Novel modes of localization and function of nanos in the wasp Nasonia

Development

Volumn 137, Issue 22, 2010, Pages 3813-3821

  Lynch, Jeremy A ^a,b   Desplan, Claude ^a  

^a NEW YORK UNIVERSITY   (United States)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Evo devo; Germ plasm; Nanos; Nasonia; Patterning

Indexed keywords

HUNCHBACK PROTEIN; MESSENGER RNA; NANOS PROTEIN; PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; INSECT PROTEIN; RNA BINDING PROTEIN;

ARTICLE; FLY; GENE REPRESSION; GERM CELL; INSECT; NASONIA VITRIPENNIS; NONHUMAN; OOCYTE DEVELOPMENT; OVARY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA TRANSLATION; ANIMAL; ANIMAL EMBRYO; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORPHOGENESIS; PRENATAL DEVELOPMENT; PROTEIN SYNTHESIS; WASP;

NASONIA; NASONIA VITRIPENNIS;

ANIMALS; BODY PATTERNING; DNA-BINDING PROTEINS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSECT PROTEINS; PROTEIN BIOSYNTHESIS; RNA, MESSENGER, STORED; RNA-BINDING PROTEINS; WASPS;

EID: 78149236056     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.054213     Document Type: Article

References (61)

1. Achtelig, M. and Krause, G. (1971). Experiments on uncleared egg of Pimplaturionellae L. (Hymenoptera) for functional analysis of oosome region. Dev. Genes Evol. 167, 164-182.
2. Benoit, B., He, C. H., Zhang, F., Votruba, S. M., Tadros, W., Westwood, J. T., Smibert, C. A., Lipshitz, H. D. and Theurkauf, W. E. (2009). An essential role for the RNA-binding protein Smaug during the Drosophila maternal-to-zygotic transition. Development 136, 923-932.
3. Bergsten, S. E. and Gavis, E. R. (1999). Role for mRNA localization in translational activation but not spatial restriction of nanos RNA. Development 126, 659-669.
4. Berleth, T., Burri, M., Thoma, G., Bopp, D., Richstein, S., Frigerio, G., Noll, M. and Nusslein-Volhard, C. (1988). The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J. 7, 1749-1756.
5. Bilinski, S. M. and Jaglarz, M. K. (1999). Organization and possible functions of microtubule cytoskeleton in hymenopteran nurse cells. Cell Motil. Cytoskeleton 43, 213-220.
6. Bilinski, S. M. and Kloc, M. (2002). Accessory nuclei revisited: the translocation of snRNPs from the germinal vesicle to the periphery of the future embryo. Chromosoma 111, 62-68.
7. Brent, A. E., Schweitzer, R. and Tabin, C. J. (2003). A somitic compartment of tendon progenitors. Cell 113, 235-248.
8. Brent, A. E., Yucel, G., Small, S. and Desplan, C. (2007). Permissive and instructive anterior patterning rely on mRNA localization in the wasp embryo. Science 315, 1841-1843. (Pubitemid 46580142)
9. Bull, A. L. (1982). Stages of living embryos in the jewel wasp Mormoniella (Nasonia) vitripennis (Walker). Int. J. Insect Morphol. Embryol. 11, 1-23.
10. Chang, C. C., Lee, W. C., Cook, C. E., Lin, G. W. and Chang, T. (2006). Germplasm specification and germline development in the parthenogenetic pea aphid Acyrthosiphon pisum: Vasa and Nanos as markers. Int. J. Dev. Biol. 50, 413-421.
11. Cinnamon, E., Gur-Wahnon, D., Helman, A., St Johnston, D., Jimenez, G. and Paroush, Z. (2004). Capicua integrates input from two maternal systems in Drosophila terminal patterning. EMBO J. 23, 4571-4582.
12. Curtis, D., Apfeld, J. and Lehmann, R. (1995). nanos is an evolutionarily conserved organizer of anterior-posterior polarity. Development 121, 1899-1910.
13. da Fonseca, R. N., Lynch, J. A. and Roth, S. (2009). Evolution of axis formation: mRNA localization, regulatory circuits and posterior specification in non-model arthropods. Curr. Opin. Genet. Dev. 19, 404-411.
14. Dahanukar, A., Walker, J. A. and Wharton, R. P. (1999). Smaug, a novel RNA-binding protein that operates a translational switch in Drosophila. Mol. Cell 4, 209-218.
15. Dearden, P. K. (2006). Germ cell development in the Honeybee (Apis mellifera); vasa and nanos expression. BMC Dev. Biol. 6, 6.
