Novel function of Distal-less as a gap gene during spider segmentation

PLoS Genetics

Volumn 7, Issue 10, 2011, Pages

  Pechmann, Matthias ^a   Khadjeh, Sara ^a   Turetzek, Natascha ^a   McGregor, Alistair P ^b,c   Damen, Wim G M ^d   Prpic, Nikola Michael ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^c OXFORD BROOKES UNIVERSITY   (United Kingdom)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACHAEARANEA TEPIDARIORUM; ARACHNID; ARTICLE; CELL DEATH; CONSERVATION GENETICS; CONTROLLED STUDY; DISTAL LESS GENE; DROSOPHILA MELANOGASTER; EMBRYO; EMBRYO SEGMENTATION; ENGRAILED GENE; EVOLUTIONARY HOMOLOGY; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HEDGEHOG GENE; HOMEOBOX; IN SITU HYBRIDIZATION; INSECT DEVELOPMENT; LIMB BUD; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; RNA INTERFERENCE; SPECIES DIFFERENCE; STRUCTURAL HOMOLOGY; ANIMAL; CELL POLARITY; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; LIMB; MORPHOGENESIS; PHYSIOLOGY; SPIDER;

ACHAEARANEA TEPIDARIORUM; ARANEAE; ARTHROPODA; CRUSTACEA; ERINACEIDAE; HEXAPODA; METAZOA; PHOLCUS PHALANGIOIDES;

DISTAL LESS PROTEIN, INSECT; DISTAL-LESS PROTEIN, INSECT; HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR;

ANIMALS; BIOLOGICAL EVOLUTION; BODY PATTERNING; CELL POLARITY; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; PHENOTYPE; RNA INTERFERENCE; SPIDERS; TRANSCRIPTION FACTORS;

EID: 80055066823     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002342     Document Type: Article

References (51)

