Patterning of the adult mandibulate mouthparts in the red flour beetle, Tribolium castaneum

Genetics

Volumn 190, Issue 2, 2012, Pages 639-654

  Angelini, David R ^a,b   Smith, Frank W ^b   Aspiras, Ariel C ^a   Kikuchi, Moto ^b   Jockusch, Elizabeth L ^b  

^a AMERICAN UNIVERSITY   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; NOTCH RECEPTOR; RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DACHSHUND; TRANSCRIPTION FACTOR HOMOTHORAX; UNCLASSIFIED DRUG;

ARTICLE; BODY REGIONS; INSECT MANDIBULATE MOUTHPART; LIP; MAXILLA; METAMORPHOSIS; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRIBOLIUM;

ANIMALS; BODY PATTERNING; GENES, INSECT; HOMEODOMAIN PROTEINS; LIGANDS; MANDIBLE; MAXILLA; METAMORPHOSIS, BIOLOGICAL; NUCLEAR PROTEINS; PHENOTYPE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, NOTCH; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; SIGNAL TRANSDUCTION; TRIBOLIUM; ZINC FINGERS;

EID: 84857383171     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.111.134296     Document Type: Article

References (86)

1. Abouheif, E., and G. A. Wray, 2002 Evolution of the gene network underlying wing polyphenism in ants. Science 297: 249-252.
2. Abu-Shaar, M., and R. S. Mann, 1998 Generation of multiple antagonistic domains along the proximodistal axis during Drosophila leg development. Development 125: 3821-3830.
3. Abzhanov, A., and T. C. Kaufman, 2000 Homologs of Drosophila appendage genes in the patterning of arthropod limbs. Dev. Biol. 227: 673-689.
4. Abzhanov, A., S. Holtzman, and T. C. Kaufman, 2001 The Drosophila proboscis is specified by two Hox genes, proboscipedia and Sex combs reduced, via repression of leg and antennal appendage genes. Development 128: 2803-2814.
5. Angelini, D. R., and T. C. Kaufman, 2004 Functional analyses in the hemipteran Oncopeltus fasciatus reveal conserved and derived aspects of appendage patterning in insects. Dev. Biol. 271: 306-321.
6. Angelini, D. R., and T. C. Kaufman, 2005a Functional analyses in the milkweed bug Oncopeltus fasciatus (Hemiptera) support a role for Wnt signaling in body segmentation but not appendage development. Dev. Biol. 283: 409-423.
7. Angelini, D. R., and T. C. Kaufman, 2005b Insect appendages and comparative ontogenetics. Dev. Biol. 286: 57-77.
8. Angelini, D. R., M. Kikuchi, and E. L. Jockusch, 2009 Genetic patterning in the adult capitate antenna of the beetle Tribolium castaneum. Dev. Biol. 327: 240-251.
9. Angelini, D. R., F. W. Smith, M., and E. L. Jockusch, 2012 Extent with modification: patterning in the legs of Tribolium castaneum and the evolution of serial homologs. G3: Genes, Genomes, Genetics 2: 235-248.
10. Aspiras, A. C., F. W. Smith, and D. R. Angelini, 2011 Sex-specific gene interactions in the patterning of insect genitalia. Dev. Biol. 360: 369-380.
11. Beermann, A., D. G. Jay, R. W. Beeman, M. Hulskamp, D. Tautz et al., 2001 The Short antennae gene of Tribolium is required for limb development and encodes the orthologue of the Drosophila Distal-less protein. Development 128: 287-297.
12. Bishop, S. A., T. Klein, A. M. Arias, and J. P. Couso, 1999 Composite signalling from Serrate and Delta establishes leg segments in Drosophila through Notch. Development 126: 2993-3003.
13. Boyden, A., 1947 Homology and analogy. A critical review of the meanings and implications of these concepts in biology. Am. Midl. Nat. 37: 648-669.
14. Boxshall, G. A., 2004 The evolution of arthropod limbs. Biol. Rev. Camb. Philos. Soc. 79: 253-300.
15. Brown, S., S. Holtzman, T. Kaufman, and R. Denell, 1999 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: 389-398.
16. Brown, S., M. DeCamillis, K. Gonzalez-Charneco, M. Denell, R. Beeman et al., 2000 Implications of the Tribolium Deformed mutant phenotype for the evolution of Hox gene function. Proc. Natl. Acad. Sci. USA 97: 4510-4514.