16. Draper, B. W., McCallum, C. M. and Moens, C. B. (2007). nanos1 is required to maintain oocyte production in adult zebrafish. Dev. Biol. 305, 589-598.
17. Driever, W. and Nusslein-Volhard, C. (1988a). A gradient of bicoid protein in Drosophila embryos. Cell 54, 83-93.
18. Driever, W. and Nusslein-Volhard, C. (1988b). The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54, 95-104.
19. Driever, W., Thoma, G. and Nusslein-Volhard, C. (1989). Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen. Nature 340, 363-367.
20. Ephrussi, A., Dickinson, L. K. and Lehmann, R. (1991). oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66, 37-50.
21. Ferree, P. M., McDonald, K., Fasulo, B. and Sullivan, W. (2006). The origin of centrosomes in parthenogenetic hymenopteran insects. Curr. Biol. 16, 801-807.
22. Forbes, A. and Lehman, R. (1998). Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development 125, 679-690.
23. Forrest, K. M. and Gavis, E. R. (2003). Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila. Curr. Biol. 13, 1159-1168.
24. Gavis, E. R. and Lehmann, R. (1992). Localization of nanos RNA controls embryonic polarity. Cell 71, 301-313.
25. Goltsev, Y., Hsiong, W., Lanzaro, G. and Levine, M. (2004). Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos. Dev. Biol. 275, 435-446. (Pubitemid 40288097)
26. Grbic, M. (2003). Polyembryony in parasitic wasps: evolution of a novel mode of development. Int. J. Dev. Biol. 47, 633-642.
27. Hulskamp, M., Schroder, C., Pfeifle, C., Jackle, H. and Tautz, D. (1989). Posterior segmentation of the Drosophila embryo in the absence of a maternal posterior organizer gene. Nature 338, 629-632.
28. Hülskamp, M., Pfeifle, C. and Tautz, D. (1990). A morphogenetic gradient of hunchback protein organizes the expression of the gap genes Krüppel and knirps in the early Drosophila embryo. Nature 346, 577-580.
29. Irish, V., Lehman, R. and Akam, A. M. (1989). The Drosophila posterior-group gene nanos functions by repressing hunchback activity. Nature 338, 646-648.
30. Jaglarz, M. K., Bilinski, S. M. and Kloc, M. (2005). Assembly and breakdown of Cajal bodies in accessory nuclei of Hymenoptera. Differentiation 73, 99-108.
31. Kotkamp, K., Klingler, M. and Schoppmeier, M. (2010). Apparent role of Tribolium orthodenticle in anteroposterior blastoderm patterning largely reflects novel functions in dorsoventral axis formation and cell survival. Development 137, 1853-1862.
32. Lall, S., Ludwig, M. Z. and Patel, N. H. (2003). Nanos plays a conserved role in axial patterning outside of the Diptera. Curr. Biol. 13, 224-229.
33. Lehmann, R. and Nusslein-Volhard, C. (1991). The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo. Development 112, 679-691. (Pubitemid 21900274)
34. Lynch, J. A. and Desplan, C. (2006). A method for parental RNA interference in the wasp Nasonia vitripennis. Nat. Protoc. 1, 486-494.
35. Lynch, J. A., Olesnicky, E. C. and Desplan, C. (2006a). Regulation and function of tailless in the long germ wasp Nasonia vitripennis. Dev. Genes Evol. 216, 493-498.
36. Lynch, J. A., Brent, A. E., Leaf, D. S., Pultz, M. A. and Desplan, C. (2006b). Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature 439, 728-732.
37. Marques-Souza, H., Aranda, M. and Tautz, D. (2008). Delimiting the conserved features of hunchback function for the trunk organization of insects. Development 135, 881-888.
38. Mochizuki, K., Sano, H., Kobayashi, S., Nishimiya-Fujisawa, C. and Fujisawa, T. (2000). Expression and evolutionary conservation of nanos-related genes in Hydra. Dev. Genes Evol. 210, 591-602.
39. Olesnicky, E. C. and Desplan, C. (2007). Distinct mechanisms for mRNA localization during embryonic axis specification in the wasp Nasonia. Dev. Biol. 306, 134-142.
