Novel Function of as a Gap Gene during Spider Segmentation
Despite many aspects of the regulation of segmentation being conserved among arthropods, the evolution of novel gene functions has played an important role in the evolution of developmental regulation and the emergence of new segmental structures. Moreover the study of such novel gene functions can be informative with respect to the patterns and direction of evolutionary changes in developmental programs. The homeobox gene Distal-less (Dll) is known for its conserved function in appendage development in metazoans. In arthropods, Dll is required for the specification of distal appendage structures. Here we describe a novel and unexpected role of Dll in the spider Achaearanea tepidariorum. We detect At-Dll transcripts not only in the appendages, but unexpectedly also in an anterior domain during early development, prior to the specification of the limb primordia. A similar early Dll domain is present in the distantly related spider Pholcus phalangioides. In A. tepidariorum this early At-Dll expression is required for head segmentation. RNA interference results in spiders that lack either the first or the first and the second walking leg segments. The early At-Dll expression is also required for the activation of the segment polarity genes engrailed and hedgehog in this region. Our work identifies the Distal-less gene as a novel factor in anterior spider segmentation with a gap gene-like function. This novel role of Dll is interesting because Dll expression is reduced in this region in crustaceans and the homologous insect segment, the mandible segment, does not express Dll and does not require this gene for patterning. We therefore discuss the possible implications of our results for understanding the evolution and diversification of the mandible segment.
Vyšlo v časopise:
Novel Function of as a Gap Gene during Spider Segmentation. PLoS Genet 7(10): e32767. doi:10.1371/journal.pgen.1002342
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002342
Souhrn
Despite many aspects of the regulation of segmentation being conserved among arthropods, the evolution of novel gene functions has played an important role in the evolution of developmental regulation and the emergence of new segmental structures. Moreover the study of such novel gene functions can be informative with respect to the patterns and direction of evolutionary changes in developmental programs. The homeobox gene Distal-less (Dll) is known for its conserved function in appendage development in metazoans. In arthropods, Dll is required for the specification of distal appendage structures. Here we describe a novel and unexpected role of Dll in the spider Achaearanea tepidariorum. We detect At-Dll transcripts not only in the appendages, but unexpectedly also in an anterior domain during early development, prior to the specification of the limb primordia. A similar early Dll domain is present in the distantly related spider Pholcus phalangioides. In A. tepidariorum this early At-Dll expression is required for head segmentation. RNA interference results in spiders that lack either the first or the first and the second walking leg segments. The early At-Dll expression is also required for the activation of the segment polarity genes engrailed and hedgehog in this region. Our work identifies the Distal-less gene as a novel factor in anterior spider segmentation with a gap gene-like function. This novel role of Dll is interesting because Dll expression is reduced in this region in crustaceans and the homologous insect segment, the mandible segment, does not express Dll and does not require this gene for patterning. We therefore discuss the possible implications of our results for understanding the evolution and diversification of the mandible segment.