1. Cohen SM, Jürgens G, (1991) Drosophila headlines. Trends Genet 7: 267-272.
2. Jürgens G, Hartenstein V, (1993) The terminal regions of the body pattern. In: Bate M, Martinez Arias A, editors. The Development of Drosophila melanogaster Cold Spring Harbor Cold Spring Harbor Laboratory Press pp. 687-746.
3. Rosenberg MI, Lynch JA, Desplan C, (2009) Heads and tails: Evolution of antero-posterior patterning in insects. Biochim Biophys Acta 1789: 333-342.
4. Damen WGM, Hausdorf M, Seyfarth EA, Tautz D, (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. Telford MJ, Thomas RH, (1998) Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc Natl Acad Sci USA 95: 10671-10675.
6. Liu PZ, Kaufman TC, (2005) Short and long germ segmentation: unanswered questions in the evolution of a developmental mode. Evol Dev 7: 629-646.
7. Cohen SM, Jürgens G, (1990) Mediation of Drosophila head development by gap-like segmentation genes. Nature 346: 482-485.
8. Finkelstein R, Perrimon N, (1990) The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature 346: 485-488.
9. Driever W, (1993) Maternal control of anterior development in the Drosophila embryo. In: Bate M, Martinez Arias A, editors. The Development of Drosophila melanogaster Cold Spring Harbor Cold Spring Harbor Laboratory Press pp. 301-324.
10. Pechmann M, McGregor AP, Schwager EE, Feitosa NM, Damen WGM, (2009) Dynamic gene expression is required for anterior regionalization in a spider. Proc Natl Acad Sci USA 106: 1468-1472.
11. Vincent A, Blankenship JT, Wieschaus E, (1997) Integration of the head and trunk segmentation systems controls cephalic furrow formation in Drosophila. Development 124: 3747-3754.
12. Pankratz MJ, Jäckle H, (1993) Blastoderm segmentation. In: Bate M, Martinez Arias A, editors. The Development of Drosophila melanogaster Cold Spring Harbor Cold Spring Harbor Laboratory Press pp. 467-516.
13. Crozatier M, Valle D, Dubois L, Ibnsouda S, Vincent A, (1999) Head versus trunk patterning in the Drosophila embryo; collier requirement for formation of the intercalary segment. Development 126: 4385-4394.
14. Schwager EE, Pechmann M, Feitosa NM, McGregor AP, Damen WGM, (2009) hunchback functions as a segmentation gene in the spider Achaearanea tepidariorum. Curr Biol 19: 1333-1340.
15. Akiyama-Oda Y, Oda H, (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. Schaeper ND, Pechmann M, Damen WGM, Prpic NM, Wimmer EA, (2010) Evolutionary plasticity of collier function in head development of diverse arthropods. Dev Biol 344: 363-376.
17. Scholtz G, Mittmann B, Gerberding M, (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. Popadic A, Panganiban G, Rusch D, Shear WA, Kaufman TC, (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. Panganiban G, Nagy L, Carroll SB, (1994) The role of the Distal-less gene in the development and evolution of insect limbs. Curr Biol 4: 671-675.
20. Popadic A, Rusch D, Peterson M, Rogers BT, Kaufman TC, (1996) Origin of the arthropod mandible. Nature 380: 395.
21. Akiyama-Oda Y, Oda H, (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. Oda H, Akiyama-Oda Y, (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. Barth FG, Libera W, (1970) Ein Atlas der Spaltsinnesorgane von Cupiennius salei Keys. Chelicerata (Araneae). Z Morph Tiere 68: 343-369.
24. Mohler J, (1995) Spatial regulation of segment polarity gene expression in the anterior terminal region of the Drosophila blastoderm embryo. Mech Dev 50: 151-161.
25. Yamazaki K, Akiyama-Oda Y, Oda H, (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. McGregor AP, (2005) How to get ahead: the origin, evolution and function of bicoid. BioEssays 27: 904-913.
27. McGregor AP, Hilbrant M, Pechmann M, Schwager EE, Prpic NM, Damen WGM, (2008) Cupiennius salei and Achaearanea tepidariorum: spider models for investigating evolution and development. BioEssays 30: 487-498.
28. Simpson-Brose M, Treisman J, Desplan C, (1994) Synergy between the hunchback and bicoid morphogens is required for anterior patterning in Drosophila. Cell 78: 855-865.
29. Wimmer EA, Simpson-Brose M, Cohen SM, Desplan C, Jäckle H, (1995) Trans- and cis-acting requirements for blastodermal expression of the head gap gene buttonhead. Mech Dev 53: 235-245.
30. Lemke S, Busch SE, Antonopoulos DA, Meyer F, Domanus MH, et al. (2010) Maternal activation of gap genes in the hover fly Episyrphus. Development 137: 1709-1719.
31. Schoppmeier M, Fischer S, Schmitt-Engel C, Löhr U, Klingler M, (2009) An ancient anterior patterning system promotes caudal repression and head formation in ecdysozoa. Curr Biol 19: 1811-1815.
32. Schinko JB, Kreuzer N, Offen N, Posnien N, Wimmer EA, et al. (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. Slack JM, Holland PW, Graham CF, (1993) The zootype and the phylotypic stage. Nature 361: 490-492.
34. Tautz D, Schmid KJ, (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. Kalinka AT, Varga KM, Gerrard DT, Preibisch S, Corcoran DL, et al. (2010) Gene expression divergence recapitulates the developmental hourglass model. Nature 468: 811-814.
36. Domazet-Loso T, Tautz D, (2010) A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468: 815-818.
37. Panganiban G, Sebring A, Nagy L, Carroll S, (1995) The development of crustacean limbs and the evolution of arthropods. Science 270: 1363-1366.
38. Schoppmeier M, Damen WGM, (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. Khila A, Grbic M, (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. Lee SE, Jacobs DK, (1999) Expression of Distal-less in molluscan eggs, embryos, and larvae. Evol Dev 1: 172-179.
41. Lowe CJ, Wu M, Salic A, Evans L, Lander E, et al. (2003) Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113: 853-865.
42. Ryan JF, Mazza ME, Pang K, Matus DQ, Baxevanis AD, et al. (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. Lemons D, Fritzenwanker JH, Gerhart J, Lowe CJ, McGinnis W, (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. Pechmann M, Prpic NM, (2009) Appendage patterning in the South American bird spider Acanthoscurria geniculata (Araneae: Mygalomorphae). Dev Genes Evol 219: 189-198.
45. Prpic NM, Schoppmeier M, Damen WGM, (2008) Collection and fixation of spider embryos. CSH Protocols 3: 930-932 doi:10.1101/pdb.prot5067.
46. Prpic NM, Tautz D, (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-Oda Y, Oda H, (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. Prpic NM, Schoppmeier M, Damen WGM, (2008) Whole-mount in situ hybridization of spider embryos. CSH Protocols 3: 933-936 doi:10.1101/pdb.prot5068.
49. Prpic NM, Damen WGM, (2005) Cell death during germ band inversion, dorsal closure and nervous system development in the spider Cupiennius salei. Dev Dyn 234: 222-228.
50. Abzhanov A, Kaufman TC, (2000) Homologs of Drosophila appendage genes in the patterning of arthropod limbs. Dev Biol 227: 673-89.
51. Coddington JA, Levi HW, (1991) Systematics and evolution of spiders (Araneae). Ann Rev Ecol Syst 22: 565-592.