40. Olesnicky, E. C., Brent, A. E., Tonnes, L., Walker, M., Pultz, M. A., Leaf, D. and Desplan, C. (2006). A caudal mRNA gradient controls posterior development in the wasp Nasonia. Development 133, 3973-3982.
41. Patel, N. H., Hayward, D. C., Lall, S., Pirkl, N. R., DiPietro, D. and Ball, E. E. (2001). Grasshopper hunchback expression reveals conserved and novel aspects of axis formation and segmentation. Development 128, 3459-3472.
42. Pultz, M. A. and Leaf, D. S. (2003). The jewel wasp Nasonia: querying the genome with haplo-diploid genetics. Genesis 35, 185-191.
43. Pultz, M. A., Westendorf, L., Gale, S. D., Hawkins, K., Lynch, J., Pitt, J. N., Reeves, N. L., Yao, J. C., Small, S., Desplan, C. et al. (2005). A major role for zygotic hunchback in patterning the Nasonia embryo. Development 132, 3705-3715.
44. Raz, E. (2000). The function and regulation of vasa-like genes in germ-cell development. Genome Biol. 1, REVIEWS1017.
45. Rose, T. M., Schultz, E. R., Henikoff, J. G., Pietrokovski, S., McCallum, C. M. and Henikoff, S. (1998). Consensus-degenerate hybrid oligonucleotide primers for amplification of distantly related sequences. Nucleic Acids Res. 26, 1628-1635.
46. Savard, J., Tautz, D., Richards, S., Weinstock, G. M., Gibbs, R. A., Werren, J. H., Tettelin, H. and Lercher, M. J. (2006). Phylogenomic analysis reveals bees and wasps (Hymenoptera) at the base of the radiation of Holometabolous insects. Genome Res. 16, 1334-1338.
47. Schroder, R. (2003). The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 422, 621-625.
48. Simpson-Brose, M., Treisman, J. and Desplan, C. (1994). Synergy between the hunchback and bicoid morphogens is required for anterior patterning in Drosophila. Cell 78, 855-865.
49. Smibert, C. A., Wilson, J. E., Kerr, K. and Macdonald, P. M. (1996). smaug protein represses translation of unlocalized nanos mRNA in the Drosophila embryo. Genes Dev. 10, 2600-2609.
50. Smibert, C. A., Lie, Y. S., Shillinglaw, W., Henzel, W. J. and Macdonald, P. M. (1999). Smaug, a novel and conserved protein, contributes to repression of nanos mRNA translation in vitro. RNA 5, 1535-1547.
51. Struhl, G. (1989). Differing strategies for organizing anterior and posterior body pattern in Drosophila embryos. Nature 338, 741-744.
52. Struhl, G., Struhl, K. and Macdonald, P. M. (1989). The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell 57, 1259-1273.
53. Tautz, D. (1988). Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres. Nature 332, 281-284.
54. Tsuda, M., Sasaoka, Y., Kiso, M., Abe, K., Haraguchi, S., Kobayashi, S. and Saga, Y. (2003). Conserved role of nanos proteins in germ cell development. Science 301, 1239-1241. (Pubitemid 37052213)
55. Wang, C. and Lehmann, R. (1991). Nanos is the localized posterior determinant in Drosophila. Cell 66, 637-647.
56. Wang, C., Dickinson, L. K. and Lehmann, R. (1994). Genetics of nanos localization in Drosophila. Dev. Dyn. 199, 103-115.
57. Wang, Z. and Lin, H. (2004). Nanos maintains germline stem cell self-renewal by preventing differentiation. Science 303, 2016-2019.
58. Werren, J. H., Richards, S., Desjardins, C. A., Niehuis, O., Gadau, J., Colbourne, J. K., Beukeboom, L. W., Desplan, C., Elsik, C. G., Grimmelikhuijzen, C. J. P. et al. (2010). Functional and evolutionary insights from the genomes of three parasitoid nasonia species. Science 327, 343-348.
59. Wharton, R. P. and Struhl, G. (1991). RNA regulatory elements mediate control of drosophila body pattern by the posterior morphogen nanos. Cell 67, 955-967.
60. Wiegmann, B. M., Trautwein, M. D., Kim, J. W., Cassel, B. K., Bertone, M. A., Winterton, S. L. and Yeates, D. K. (2009). Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biol. 7, 34.
61. Wolff, C., Sommer, R., Schroder, R., Glaser, G. and Tautz, D. (1995). Conserved and divergent expression aspects of the Drosophila segmentation gene hunchback in the short germ band embryo of the flour beetle Tribolium. Development 121, 4227-4236.