Zdroje
1. CohenSMJürgensG 1991 Drosophila headlines. Trends Genet 7 267 272
2. JürgensGHartensteinV 1993 The terminal regions of the body pattern. BateMMartinez AriasA The Development of Drosophila melanogaster Cold Spring Harbor Cold Spring Harbor Laboratory Press 687 746
3. RosenbergMILynchJADesplanC 2009 Heads and tails: Evolution of antero-posterior patterning in insects. Biochim Biophys Acta 1789 333 342
4. DamenWGMHausdorfMSeyfarthEATautzD 1998 A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc Natl Acad Sci USA 95 10665 10670
5. TelfordMJThomasRH 1998 Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc Natl Acad Sci USA 95 10671 10675
6. LiuPZKaufmanTC 2005 Short and long germ segmentation: unanswered questions in the evolution of a developmental mode. Evol Dev 7 629 646
7. CohenSMJürgensG 1990 Mediation of Drosophila head development by gap-like segmentation genes. Nature 346 482 485
8. FinkelsteinRPerrimonN 1990 The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature 346 485 488
9. DrieverW 1993 Maternal control of anterior development in the Drosophila embryo. BateMMartinez AriasA The Development of Drosophila melanogaster Cold Spring Harbor Cold Spring Harbor Laboratory Press 301 324
10. PechmannMMcGregorAPSchwagerEEFeitosaNMDamenWGM 2009 Dynamic gene expression is required for anterior regionalization in a spider. Proc Natl Acad Sci USA 106 1468 1472
11. VincentABlankenshipJTWieschausE 1997 Integration of the head and trunk segmentation systems controls cephalic furrow formation in Drosophila. Development 124 3747 3754
12. PankratzMJJäckleH 1993 Blastoderm segmentation. BateMMartinez AriasA The Development of Drosophila melanogaster Cold Spring Harbor Cold Spring Harbor Laboratory Press 467 516
13. CrozatierMValleDDuboisLIbnsoudaSVincentA 1999 Head versus trunk patterning in the Drosophila embryo; collier requirement for formation of the intercalary segment. Development 126 4385 4394
14. SchwagerEEPechmannMFeitosaNMMcGregorAPDamenWGM 2009 hunchback functions as a segmentation gene in the spider Achaearanea tepidariorum. Curr Biol 19 1333 1340
15. Akiyama-OdaYOdaH 2010 Cell migration that orients the dorsoventral axis is coordinated with anteroposterior patterning mediated by Hedgehog signaling in the early spider embryo. Development 137 1263 1273
16. SchaeperNDPechmannMDamenWGMPrpicNMWimmerEA 2010 Evolutionary plasticity of collier function in head development of diverse arthropods. Dev Biol 344 363 376
17. ScholtzGMittmannBGerberdingM 1998 The pattern of Distal-less expression in the mouthparts of crustaceans, myriapods and insects: new evidence for a gnathobasic mandible and the common origin of Mandibulata. Int J Dev Biol 42 801 810
18. PopadicAPanganibanGRuschDShearWAKaufmanTC 1998 Molecular evidence for the gnathobasic derivation of arthropod mandibles and for the appendicular origin of the labrum and other structures. Dev Genes Evol 208 142 150
19. PanganibanGNagyLCarrollSB 1994 The role of the Distal-less gene in the development and evolution of insect limbs. Curr Biol 4 671 675
20. PopadicARuschDPetersonMRogersBTKaufmanTC 1996 Origin of the arthropod mandible. Nature 380 395
21. Akiyama-OdaYOdaH 2003 Early patterning of the spider embryo: a cluster of mesenchymal cells at the cumulus produces Dpp signals received by germ disc epithelial cells. Development 130 1735 1747
22. OdaHAkiyama-OdaY 2008 Differing strategies for forming the arthropod body plan: Lessons from Dpp, Sog and Delta in the fly Drosophila and spider Achaearanea. Develop Growth Differ 50 203 214
23. BarthFGLiberaW 1970 Ein Atlas der Spaltsinnesorgane von Cupiennius salei Keys. Chelicerata (Araneae). Z Morph Tiere 68 343 369
24. MohlerJ 1995 Spatial regulation of segment polarity gene expression in the anterior terminal region of the Drosophila blastoderm embryo. Mech Dev 50 151 161
25. YamazakiKAkiyama-OdaYOdaH 2005 Expression patterns of a twist-related gene in embryos of the spider Achaearanea tepidariorum reveal divergent aspects of mesoderm development in the fly and spider. Zoolog Sci 22 177 185
26. McGregorAP 2005 How to get ahead: the origin, evolution and function of bicoid. BioEssays 27 904 913