17. Brusca, R. C., G. J. Brusca, and N. Haver, 2002 The Invertebrates. Sinauer Associates, Sunderland, MA.
18. Campbell, G., 2002 Distalization of the Drosophila leg by graded EGF-receptor activity. Nature 418: 781-785.
19. Caubit, X., R. Thangarajah, T. Theil, J. Wirth, H. G. Nothwang et al., 1999 Mouse Dac a novel nuclear factor with homology to Drosophila Dachshund shows a dynamic expression in the neural crest, the eye, the neocortex, and the limb bud. Dev. Dyn. 214: 66-80.
20. Cifuentes, F. J., and A. García-Bellido, 1997 Proximo-distal specification in the wing disc of Drosophila by the nubbin gene. Proc. Natl. Acad. Sci. USA 94: 11405-11410.
21. Cohen, S. M., and G. Jürgens, 1989 Proximal-distal pattern formation in Drosophila: graded requirement for Distal-less gene activity during limb development. Roux's Arch. Dev. Biol. 198: 157-169.
22. Daly, H. V., and A. Sokoloff, 1965 Labiopedia, a sex-linked mutant in Tribolium confusum Duval (Coleoptera: Tenebrionidae). J. Morphol. 117: 251-269.
23. Daly, H. V., J. T. Doyen, and A. H. I. Purcell, 1998 Introduction to Insect Biology and Diversity. Oxford University Press, Oxford.
24. de Celis, J. F., D. M. Tyler, J. de Celis, and S. J. Bray, 1998 Notch signalling mediates segmentation of the Drosophila leg. Development 125: 4617-4626.
25. de Celis Ibeas, J. M., and S. J. Bray, 2003 Bowl is required downstream of Notch for elaboration of distal limb patterning. Development 130: 5943-5952.
26. Diaz-Benjumea, F. J., and A. Garcia-Bellido, 1990 Genetic analysis of the wing vein pattern of Drosophila. Rouxs Arch. Dev. Biol. 198: 336-354.
27. El-Kifl, A. H., 1953 Morphology of the adult Tribolium confusum Duv. and its differentiation from Tribolium (Stene) castaneum Herbst. Bull. Soc. Entomol. Égypte 37: 173-249.
28. Galindo, M. I., S. A. Bishop, S. Greig, and J. P. Couso, 2002 Leg patterning driven by proximal-distal interactions and EGFR signaling. Science 297: 256-259.
29. Galindo, M. I., S. A. Bishop, and J. P. Couso, 2005 Dynamic EGFRRas signalling in Drosophila leg development. Dev. Dyn. 233: 1496-1508.
30. Giorgianni, M. W., and N. H. Patel, 2004 Patterning of the branched head appendages in Schistocerca americana and Tribolium castaneum. Evol. Dev. 6: 402-410.
31. Greenberg, L., and V. Hatini, 2009 Essential roles for lines in mediating leg and antennal proximodistal patterning and generating a stable Notch signaling interface at segment borders. Dev. Biol. 330: 93-104.
32. Grieder, N. C., I. Charlafti, U. Kloter, H. Jäckle, U. Schäfer et al., 2007 Misexpression screen in Drosophila melanogaster aiming to reveal novel factors involved in formation of body parts. Genetics 175: 1707-1718.
33. Grimaldi, D., and M. S. Engel, 2005 Evolution of the Insects, Cambridge University Press, New York.
34. Hao, I., R. B. Green, O. Dunaevsky, J. A. Lengyel, and C. Rauskolb, 2003 The odd-skipped family of zinc finger genes promotes Drosophila leg segmentation. Dev. Biol. 263: 282-295.
35. Hrycaj, S., M. Mihajlovic, N. Mahfooz, J. P. Couso, and A. Popadić, 2008 RNAi analysis of nubbin embryonic functions in a hemimetabolous insect, Oncopeltus fasciatus. Evol. Dev. 10: 705-716.
36. Hu, S., D. Fambrough, J. R. Atashi, C. S. Goodman, and S. T. Crews, 1995 The Drosophila abrupt gene encodes a BTB-zinc finger regulatory protein that controls the specificity of neuromuscular connections. Genes Dev. 9: 2936-2948.
37. Huet, C., and J. J. Lenoir-Rousseaux, 1976 Etude de la mise en place de la patte imaginale de Tenebrio molitor. 1. Analyse expérimentale des processus de restauration au cours de la morphogenése. J. Embryol. Exp. Morphol. 35: 303-321.
38. Inbal, A., N. Halachmi, C. Dibner, D. Frank, and A. Salzberg, 2001 Genetic evidence for the transcriptional-activating function of Homothorax during adult fly development. Development 128: 3405-3413.
