Hox gene expression leads to differential hind leg development between honeybee castes

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Bomtorin, Ana Durvalina ^a   Barchuk, Angel Roberto ^b   Moda, Livia Maria ^a   Simoes, Zila Luz Paulino ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF ALFENAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

HOX PROTEIN;

ABDOMINAL A GENE; ANIMAL TISSUE; ARTICLE; ATAXIN 2 GENE; CRYPTOCEPHAL GENE; DACHSHUND GENE; DEVELOPMENTAL GENE; DISTAL LESS GENE; FEMALE; FUNCTIONAL MORPHOLOGY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE LOCATION; GRUNGE GENE; HINDLIMB; HONEYBEE; HOX GENE; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; INSECT CASTE; INSECT DEVELOPMENT; MICROARRAY ANALYSIS; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; RFABP GENE; ULTRABITHORAX GENE;

ANIMALS; BEES; DROSOPHILA MELANOGASTER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HINDLIMB; HOMEODOMAIN PROTEINS; INSECT PROTEINS; LARVA; MORPHOGENESIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS;

APIS MELLIFERA; CORBICULA; HEXAPODA;

EID: 84864327458     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040111     Document Type: Article

References (60)

1. Moczek AP, Sultan S, Foster S, Ledon-Rettig C, Dworkin I, et al. (2011) The role of developmental plasticity in evolutionary innovation. Proc Biol Sci. England: This journal is 2011 The Royal Society pp. 2705-2713.
2. Kamakura M, (2011) Royalactin induces queen differentiation in honeybees. Nature 473: 478-483.
3. Hartfelder K, Emlen DJ, Lawrence IG, (2012) 11- Endocrine Control of Insect Polyphenism. Insect Endocrinology. San Diego: Academic Press pp. 464-522.
4. Barchuk AR, Cristino AS, Kucharski R, Costa LF, Simoes ZLP, et al. (2007) Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. Bmc Developmental Biology 7.
5. Haydak MH, (1943) Larval food and development of castes in the honeybee. Journal of Economic Entomology 36: 778-792.
6. Michener CD, (2000) The bees of the world. The bees of the world. pp. i.
7. Patel A, Fondrk MK, Kaftanoglu O, Emore C, Hunt G, et al. (2007) The making of a queen: TOR pathway is a key player in diphenic caste development. PLoS One 2: e509.
8. Dedej S, Hartfelder K, Aumeier P, Rosenkranz P, Engels W, (1998) Caste determination is a sequential process: effect of larval age at grafting on ovariole number, hind leg size and cephalic volatiles in the honey bee (Apis mellifera carnica). Journal of Apicultural Research 37: 183-190.
9. Mutti NS, Dolezal AG, Wolschin F, Mutti JS, Gill KS, et al. (2011) IRS and TOR nutrient-signaling pathways act via juvenile hormone to influence honey bee caste fate. The Journal of Experimental Biology 214: 3977-3984.
10. Michener CD, (1990) Classification of the Apidae (Hymenoptera). University of Kansas Science Bulletin 54: 75-164.
11. Mahfooz NS, Li H, Popadic A, (2004) Differential expression patterns of the hox gene are associated with differential growth of insect hind legs. Proceedings of the National Academy of Sciences of the United States of America 101: 4877-4882.
12. Cohen SM, Jurgens G, (1989) Proximal-distal pattern formation in Drosophila: cell autonomous requirement for Distal-less gene activity in limb development. EMBO J 8: 2045-2055.
13. Rozowski M, Akam M, (2002) Hox gene control of segment-specific bristle patterns in Drosophila. Genes & Development 16: 1150-1162.
14. Snodgrass RE, (1956) Anatomy of the honey bee. Anatomy of the honey bee: xiv +334.
15. Ford DM, Hepburn HR, Moseley FB, Rigby RJ, (1981) Displacement sensors in the honeybee pollen basket. Journal of Insect Physiology 27: 339-&.
