Evidence against a germ plasm in the milkweed bug Oncopeltus fasciatus, a hemimetabolous insect

Biology Open

Volumn 2, Issue 6, 2013, Pages 556-568

  Ewen Campen, Ben ^a   Jones, Tamsin E M ^a   Extavour, Cassandra G ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

Boule; Germ line; RNA interference; Spermatogenesis; Tudor; Vasa

Indexed keywords

EID: 84965054178     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20134390     Document Type: Article

References (130)

1. Achtelig, M. and Krause, G. (1971). Experimente am ungefurchten ei von Pimpla turionellae L. (Hymenoptera) zur funktionsanalyse des oosombereichs. Wilhelm Roux Arch. Entwickl. Mech. Org. 167, 164-182.
2. Akam, M. (1998). Hox genes: from master genes to micromanagers. Curr. Biol. 8, R676-R678.
3. Anastas, A., Hunt, C. and Stebbings, H. (1991). Characterization of a nucleotidesensitive high molecular weight microtubule-associated protein in the ovary of a hemipteran insect. Cell Motil. Cytoskeleton 19, 37-48.
4. Anderson, D. T. (1973). Embryology And Phylogeny In Annelids And Arthropods. Oxford: Pergamon Press.
5. Arkov, A. L. and Ramos, A. (2010). Building RNA-protein granules: insight from the germline. Trends Cell Biol. 20, 482-490.
6. Baena-Lopez, L. A. and García-Bellido, A. (2006). Control of growth and positional information by the graded vestigial expression pattern in the wing of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 103, 13734-13739.
7. Bardsley, A., McDonald, K. and Boswell, R. E. (1993). Distribution of tudor protein in the Drosophila embryo suggests separation of functions based on site of localization. Development 119, 207-219.
8. Bonhag, P. F. and Wick, J. R. (1953). The functional anatomy of the male and female reproductive systems of the milkweed bug, Oncopeltus fasciatus (Dallas) (Heteroptera: Lygaeidae). J. Morphol. 93, 177-283.
9. Boswell, R. E. and Mahowald, A. P. (1985). tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster. Cell 43, 97-104.
10. Braat, A. K., van de Water, S., Korving, J. and Zivkovic, D. (2001). A zebrafish vasa morphant abolishes vasa protein but does not affect the establishment of the germline. Genesis 30, 183-185.
11. Bronskill, J. F. (1959). Embryology of Pimpla turionellae (L.) (Hymenoptera: Ichneumonidae). Can. J. Zool. 37, 655-688.
12. Büning, J. (1994). The Insect Ovary: Ultrastructure, Previtellogenic Growth And Evolution. London: Chapman and Hall.
13. Buss, L. W. (1987). The Evolution Of Individuality. Princeton, NJ: Princeton University Press.
14. Butt, F. H. (1949). Embryology Of The Milkweed Bug: Oncopeltus Fasciatus (Hemiptera), pp. 2-43. Ithaca, NY: Cornell University Agricultural Experiment Station.
15. Callebaut, M. (2008). A review: Historical evolution of preformistic versus neoformistic (epigenetic) thinking in embryology. Belg. J. Zool. 138, 20-35.
16. Calvo, E., Walter, M., Adelman, Z. N., Jimenez, A., Onal, S., Marinotti, O. and James, A. A. (2005). Nanos (nos) genes of the vector mosquitoes, Anopheles gambiae, Anopheles stephensi and Aedes aegypti. Insect Biochem. Mol. Biol. 35, 789-798.
17. Chang, C. C., Lee, W. C., Cook, C. E., Lin, G.W. and Chang, T. (2006). Germ-plasm specification and germline development in the parthenogenetic pea aphid Acyrthosiphon pisum: Vasa and Nanos as markers. Int. J. Dev. Biol. 50, 413-421.
18. Chang, C. C., Lin, G. W., Cook, C. E., Horng, S. B., Lee, H. J. and Huang, T. Y. (2007). Apvasa marks germ-cell migration in the parthenogenetic pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Dev. Genes Evol. 217, 275-287.
19. Chang, C. C., Huang, T. Y., Cook, C. E., Lin, G. W., Shih, C. L. and Chen, R. P. (2009). Developmental expression of Apnanos during oogenesis and embryogenesis in the parthenogenetic pea aphid Acyrthosiphon pisum. Int. J. Dev. Biol. 53, 169-176.
20. Craig, L. R. (2009). Defending evo-devo: a response to Hoekstra and Coyne. Philos. Sci. 76, 335-344.