39. Inoue, Y., T. Mito, K. Miyawaki, K. Matsushima, Y. Shinmyo et al., 2002 Correlation of expression patterns of homothorax, dachshund, and Distal-less with the proximodistal segmentation of the cricket leg bud. Mech. Dev. 113: 141-148.
40. Jockusch, E. L., C. Nulsen, S. J. Newfeld, and L. M. Nagy, 2000 Leg development in flies vs. grasshoppers: differences in dpp expression do not lead to differences in the expression of downstream components of the leg patterning pathway. Development 127: 1617-1626.
41. Jockusch, E. L., T. A. Williams, and L. M. Nagy, 2004 The evolution of patterning of serially homologous appendages in insects. Dev. Genes Evol. 214: 324-338.
42. Joulia, L., H.-M. Bourbon, and D. L. Cribbs, 2005 Homeotic proboscipedia function modulates hedgehog-mediated organizer activity to pattern adult Drosophila mouthparts. Dev. Biol. 278: 496-510.
43. Joulia, L., J. Deutsch, H.-M. Bourbon, and D. Cribbs, 2006 The specification of a highly derived arthropod appendage, the Drosophila labial palps, requires the joint action of selectors and signaling pathways. Dev. Genes Evol. 216: 431-442.
44. Kukalová-Peck, J., 1998 Arthropod phylogeny and 'basal' morphological structures, pp. 249-268 in Arthropod Relationships, edited by R. A. Fortey and R. H. Thomas. Chapman & Hall, London.
45. Lecuit, T., and S. M. Cohen, 1997 Proximal-distal axis formation in the Drosophila leg. Nature 388: 139-145.
46. Li, H., and A. Popadić, 2004 Analysis of nubbin expression patterns in insects. Evol. Dev. 6: 310-324.
47. Lord, J. C., K. Hartzer, M. Toutges, and B. Oppert, 2010 Evaluation of quantitative PCR reference genes for gene expression studies in Tribolium castaneum after fungal challenge. J. Microbiol. Methods 80: 219-221.
48. Manton, S. M., 1964 Mandibular mechanisms and the evolution of arthropods. Philos. Trans. R. Soc. Lond. B Biol. Sci. 247: 1-183.
49. Moczek, A. P., and D. J. Rose, 2009 Differential recruitment of limb patterning genes during development and diversification of beetle horns. Proc. Natl. Acad. Sci. USA 106: 8992-8997.
50. Ng, M., F. J. Diaz-Benjumea, and S. M. Cohen, 1995 Nubbin encodes a POU-domain protein required for proximal-distal patterning in the Drosophila wing. Development 121: 589-599.
51. Niimi, T., H. Kuwayama, and T. Yaginuma, 2005 Larval RNAi applied to the analysis of postembryonic development in the ladybird beetle, Harmonia axyridis. J. Insect Biotechnol. Sericol. 74: 95-102.
52. Olesen, J., S. Richter, and G. Scholtz, 2001 The evolutionary transformation of phyllopodous to stenopodous limbs in the Branchiopoda (Crustacea): Is there a common mechanism for early limb development in arthropods? Int. J. Dev. Biol. 45: 869-876.
53. Palopoli, M. F., and N. H. Patel, 1998 Evolution of the interaction between Hox genes and a downstream target. Curr. Biol. 8: 587-590.
54. Panganiban, G., L. Nagy, and S. B. Carroll, 1994 The role of the Distal-less gene in the development and evolution of insect limbs. Curr. Biol. 4: 671-675.
55. Pfaffl, M. W., 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: e45.
56. Pfaffl, M. W., 2004 Quantification strategies in real-time PCR, pp. 87-112 in A-Z of Quantitative PCR, edited by S. A. Bustin. International University Line Press, La Jolla, CA.
57. Popadić, A.G. Panganiban, D. Rusch, W. A. Shear, and T. C. Kaufman, 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.
58. Prpic, N.-M., and W. G. M. Damen, 2009 Notch-mediated segmentation of the appendages is a molecular phylotypic trait of the arthropods. Dev. Biol. 326: 262-271.
59. Prpic, N.-M., B. Wigand, W. G. Damen, and M. Klingler, 2001 Expression of dachshund in wild-type and Distal-less mutant Tribolium corroborates serial homologies in insect appendages. Dev. Genes Evol. 211: 467-477.
