis segmentation.

【 授权许可】

   
2014 Hogvall et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Oliveira Ide S, Read VM, Mayer G: A world checklist of Onychophora (velvet worms), with notes on nomenclature and status of names. Zookeys 2012, 211:1-70.
  • [2]Campbell LI, Rota-Stabelli O, Edgecombe GD, Marchioro T, Longhorn SJ, Telford MJ, Philippe H, Rebecchi L, Peterson KJ, Pisani D: MicroRNAs and phylogenomics resolve the relationships of Tardigrada and suggest that velvet worms are the sister group of Arthropoda. Proc Natl Acad Sci U S A 2011, 108:15920-15924.
  • [3]Tautz D: Segmentation. Dev Cell 2004, 7:301-312.
  • [4]Damen WG: Evolutionary conservation and divergence of the segmentation process in arthropods. Dev Dyn 2007, 236:1379-1391.
  • [5]Peel AD: The evolution of developmental gene networks: lessons from comparative studies on holometabolous insects. Philos Trans R Soc Lond B Biol Sci 2008, 363:1539-1547.
  • [6]Chipman AD: Parallel evolution of segmentation by co-option of ancestral gene regulatory networks. Bioessays 2010, 32:60-70.
  • [7]Andrioli LP: Toward new Drosophila paradigms. Genesis 2012, 50:585-598.
  • [8]Nüsslein-Volhard C, Wieschaus E: Mutations affecting segment number and polarity in Drosophila. Nature 1980, 287:795-801.
  • [9]Nüsslein-Volhard C, Kluding H, Jürgens G: Genes affecting the segmental subdivision of the Drosophila embryo. Cold Spring Harb Symp Quant Biol 1985, 50:145-154.
  • [10]Ahzhanov A, Kaufman TC: Evolution of distinct expression patterns for engrailed paralogues in higher crustaceans (Malacostraca). Dev Genes Evol 2000, 210:493-506.
  • [11]Hughes CL, Kaufman TC: Exploring myriapod segmentation: the expression patterns of even-skipped, engrailed, and wingless in a centipede. Dev Biol 2002, 247:47-61.
  • [12]Damen WG: Parasegmental organization of the spider embryo implies that the parasegment is an evolutionary conserved entity in arthropod embryogenesis. Development 2002, 129:1239-1250.
  • [13]Simonnet F, Deutsch J, Queinnec E: hedgehog is a segment polarity gene in a crustacean and a chelicerate. Dev Genes Evol 2004, 214:345-537.
  • [14]Janssen R, Prpic NM, Damen WG: Gene expression suggests decoupled dorsal and ventral segmentation in the millipede Glomeris marginata (Myriapoda: Diplopoda). Dev Biol 2004, 268:89-104.
  • [15]Farzana L, Brown SJ: Hedgehog signaling pathway function conserved in Tribolium segmentation. Dev Genes Evol 2008, 218:181-192.
  • [16]Janssen R: Segment polarity gene expression in a myriapod reveals conserved and diverged aspects of early head patterning in arthropods. Dev Genes Evol 2012, 222:299-309.
  • [17]Eriksson BJ, Tait NN, Budd GE, Akam M: The involvement of engrailed and wingless during segmentation in the onychophoran Euperipatoides kanangrensis (Peripatopsidae: Onychophora) (Reid 1996). Dev Genes Evol 2009, 219:249-264.
  • [18]Janssen R, Budd GE: Deciphering the onychophoran ‘segmentation gene cascade’: gene expression reveals limited involvement of pair rule gene orthologs in segmentation, but a highly conserved segment polarity gene network. Dev Biol 2013, 382:224-234.
  • [19]Cho SJ, Valles Y, Giani VC Jr, Seaver EC, Weisblat DA: Evolutionary dynamics of the Wnt gene family: a lophotrochozoan perspective. Mol Biol Evol 2010, 27:1645-1658.
  • [20]Janssen R, Eriksson BJ, Budd GE, Akam M, Prpic NM: Gene expression patterns in an onychophoran reveal that regionalization predates limb segmentation in pan-arthropods. Evol Dev 2010, 12:363-372.
  • [21]Janssen R, Le Gouar M, Pechmann M, Poulin F, Bolognesi R, Schwager EE, Hopfen C, Colbourne JK, Budd GE, Brown SJ, Prpic NM, Kosiol C, Vervoort M, Damen WG, Balavoine G, McGregor AP: Conservation, loss, and redeployment of Wnt ligands in protostomes: implications for understanding the evolution of segment formation. BMC Evol Biol 2010, 10:374. BioMed Central Full Text
  • [22]Notredame C, Higgins DG, Heringa J: T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 2000, 302:205-217.
  • [23]Gouy M, Guindon S, Gascuel O: SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010, 27:221-224.
