Evolutionary flexibility of pair-rule patterning revealed by functional analysis of secondary pair-rule genes, paired and sloppy-paired in the short-germ insect, Tribolium castaneum

Developmental Biology

Volumn 302, Issue 1, 2007, Pages 281-294

  Choe, Chong Pyo ^a   Brown, Susan J ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

Pair rule gene; paired; Segmentation; sloppy paired; Tribolium castaneum

Indexed keywords

ARTICLE; DROSOPHILA; EMBRYO PATTERN FORMATION; EMBRYO SEGMENTATION; ENGRAILED GENE; EVEN SKIPPED GENE; GENE; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENETIC CONSERVATION; INSECT; INSECT GENETICS; MOLECULAR EVOLUTION; NONHUMAN; ODD SKIPPED GENE; PAIRED GENE; PRIORITY JOURNAL; RUNT GENE; SEQUENCE HOMOLOGY; SLOPPY PAIRED GENE; TRIBOLIUM CASTANEUM; WINGLESS GENE;

HEXAPODA; TRIBOLIUM CASTANEUM;

EID: 33846212803     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2006.09.037     Document Type: Article

References (52)

1. Anderson P. Mutagenesis. Methods Cell Biol. 48 (1995) 31-58
2. Baumgartner S., and Noll M. Network of interactions among pair-rule genes regulating paired expression during primordial segmentation of Drosophila. Mech. Dev. 33 (1990) 1-18
3. Benedyk M.J., Mullen J.R., and DiNardo S. odd-paired: a zinc finger pair-rule protein required for the timely activation of engrailed and wingless in Drosophila embryos. Genes Dev. 8 (1994) 105-117
4. Bennett R.L., Brown S.J., and Denell R.E. Molecular and genetic analysis of the Tribolium Ultrabithorax ortholog, Ultrathorax. Dev. Genes Evol. 209 (1999) 608-619
5. Bertuccioli C., Fasano L., Jun S., Wang S., Sheng G., and Desplan C. In vivo requirement for the paired domain and homeodomain of the paired segmentation gene product. Development 122 (1996) 2673-2685
6. Brown S.J., Hilgenfeld R.B., and Denell R.E. The beetle Tribolium castaneum has a fushi tarazu homolog expressed in stripes during segmentation. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 12922-12926
7. Brown S.J., Parrish J.K., Beeman R.W., and Denell R.E. Molecular characterization and embryonic expression of the even-skipped ortholog of Tribolium castaneum. Mech. Dev. 61 (1997) 165-173
8. Brown S., Holtzman S., Kaufman T., and Denell R. Characterization of the Tribolium Deformed ortholog and its ability to directly regulate Deformed target genes in the rescue of a Drosophila Deformed null mutant. Dev. Genes Evol. 209 (1999) 389-398
9. Brown S.J., Mahaffey J.P., Lorenzen M.D., Denell R.E., and Mahaffey J.W. Using RNAi to investigate orthologous homeotic gene function during development of distantly related insects. Evol. Dev. 1 (1999) 11-15
10. Bucher G., and Klingler M. Divergent segmentation mechanism in the short germ insect Tribolium revealed by giant expression and function. Development 131 (2004) 1729-1740
11. Bucher G., Scholten J., and Klingler M. Parental RNAi in Tribolium (Coleoptera). Curr. Biol. 12 (2002) R85-R86
12. Cadigan K.M., Grossniklaus U., and Gehring W.J. Functional redundancy: the respective roles of the two sloppy paired genes in Drosophila segmentation. Proc. Natl. Acad. Sci. U. S. A 91 (1994) 6324-6328
13. Cadigan K.M., Grossniklaus U., and Gehring W.J. Localized expression of sloppy paired protein maintains the polarity of Drosophila parasegments. Genes Dev. 8 (1994) 899-913
14. Cerny A.C., Bucher G., Schroder R., and Klingler M. Breakdown of abdominal patterning in the Tribolium Kruppel mutant jaws. Development 132 (2005) 5353-5363
15. Chipman A.D., Arthur W., and Akam M. A double segment periodicity underlies segment generation in centipede development. Curr. Biol. 14 (2004) 1250-1255
16. Choe C.P., Miller S.C., and Brown S.J. A pair-rule gene circuit defines segments sequentially in the short-germ insect Tribolium castaneum. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 6560-6564
17. Coulter D.E., and Wieschaus E. Gene activities and segmental patterning in Drosophila: analysis of odd-skipped and pair-rule double mutants. Genes Dev. 2 (1988) 1812-1823
18. Curtis C.D., Brisson J.A., DeCamillis M.A., Shippy T.D., Brown S.J., and Denell R.E. Molecular characterization of Cephalothorax, the Tribolium ortholog of Sex combs reduced. Genesis 30 (2001) 12-20
19. Damen W.G., Hausdorf M., Seyfarth E.A., and Tautz D. A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 10665-10670
20. Damen W.G., Janssen R., and Prpic N.M. Pair rule gene orthologs in spider segmentation. Evol. Dev. 7 (2005) 618-628
21. Davis G.K., and Patel N.H. Short, long, and beyond: molecular and embryological approaches to insect segmentation. Annu. Rev. Entomol. 47 (2002) 669-699
22. Davis G.K., Jaramillo C.A., and Patel N.H. Pax group III genes and the evolution of insect pair-rule patterning. Development 128 (2001) 3445-3458