16. Rachinsky A, Strambi C, Strambi A, Hartfelder K, (1990) Caste and metamorphosis: hemolymph titers of juvenile hormone and ecdysteroids in last instar honeybee larvae. Gen Comp Endocrinol 79: 31-38.
17. Pepple KL, Atkins M, Venken K, Wellnitz K, Harding M, et al. (2008) Two-step selection of a single R8 photoreceptor: a bistable loop between senseless and rough locks in R8 fate. Development 135: 4071-4079.
18. Kojima T, (2004) The mechanism of Drosophila leg development along the proximodistal axis. Development Growth & Differentiation 46: 115-129.
19. Satterfield TF, Jackson SM, Pallanck LJ, (2002) A drosophila homolog of the polyglutamine disease gene SC42 is a dosage-sensitive regulator of actin filament formation. Genetics 162: 1687-1702.
20. Hewes RS, Schaefer AM, Taghert PH, (2000) The cryptocephal gene (ATF4) encodes multiple basic-leucine zipper proteins controlling molting and metamorphosis in Drosophila. Genetics 155: 1711-1723.
21. Jousse C, Averous J, Bruhat A, Carraro V, Mordier S, et al. (2004) Amino acids as regulators of gene expression: molecular mechanisms. Biochemical and Biophysical Research Communications 313: 447-452.
22. Mardon G, Solomon NM, Rubin GM, (1994) Dachshund encodes a nuclear-protein required for normal eye and leg development in Drosophila. Development 120: 3473-3486.
23. Charroux B, Freeman M, Kerridge S, Baonza A, (2006) Atrophin contributes to the negative regulation of epidermal growth factor receptor signaling in Drosophila. Developmental Biology 291: 278-290.
24. Stern DL, (1998) A role of Ultrabithorax in morphological differences between Drosophila species. Nature 396: 463-466.
25. Kelsh R, Weinzierl ROJ, White RAH, Akam M, (1994) Homeotic gene expression in the locust Schistocerca: an antibody that detects conserved epitopes in Ultrabithorax and Abdominal-A proteins. Developmental Genetics 15: 19-31.
26. Lees AD, Waddington CH, (1942) The development of the bristles in normal and some mutant types of Drosophila melanogaster. Proceedings of the Royal Society of London Series B-Biological Sciences 131: 87-110.
27. Thurm U, (1964) Mechanoreceptors in cuticle of honey bee- fine structure + stimulus mechanism. Science 145: 1063-1065.
28. McIver SB, (1975) Structure of cuticular mechanoreceptors of Arthropods. Annual Review of Entomology 20: 381-397.
29. Willingham AT, Keil T, (2004) A tissue specific cytochrome P450 required for the structure and function of Drosophila sensory organs. Mechanisms of Development 121: 1289-1297.
30. Maibeche-Coisne M, Monti-Dedieu L, Aragon S, Dauphin-Villemant C, (2000) A new cytochrome P450 from Drosophila melanogaster, CYP4G15, expressed in the nervous system. Biochemical and Biophysical Research Communications 273: 1132-1137.
31. Kawasaki H, Hirose S, Ueda H, (2002) beta FTZ-F1 dependent and independent activation of Edg78E, a pupal cuticle gene, during the early metamorphic period in Drosophila melanogaster. Development Growth & Differentiation 44: 419-425.
32. Kayashima Y, Hirose S, Ueda H, (2005) Anterior epidermis-specific expression of the cuticle gene EDG84A is controlled by many cis-regulatory elements in Drosophila melanogaster. Development Genes and Evolution 215: 545-552.
33. Rebers JE, Riddiford LM, (1988) Structure and Expression of a Manduca-Sexta Larval Cuticle Gene Homologous to Drosophila Cuticle Genes. Journal of Molecular Biology 203: 411-423.
34. Willis JH, (2010) Structural cuticular proteins from arthropods: Annotation, nomenclature, and sequence characteristics in the genomics era. Insect Biochemistry and Molecular Biology 40: 189-204.
35. Andersen SO, (2011) Are structural proteins in insect cuticles dominated by intrinsically disordered regions? Insect Biochemistry and Molecular Biology 41: 620-627.