  • [24]Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
  • [25]Eriksson BJ, Tait NN, Budd GE, Janssen R, Akam M: Head patterning and Hox gene expression in an onychophoran and its implications for the arthropod head problem. Dev Genes Evol 2010, 220:117-122.
  • [26]Janssen R, Eriksson BJ, Tait NN, Budd GE: Onychophoran Hox genes and the evolution of arthropod Hox gene expression. Front Zool 2014, 11:22. BioMed Central Full Text
  • [27]Janssen R, Damen WG: The ten Hox genes of the millipede Glomeris marginata. Dev Genes Evol 2006, 216:451-465.
  • [28]Sharma PP, Schwager EE, Extavour CG, Giribet G: Hox gene expression in the harvestman Phalangium opilio reveals divergent patterning of the chelicerate opisthosoma. Evol Dev 2012, 14:450-463.
  • [29]Hughes CL, Kaufman TC: Hox genes and the evolution of the arthropod body plan. Evol Dev 2002, 4:459-499.
  • [30]Jaeger J: The gap gene network. Cell Mol Life Sci 2011, 68:243-274.
  • [31]Eriksson BJ, Tait NN: Early development in the velvet worm Euperipatoides kanangrensis Reid 1996 (Onychophora: Peripatopsidae). Arthropod Struct Dev 2012, 41:483-493.
  • [32]Klingensmith J, Nusse R: Signaling by wingless in Drosophila. Dev Biol 1994, 166:396-414.
  • [33]Sanson B: Generating patterns from fields of cells. EMBO Rep 2001, 2:1083-1088.
  • [34]Gonsalves FC, DasGupta R: Function of the wingless signaling pathway in Drosophila. Methods Mol Biol 2008, 469:115-125.
  • [35]Baker NB: Molecular cloning of sequences from wingless, a segment polarity gene in Drosophila: the spatial distribution of a transcript in embryos. EMBO J 1987, 6:1765-1773.
  • [36]Ingham P, Baker N, Martinez Arias A: Positive and negative regulation of segment polarity genes in the Drosophila blastoderm by the pair rule genes fushi tarazu and even skipped. Nature 1988, 331:73-75.
  • [37]Miyawaki K, Mito T, Sarashina I, Zhang H, Shinmyo Y, Ohuchi H, Noji S: Involvement of Wingless/Armadillo signaling in the posterior sequential segmentation in the cricket, Gryllus bimaculatus (Orthoptera), as revealed by RNAi analysis. Mech Dev 2004, 121:119-130.
  • [38]Angelini DR, Kaufman TC: Functional analyses in the milkweed bug Oncopeltus fasciatus (Hemiptera) support a role for Wnt signaling in body segmentation but not appendage development. Dev Biol 2005, 283:409-423.
  • [39]Bolognesi R, Farzana L, Fischer TD, Brown SJ: Multiple Wnt genes are required for segmentation in the short-germ embryo of Tribolium castaneum. Curr Biol 2008, 18:1624-1629.
  • [40]Bolognesi R, Fischer TD, Brown SJ: Loss of Tc-arrow and canonical Wnt signaling alters posterior morphology and pair-rule gene expression in the short-germ insect, Tribolium castaneum. Dev Genes Evol 2009, 219:369-375.
  • [41]Beermann A, Prühs R, Lutz R, Schröder R: A context-dependent combination of Wnt receptors controls axis elongation and leg development in a short germ insect. Development 2011, 38:2793-2805.
  • [42]McGregor AP, Pechmann M, Schwager EE, Feitosa NM, Kruck S, Aranda M, Damen WG: Wnt8 is required for growth-zone establishment and development of opisthosomal segments in a spider. Curr Biol 2008, 18:1619-1623.
  • [43]McGregor AP, Pechmann M, Schwager EE, Damen WG: An ancestral regulatory network for posterior development in arthropods. Commun Integr Biol 2009, 2:174-176.
  • [44]Chesebro JE, Pueyo JI, Couso JP: Interplay between a Wnt-dependent organizer and the Notch segmentation clock regulates posterior development in Periplaneta americana. Biol Open 2013, 2:227-237.
  • [45]Murat S, Hopfen C, McGregor AP: The function and evolution of Wnt genes in arthropods. Arthropod Struct Dev 2010, 39:446-452.
  • [46]Bejsovec A: Wingless/Wnt signaling in Drosophila: the pattern and the pathway. Mol Reprod Dev 2013, 80:882-894.
  • [47]Ober KA, Jockusch EL: The roles of wingless and decapentaplegic in axis and appendage development in the red flour beetle, Tribolium castaneum. Dev Biol 2006, 294:391-405.
  • [48]Janssen R, Posnien N: Identification and embryonic expression of Wnt2, Wnt4, Wnt5 and Wnt9 orthologs in the millipede Glomeris marginata (Myriapoda: Diplopoda). Gene Expr Patterns 2014, 14:55-61.