21. Curtis, D., Apfeld, J. and Lehmann, R. (1995). nanos is an evolutionarily conserved organizer of anterior-posterior polarity. Development 121, 1899-1910.
22. Davis, B. K. (1971). Genetic analysis of a meiotic mutant resulting in precocious sistercentromere separation in Drosophila melanogaster. Mol. Gen. Genet. 113, 251-272.
23. Dearden, P. K. (2006). Germ cell development in the honeybee (Apis mellifera); vasa and nanos expression. BMC Dev. Biol. 6, 6.
24. Diez-Roux, G., Banfi, S., Sultan, M., Geffers, L., Anand, S., Rozado, D., Magen, A., Canidio, E., Pagani, M., Peluso, I. et al. (2011). A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoS Biol. 9, e1000582.
25. Donnell, D. M., Corley, L. S., Chen, G. and Strand, M. R. (2004). Caste determination in a polyembryonic wasp involves inheritance of germ cells. Proc. Natl. Acad. Sci. USA 101, 10095-10100.
26. Dumser, J. B. (1980). The regulation of spermatogenesis in insects. Annu. Rev. Entomol. 25, 341-369.
27. Eberhart, C. G., Maines, J. Z. and Wasserman, S. A. (1996). Meiotic cell cycle requirement for a fly homologue of human Deleted in Azoospermia. Nature 381, 783-785.
28. Economopoulos, A. P. and Gordon, H. T. (1971). Growth and differentiation of the testes in the large milkweed bug, Oncopeltus fasciatus (Dallas). J. Exp. Zool. B 177, 391-405.
29. Erezyilmaz, D. F., Rynerson, M. R., Truman, J. W. and Riddiford, L. M. (2009). The role of the pupal determinant broad during embryonic development of a directdeveloping insect. Dev. Genes Evol. 219, 535-544.
30. Ewen-Campen, B., Schwager, E. E. and Extavour, C. G. (2010). The molecular machinery of germ line specification. Mol. Reprod. Dev. 77, 3-18.
31. Ewen-Campen, B., Shaner, N., Panfilio, K. A., Suzuki, Y., Roth, S. and Extavour, C. G. (2011). The maternal and early embryonic transcriptome of the milkweed bug Oncopeltus fasciatus. BMC Genomics 12, 61.
32. Ewen-Campen, B., Srouji, J. R., Schwager, E. E. and Extavour, C. G. (2012). oskar predates the evolution of germ plasm in insects. Curr. Biol. 22, 2278-2283.
33. Ewen-Campen, B., Donoughe, S., Clarke, D. N. and Extavour, C. G. (2013). Germ cell specification requires zygotic mechanisms rather than germ plasm in a basally branching insect. Curr. Biol. (in press).
34. Extavour, C. G. (2007). Evolution of the bilaterian germ line: lineage origin and modulation of specification mechanisms. Integr. Comp. Biol. 47, 770-785.
35. Extavour, C. G. and Akam, M. E. (2003). Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130, 5869-5884.
36. Fabioux, C., Corporeau, C., Quillien, V., Favrel, P. and Huvet, A. (2009). In vivo RNA interference in oyster - vasa silencing inhibits germ cell development. FEBS J. 276, 2566-2573.
37. Fleischmann, V. G. (1975). Origin and embryonic development of fertile gonads with and without pole cells of Pimpla turionellae L. (Hymenoptera, Ichneumonidae). Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere. 94, 375-411.
38. Fujiwara, Y., Komiya, T., Kawabata, H., Sato, M., Fujimoto, H., Furusawa, M. and Noce, T. (1994). Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc. Natl. Acad. Sci. USA 91, 12258-12262.
39. Golumbeski, G. S., Bardsley, A., Tax, F. and Boswell, R. E. (1991). tudor, a posteriorgroup gene of Drosophila melanogaster, encodes a novel protein and an mRNA localized during mid-oogenesis. Genes Dev. 5, 2060-2070.
40. Goss, R. J. (1952). The early embryology of the book louse, Liposcelis divergens Badonnel (Psocoptera; liposcelidae). J. Morphol. 91, 135-167.
41. Handler, D., Olivieri, D., Novatchkova, M., Gruber, F. S., Meixner, K., Mechtler, K., Stark, A., Sachidanandam, R. and Brennecke, J. (2011). A systematic analysis of Drosophila TUDOR domain-containing proteins identifies Vreteno and the Tdrd12 family as essential primary piRNA pathway factors. EMBO J. 30, 3977-3993.
42. Hardy, R. W., Tokuyasu, K. T., Lindsley, D. L. and Garavito, M. (1979). The germinal proliferation center in the testis of Drosophila melanogaster. J. Ultrastruct. Res. 69, 180-190.