36. Magkrioti CK, Spyropoulos IC, Iconomidou VA, Willis JH, Hamodrakas SJ, (2004) cuticleDB: a relational database of Arthropod cuticular proteins. BMC Bioinformatics 5: 138.
37. Karouzou MV, Spyropoulos Y, Iconomidou VA, Cornman RS, Hamodrakas SJ, et al. (2007) Drosophila cuticular proteins with the R&R Consensus: annotation and classification with a new tool for discriminating RR-1 and RR-2 sequences. Insect Biochem Mol Biol 37: 754-760.
38. McGinnis W, Krumlauf R, (1992) Homeobox genes and axial patterning. Cell 68: 283-302.
39. Alonso CR, (2002) Hox proteins: Sculpting body parts by activating localised cell death. Current Biology 12: R776-R778.
40. Pearson JC, Lemons D, McGinnis W, (2005) Modulating Hox gene functions during animal body patterning. Nature Reviews Genetics 6: 893-904.
41. Lewis EB, (1978) Gene complex controlling segmentation in Drosophila. Nature 276: 565-570.
42. Holland PWH, GarciaFernandez J, (1996) Hox genes and chordate evolution. Developmental Biology 173: 382-395.
43. Galant R, Carroll SB, (2002) Evolution of a transcriptional repression domain in an insect Hox protein. Nature 415: 910-913.
44. Ronshaugen M, McGinnis N, McGinnis W, (2002) Hox protein mutation and macroevolution of the insect body plan. Nature 415: 914-917.
45. Garaulet DL, Foronda D, Calleja M, Sánchez-Herrero E, (2008) Polycomb-dependent Ultrabithorax Hox gene silencing induced by high Ultrabithorax levels in Drosophila. Development 135: 3219-3228.
46. Crickmore MA, Ranade V, Mann RS, (2009) Regulation of Ubx expression by epigenetic enhancer silencing in response to Ubx levels and genetic variation. PLoS Genet 5: e1000633.
47. Ringrose L, Paro R, (2004) Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu Rev Genet 38: 413-443.
48. van der Knaap JA, Kumar BRP, Moshkin YM, Langenberg K, Krijgsveld J, et al. (2005) GMP synthetase stimulates histone H2B deubiquitylation by the epigenetic silencer USP7. Molecular Cell 17: 695-707.
49. Abouheif E, Wray GA, (2002) Evolution of the gene network underlying wing polyphenism in ants. Science 297: 249-252.
50. Barchuk AR, Bitondi MM, Simoes ZL, (2002) Effects of juvenile hormone and ecdysone on the timing of vitellogenin appearance in hemolymph of queen and worker pupae of Apis mellifera. J Insect Sci 2: 1.
51. Michelette ERD, Soares AEE, (1993) Characterization of preimaginal developmental stages in africanized honey-bee workers (Apis-mellifera L). Apidologie 24: 431-440.
52. Rembold H, Kremer JP, Ulrich GM, (1980) Characterization of post-embryonic developmental stages of the female castes of the honey bee, Apis-mellifera L. Apidologie 11: 29-38.
53. Brazma A, (2009) Minimum Information About a Microarray Experiment (MIAME)- Successes, Failures, Challenges. Thescientificworldjournal 9: 420-423.
54. Johnson RM, Evans JD, Robinson GE, Berenbaum MR, (2009) Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). Proc Natl Acad Sci U S A 106: 14790-14795.
55. Lourenco AP, Mackert A, Cristino AD, Simoes ZLP, (2008) Validation of reference genes for gene expression studies in the honey bee, Apis mellifera, by quantitative real-time RT-PCR. Apidologie 39: 372-U333.
56. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944-945.
57. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene Ontology: tool for the unification of biology. Nature Genetics 25: 25-29.
58. Al-Shahrour F, Diaz-Uriarte R, Dopazo J, (2004) FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 20: 578-580.
59. Patel NH, (1994) Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. Methods Cell Biol 44: 445-487.
60. Walldorf U, Binner P, Fleig R, (2000) Hox genes in the honey bee Apis mellifera. Dev Genes Evol 210: 483-492.