27. McGregorAPHilbrantMPechmannMSchwagerEEPrpicNMDamenWGM 2008 Cupiennius salei and Achaearanea tepidariorum: spider models for investigating evolution and development. BioEssays 30 487 498
28. Simpson-BroseMTreismanJDesplanC 1994 Synergy between the hunchback and bicoid morphogens is required for anterior patterning in Drosophila. Cell 78 855 865
29. WimmerEASimpson-BroseMCohenSMDesplanCJäckleH 1995 Trans- and cis-acting requirements for blastodermal expression of the head gap gene buttonhead. Mech Dev 53 235 245
30. LemkeSBuschSEAntonopoulosDAMeyerFDomanusMH 2010 Maternal activation of gap genes in the hover fly Episyrphus. Development 137 1709 1719
31. SchoppmeierMFischerSSchmitt-EngelCLöhrUKlinglerM 2009 An ancient anterior patterning system promotes caudal repression and head formation in ecdysozoa. Curr Biol 19 1811 1815
32. SchinkoJBKreuzerNOffenNPosnienNWimmerEA 2008 Divergent functions of orthodenticle, empty spiracles and buttonhead in early head patterning of the beetle Tribolium castaneum (Coleoptera). Dev Biol 317 600 613
33. SlackJMHollandPWGrahamCF 1993 The zootype and the phylotypic stage. Nature 361 490 492
34. TautzDSchmidKJ 1998 From genes to individuals: developmental genes and the generation of the phenotype. Philos Trans R Soc Lond B Biol Sci 353 231 240
35. KalinkaATVargaKMGerrardDTPreibischSCorcoranDL 2010 Gene expression divergence recapitulates the developmental hourglass model. Nature 468 811 814
36. Domazet-LosoTTautzD 2010 A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468 815 818
37. PanganibanGSebringANagyLCarrollS 1995 The development of crustacean limbs and the evolution of arthropods. Science 270 1363 1366
38. SchoppmeierMDamenWGM 2001 Double-stranded RNA interference in the spider Cupiennius salei: the role of Distal-less is evolutionarily conserved in arthropod appendage formation. Dev Genes Evol 211 76 82
39. KhilaAGrbicM 2007 Gene silencing in the spider mite Tetranychus urticae: ds RNA and siRNA parental silencing of the Distal-less gene. Dev Genes Evol 217 241 251
40. LeeSEJacobsDK 1999 Expression of Distal-less in molluscan eggs, embryos, and larvae. Evol Dev 1 172 179
41. LoweCJWuMSalicAEvansLLanderE 2003 Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113 853 865
42. RyanJFMazzaMEPangKMatusDQBaxevanisAD 2007 Pre-Bilaterian origins of the Hox cluster and the Hox code: evidence from the sea anemone, Nematostella vectensis. PLoS ONE 2 e153 doi:10.1371/journal.pone.0000153
43. LemonsDFritzenwankerJHGerhartJLoweCJMcGinnisW 2010 Co-option of an anteroposterior head axis patterning system for proximodistal patterning of appendages in early bilaterian evolution. Dev Biol 344 358 362
44. PechmannMPrpicNM 2009 Appendage patterning in the South American bird spider Acanthoscurria geniculata (Araneae: Mygalomorphae). Dev Genes Evol 219 189 198
45. PrpicNMSchoppmeierMDamenWGM 2008 Collection and fixation of spider embryos. CSH Protocols 3 930 932 doi:10.1101/pdb.prot5067
46. PrpicNMTautzD 2003 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 260 97 112
47. Akiyama-OdaYOdaH 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
48. PrpicNMSchoppmeierMDamenWGM 2008 Whole-mount in situ hybridization of spider embryos. CSH Protocols 3 933 936 doi:10.1101/pdb.prot5068
49. PrpicNMDamenWGM 2005 Cell death during germ band inversion, dorsal closure and nervous system development in the spider Cupiennius salei. Dev Dyn 234 222 228
50. AbzhanovAKaufmanTC 2000 Homologs of Drosophila appendage genes in the patterning of arthropod limbs. Dev Biol 227 673 89
51. CoddingtonJALeviHW 1991 Systematics and evolution of spiders (Araneae). Ann Rev Ecol Syst 22 565 592
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 10
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- The Glycobiome Reveals Mechanisms of Pentose and Hexose Co-Utilization in Bacteria
- Global Mapping of Cell Type–Specific Open Chromatin by FAIRE-seq Reveals the Regulatory Role of the NFI Family in Adipocyte Differentiation
- Genetic Determinants of Serum Testosterone Concentrations in Men
- MicroRNA Expression and Regulation in Human, Chimpanzee, and Macaque Brains