43. Harrison, A., Stebbings, H. and Hyams, J. S. (1991). Different patterns of α-tubulin post-translational modification in ovarian nutritive tubes of two hemipteran insects. J. Cell Sci. 100, 501-507.
44. Hegner, R. W. (1914). Studies on germ cells. I. The history of the germ cells in insects with special reference to the Keimbahn-determinants. II. The origin and significance of the Keimbahn-determinants in animals. J. Morphol. 25, 375-509.
45. Hellen, C. U. and Sarnow, P. (2001). Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev. 15, 1593-1612.
46. Heming, B. S. (1979). Origin and fate of germ cells in male and female embryos of Haplothrips verbasci (Osborn) (Insecta, Thysanoptera, Phlaeothripidae). J. Morphol. 160, 323-343.
47. Heming, B. S. and Huebner, E. (1994). Development of the germ cells and reproductive primordia in male and female embryos of Rhodnius prolixus Sta°l (Hemiptera, Reduviidae). Can. J. Zool. 72, 1100-1119.
48. Heymons, R. (1895). Die Embryonalentwicklung Von Dermapteren Und Orthopteren. Jena: G. Fischer.
49. Hoekstra, H. E. and Coyne, J. A. (2007). The locus of evolution: evo devo and the genetics of adaptation. Evolution 61, 995-1016.
50. Huettner, A. F. (1923). The origin of the germ cells in Drosophila melanogaster. J. Morphol. 37, 385-423.
51. Hurst, S., Talbot, N. J. and Stebbings, H. (1999). A staufen-like RNA-binding protein in translocation channels linking nurse cells to oocytes in Notonecta shows nucleotide-dependent attachment to microtubules. J. Cell Sci. 112, 2947-2955.
52. Hyams, J. S. and Stebbings, H. (1979). The formation and breakdown of nutritive tubes - massive microtubular organelles associated with cytoplasmic transport. J. Ultrastruct. Res. 68, 46-57.
53. Jan, E., Thompson, S. R., Wilson, J. E., Pestova, T. V., Hellen, C. U. and Sarnow, P. (2001). Initiator Met-tRNA-independent translation mediated by an internal ribosome entry site element in cricket paralysis virus-like insect viruses. Cold Spring Harb. Symp. Quant. Biol. 66, 285-292.
54. Johnstone, O. and Lasko, P. (2004). Interaction with eIF5B is essential for Vasa function during development. Development 131, 4167-4178.
55. Juhn, J. and James, A. A. (2006). oskar gene expression in the vector mosquitoes, Anopheles gambiae and Aedes aegypti. Insect Mol. Biol.15, 363-372.
56. Juhn, J., Marinotti, O., Calvo, E. and James, A. A. (2008). Gene structure and expression of nanos (nos) and oskar (osk) orthologues of the vector mosquito, Culex quinquefasciatus. Insect Mol. Biol. 17, 545-552.
57. Juliano, C. E., Swartz, S. Z. and Wessel, G. M. (2010). A conserved germline multipotency program. Development 137, 4113-4126.
58. Kainz, F., Ewen-Campen, B., Akam, M. and Extavour, C. G. (2011). Notch/Delta signalling is not required for segment generation in the basally branching insect Gryllus bimaculatus. Development 138, 5015-5026.
59. Kaye, J. S. and McMaster-Kaye, R. (1966). The fine structure and chemical composition of nuclei during spermiogenesis in the house cricket. I. Initial stages of differentiation and the loss of nonhistone protein. J. Cell Biol. 31, 159-179.
60. Kelly, G. M. and Huebner, E. (1989). Embryonic development of the hemipteran insect Rhodnius prolixus. J. Morphol. 199, 175-196.
61. Khila, A. and Abouheif, E. (2010). Evaluating the role of reproductive constraints in ant social evolution. Philos. Trans. R. Soc. B 365, 617-630.
62. Kim-Ha, J., Kerr, K. and Macdonald, P. M. (1995). Translational regulation of oskar mRNA by Bruno, an ovarian RNA-binding protein, is essential. Cell 81, 403-412.
63. Kozmik, Z. (2005). Pax genes in eye development and evolution. Curr. Opin. Genet. Dev. 15, 430-438.
64. Kumé, M. and Dan, K. (1968). Invertebrate Embryology. Belgrade: Prosveta.
65. Lasko, P. F. and Ashburner, M. (1990). Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development. Genes Dev. 4, 905-921.