  • [49]Hayden L, Arthur W: The centipede Strigamia maritima possesses a large complement of Wnt genes with diverse expression patterns. Evol Dev
  • [50]Russell J, Gennissen A, Nusse R: Isolation and expression of two novel Wnt/ wingless gene homologues in Drosophila. Development 1992, 115:475-485.
  • [51]Fradkin LG, Noordermeer JN, Nusse R: The Drosophila Wnt protein DWnt-3 is a secreted glycoprotein localized on the axon tracts of the embryonic CNS. Dev Biol 1995, 168:202-213.
  • [52]Bolognesi R, Beermann A, Farzana L, Wittkopp N, Lutz R, Balavoine G, Brown SJ, Schroeder R: Tribolium Wnts: evidence for a larger repertoire in insects with overlapping expression patterns that suggest multiple redundant functions in embryogenesis. Dev Genes Evol 2008, 218:193-202.
  • [53]Janssen R, Damen WG: Diverged and conserved aspects of heart formation in a spider. Evol Dev 2008, 10:155-165.
  • [54]Janson K, Cohen ED, Wilder EL: Expression of DWnt6, DWnt10, and DFz4 during Drosophila development. Mech Dev 2001, 103:117-120.
  • [55]Llimargas M, Lawrence PA: Seven Wnt homologues in Drosophila: a case study of the developing tracheae. Proc Natl Acad Sci U S A 2001, 98:14487-14492.
  • [56]Hayden L, Arthur W: Expression patterns of Wnt genes in the venom claws of centipedes. Evol Dev 2013, 15:365-372.
  • [57]Ganguly A, Jiang J, Ip YT: Drosophila WntD is a target and an inhibitor of the Dorsal/Twist/Snail network in the gastrulating embryo. Development 2005, 132:3419-3429.
  • [58]Gordon MD, Dionne MS, Schneider DS, Nusse R: WntD is a feedback inhibitor of Dorsal/NF-κB in Drosophila development and immunity. Nature 2005, 437:746-749.
  • [59]Graba Y, Gieseler K, Aragnol D, Laurenti P, Mariol MC, Berenger H, Sagnier T, Pradel J: DWnt-4, a novel Drosophila Wnt gene acts downstream of homeotic complex genes in the visceral mesoderm. Development 1995, 121:209-218.
  • [60]Budd GE: Tardigrades as ‘stem-group arthropods’: the evidence from the Cambrian fauna. Zool Anz 2001, 240:265-279.
  • [61]van den Heuvel M, Klingensmith J, Perrimon N, Nusse R: Cell patterning in the Drosophila segment: engrailed and wingless antigen distributions in segment polarity mutant embryos. Dev Suppl 1993, 105-114.
  • [62]Janssen R, Budd GE, Damen WG, Prpic NM: Evidence for Wg-independent tergite boundary formation in the millipede Glomeris marginata. Dev Genes Evol 2008, 218:361-370.
  • [63]Larsen CW, Hirst E, Alexandre C, Vincent JP: Segment boundary formation in Drosophila embryos. Development 2003, 130:5625-5635.
  • [64]Tabata T, Eaton S, Kornberg TB: The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Dev 1992, 6:2635-2645.
  • [65]Prpic NM, Tautz D: The expression of the proximodistal axis patterning genes Distal-less and dachshund in the appendages of Glomeris marginata (Myriapoda: Diplopoda) suggests a special role of these genes in patterning the head appendages. Dev Biol 2003, 260:97-112.
  • [66]Prpic NM: Homologs of wingless and decapentaplegic display a complex and dynamic expression profile during appendage development in the millipede Glomeris marginata (Myriapoda: Diplopoda). Front Zool 2004, 1:6. BioMed Central Full Text
  • [67]Prpic NM, Janssen R, Damen WG, Tautz D: Evolution of dorsal-ventral axis formation in arthropod appendages: H15 and optomotor-blind/bifid-type T-box genes in the millipede Glomeris marginata (Myriapoda: Diplopoda). Evol Dev 2005, 7:51-57.
  • [68]Janssen R, Feitosa NM, Damen WG, Prpic NM: The T-box genes H15 and optomotor-blind in the spiders Cupiennius salei, Tegenaria atrica and Achaearanea tepidariorum and the dorsoventral axis of arthropod appendages. Evol Dev 2008, 10:143-154.
  • [69]Svendsen PC, Formaz-Preston A, Leal SM, Brook WJ: The Tbx20 homologs midline and H15 specify ventral fate in the Drosophila melanogaster leg. Development 2009, 136:2689-2693.
  • [70]Grossmann D, Scholten J, Prpic NM: Separable functions of wingless in distal and ventral patterning of the Tribolium leg. Dev Genes Evol 2009, 219:469-479.
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