60. R Development Core Team, 2010 R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
61. Raff, R. A., 1996 The Shape of Life. University of Chicago Press, Chicago.
62. Rauskolb, C., 2001 The establishment of segmentation in the Drosophila leg. Development 128: 4511-4521.
63. Regier, J. C., J. W. Shultz, A. Zwick, A. Hussey, B. Ball et al., 2010 Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463: 1079-1083.
64. Rivera, A., and D. Weisblat, 2009 And Lophotrochozoa makes three: Notch/Hes signaling in annelid segmentation. Dev. Genes Evol. 219: 37-43.
65. Rogers, B. T., M. D. Peterson, and T. C. Kaufman, 2002 The development and evolution of insect mouthparts as revealed by the expression patterns of gnathocephalic genes. Evol. Dev. 4: 96-110.
66. Ronco, M., T. Uda, T. Mito, A. Minelli, S. Noji et al., 2008 Antenna and all gnathal appendages are similarly transformed by homothorax knock-down in the cricket Gryllus bimaculatus. Dev. Biol. 313: 80-92.
67. Roth, V. L., 1984 On homology. Biol. J. Linn. Soc. Lond. 22: 13-29.
68. Rozen, S., and H. J. Skaletsky, 2000 Primer3 on the WWW for general users and for biologist programmers, pp. 365-386 in Bioinformatics Methods and Protocols: Methods in Molecular Biology, edited by S. Krawetz and S. Misener. Humana Press, Totowa, NJ.
69. Scholtz, G., B. Mittmann, and M. Gerberding, 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.
70. Schoppmeier, M., and W. G. Damen, 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.
71. Sewell, W., T. Williams, J. Cooley, M. Terry, R. Ho et al., 2008 Evidence for a novel role for dachshund in patterning the proximal arthropod leg. Dev. Genes Evol. 218: 293-305.
72. Simonnet, F., and A. P. Moczek, 2011 Conservation and diversification of gene function during mouthpart development in Onthophagus beetles. Evol. Dev. 13: 280-289.
73. Snodgrass, R. E., 1928 Morphology and evolution of the insect head and its appendages. Smithsonian Misc. Coll. 81: 1-158.
74. Snodgrass, R. E., 1935 Principles of Insect Morphology, McGraw- Hill, New York.
75. Sokoloff, A., 1972 The Biology of Tribolium, Vol. 1. Clarendon Press, Oxford.
76. Sommer, R. J., 2008 Homology and the hierarchy of biological systems. BioEssays 30: 653-658.
77. Suzuki, Y., D. C. Squires, and L. M. Riddiford, 2009 Larval leg integrity is maintained by Distal-less and is required for proper timing of metamorphosis in the flour beetle, Tribolium castaneum. Dev. Biol. 326: 60-67.
78. Tomoyasu, Y., and R. E. Denell, 2004 Larval RNAi in Tribolium (Coleoptera) for analyzing adult development. Dev. Genes Evol. 214: 575-578.
79. Tribolium Genome Sequencing Consortium, 2008 The genome of the model beetle and pest Tribolium castaneum. Nature 452: 949-955.
80. True, J. R., and E. S. Haag, 2001 Developmental system drift and flexibility in evolutionary trajectories. Evol. Dev. 3: 109-119.
81. Turchyn, N., J. Chesebro, S. Hrycaj, J. P. Couso, and A. Popadić, 2011 Evolution of nubbin function in hemimetabolous and holometabolous insect appendages. Dev. Biol. 357: 84-95.
82. van der Meer, J. M., 1977 Optical clean and permanent whole mount preparation for phase-contrast microscopy of cuticular structures of insect larvae. Dros. Inf. Serv. 52: 160.
83. Wagner, G. P., 2007 The developmental genetics of homology. Nat. Rev. Genet. 8: 473-479.
84. Williams, T. A., 1998 Distalless expression in crustaceans and the patterning of branched limbs. Dev. Genes Evol. 207: 427-434.
85. Wu, J., and S. M. Cohen, 1999 Proximodistal axis formation in the Drosophila leg: subdivision into proximal and distal domains by Homothorax and Distal-less. Development 126: 109-117.
86. Yao, L. C., G. J. Liaw, C. Y. Pai, and Y. H. Sun, 1999 A common mechanism for antenna-to-leg transformation in Drosophila: suppression of homothorax transcription by four HOM-C genes. Dev. Biol. 211: 268-276.