23. Dawes R., Dawson I., Falciani F., Tear G., and Akam M. Dax, a locust Hox gene related to fushi-tarazu but showing no pair-rule expression. Development 120 (1994) 1561-1572
24. Dearden P.K., Donly C., and Grbic M. Expression of pair-rule gene homologues in a chelicerate: early patterning of the two-spotted spider mite Tetranychus urticae. Development 129 (2002) 5461-5472
25. Frigerio G., Burri M., Bopp D., Baumgartner S., and Noll M. Structure of the segmentation gene paired and the Drosophila PRD gene set as part of a gene network. Cell 47 (1986) 735-746
26. Gloor G.B., Preston C.R., Johnson-Schlitz D.M., Nassif N.A., Phillis R.W., Benz W.K., Robertson H.M., and Engels W.R. Type I repressors of P element mobility. Genetics 135 (1993) 81-95
27. Grossniklaus U., Pearson R.K., and Gehring W.J. The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev. 6 (1992) 1030-1051
28. Grossniklaus U., Cadigan K.M., and Gehring W.J. Three maternal coordinate systems cooperate in the patterning of the Drosophila head. Development 120 (1994) 3155-3171
29. Ingham P.W. The molecular genetics of embryonic pattern formation in Drosophila. Nature 335 (1988) 25-34
30. Ingham P.W., and Martinez-Arias A. The correct activation of Antennapedia and bithorax complex genes requires the fushi tarazu gene. Nature 324 (1986) 592-597
31. Ingham P.W., Baker N.E., and Martinez-Arias A. Regulation of segment polarity genes in the Drosophila blastoderm by fushi tarazu and even skipped. Nature 331 (1988) 73-75
32. Jaynes J.B., and Fujioka M. Drawing lines in the sand: even-skipped et al. and parasegment boundaries. Dev. Biol. 269 (2004) 609-622
33. Kilchherr F., Baumgartner S., Bopp D., Frei E., and Noll M. Isolation of the paired gene of Drosophila and its spatial expression during early embryogenesis. Nature 321 (1986) 493-499
34. Liu P.Z., and Kaufman T.C. even-skipped is not a pair-rule gene but has segmental and gap-like functions in Oncopeltus fasciatus, an intermediate germband insect. Development 132 (2005) 2081-2092
35. Maderspacher F., Bucher G., and Klingler M. Pair-rule and gap gene mutants in the flour beetle Tribolium castaneum. Dev.Genes Evol. 208 (1998) 558-568
36. Martinez Arias A., Baker N.E., and Ingham P.W. Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo. Development 103 (1988) 157-170
37. Mito T., Sarashina I., Zhang H., Iwahashi A., Okamoto H., Miyawaki K., Shinmyo Y., Ohuchi H., and Noji S. Non-canonical functions of hunchback in segment patterning of the intermediate germ cricket Gryllus bimaculatus. Development 132 (2005) 2069-2079
38. Morrissey D., Askew D., Raj L., and Weir M. Functional dissection of the paired segmentation gene in Drosophila embryos. Genes Dev. 5 (1991) 1684-1696
39. Nasiadka A., Dietrich B.H., and Krause H.M. Anterior-posterior patterning in the Drosophila embryo. Adv. Dev. Biol. Biochem. 12 (2002) 155-204
40. Niessing D., Rivera-Pomar R., La Rosee A., Hader T., Schock F., Purnell B.A., and Jackle H. A cascade of transcriptional control leading to axis determination in Drosophila. J. Cell. Physiol. 173 (1997) 162-167
41. Nulsen C., and Nagy L.M. The role of wingless in the development of multibranched crustacean limbs. Dev. Genes Evol. 209 (1999) 340-348
42. Nusslein-Volhard C., and Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature 287 (1980) 795-801
43. Osborne P.W., and Dearden P.K. Expression of Pax group III genes in the honeybee (Apis mellifera). Dev. Genes Evol. 215 (2005) 499-508
44. Patel N.H., Ball E.E., and Goodman C.S. Changing role of even-skipped during the evolution of insect pattern formation. Nature 357 (1992) 339-342
45. Patel N.H., Condron B.G., and Zinn K. Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles. Nature 367 (1994) 429-434
46. Patel N.H., Hayward D.C., Lall S., Pirkl N.R., DiPietro D., and Ball E.E. Grasshopper hunchback expression reveals conserved and novel aspects of axis formation and segmentation. Development 128 (2001) 3459-3472
47. Pourquie O. The segmentation clock: converting embryonic time into spatial pattern. Science 301 (2003) 328-330
48. Schoppmeier M., and Damen W.G. Expression of Pax group III genes suggests a single-segmental periodicity for opisthosomal segment patterning in the spider Cupiennius salei. Evol. Dev. 7 (2005) 160-169
49. Sommer R.J., and Tautz D. Involvement of an orthologue of the Drosophila pair-rule gene hairy in segment formation of the short germ-band embryo of Tribolium (Coleoptera). Nature 361 (1993) 448-450
50. Stollewerk A., Schoppmeier M., and Damen W.G. Involvement of Notch and Delta genes in spider segmentation. Nature 423 (2003) 863-865
51. Stuart J.J., Brown S.J., Beeman R.W., and Denell R.E. A deficiency of the homeotic complex of the beetle Tribolium. Nature 350 (1991) 72-74
52. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680