66. Lécuyer, E., Yoshida, H., Parthasarathy, N., Alm, C., Babak, T., Cerovina, T., Hughes, T. R., Tomancak, P. and Krause, H. M. (2007). Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131, 174-187.
67. Li, M., Hong, N., Xu, H., Yi, M., Li, C., Gui, J. and Hong, Y. (2009). Medaka vasa is required for migration but not survival of primordial germ cells. Mech. Dev. 126, 366-381.
68. Liang, L., Diehl-Jones, W. and Lasko, P. (1994). Localization of vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. Development 120, 1201-1211.
69. Liu, P. Z. and Kaufman, T. C. (2004). hunchback is required for suppression of abdominal identity, and for proper germband growth and segmentation in the intermediate germband insect Oncopeltus fasciatus. Development 131, 1515-1527.
70. Lu, H. L., Tanguy, S., Rispe, C., Gauthier, J. P., Walsh, T., Gordon, K., Edwards, O., Tagu, D., Chang, C. C. and Jaubert-Possamai, S. (2011). Expansion of genes encoding piRNA-associated argonaute proteins in the pea aphid: diversification of expression profiles in different plastic morphs. PLoS ONE 6, e28051.
71. Lynch, J. A. and Desplan, C. (2010). Novel modes of localization and function of nanos in the wasp Nasonia. Development 137, 3813-3821.
72. Lynch, J. A., Ozüak, O., Khila, A., Abouheif, E., Desplan, C. and Roth, S. (2011). The phylogenetic origin of oskar coincided with the origin of maternally provisioned germ plasm and pole cells at the base of the Holometabola. PLoS Genet. 7, e1002029.
73. Magnúsdóttir, E., Gillich, A., Grabole, N. and Surani, M. A. (2012). Combinatorial control of cell fate and reprogramming in the mammalian germline. Curr. Opin. Genet. Dev. 22, 466-474.
74. Mahowald, A. P. (2001). Assembly of the Drosophila germ plasm. Int. Rev. Cytol. 203, 187-213.
75. Medrano, J. V., Ramathal, C., Nguyen, H. N., Simon, C. and Reijo Pera, R. A. (2012). Divergent RNA-binding proteins, DAZL and VASA, induce meiotic progression in human germ cells derived in vitro. Stem Cells 30, 441-451.
76. Mellanby, H. (1935). The early embryonic development of Rhodnius prolixus (Hemiptera, Heteroptera). Q. J. Microsc. Sci. 78, 71-90.
77. Metschnikoff, E. (1866). Embryologische studien an insekten. Z. Wiss. Zool. 16, 389-500.
78. Miura, T., Braendle, C., Shingleton, A., Sisk, G., Kambhampati, S. and Stern, D. L. (2003). A comparison of parthenogenetic and sexual embryogenesis of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). J. Exp. Zool. B Mol. Dev. Evol. 295, 59-81.
79. Moczek, A. P. (2008). On the origins of novelty in development and evolution. Bioessays 30, 432-447.
80. Nakao, H. (1999). Isolation and characterization of a Bombyx vasa-like gene. Dev. Genes Evol. 209, 312-316.
81. Nakao, H., Hatakeyama, M., Lee, J. M., Shimoda, M. and Kanda, T. (2006). Expression pattern of Bombyx vasa-like (BmVLG) protein and its implications in germ cell development. Dev. Genes Evol. 216, 94-99.
82. Nelsen, O. E. (1934). The segregation of the germ cells in the grasshopper, Melanoplus differentialis (Acrididae; Orthoptera). J. Morphol. 55, 545-575.
83. Nieuwkoop, P. D. and Sutasurya, L. A. (1981). Primordial Germ Cells In The Invertebrates: From Epigenesis To Preformation. Cambridge: Cambridge University Press.
84. Nousch, M. and Eckmann, C. R. (2013). Translational control in the Caenorhabditis elegans germ line. Adv. Exp. Med. Biol. 757, 205-247.
85. Ohashi, H., Umeda, N., Hirazawa, N., Ozaki, Y., Miura, C. and Miura, T. (2007). Expression of vasa (vas)-related genes in germ cells and specific interference with gene functions by double-stranded RNA in the monogenean, Neobenedenia girellae. Int. J. Parasitol. 37, 515-523.
86. Özhan-Kizil, G., Havemann, J. and Gerberding, M. (2009). Germ cells in the crustacean Parhyale hawaiensis depend on Vasa protein for their maintenance but not for their formation. Dev. Biol. 327, 230-239.
87. Panfilio, K. A. (2008). Extraembryonic development in insects and the acrobatics of blastokinesis. Dev. Biol. 313, 471-491.
88. Pek, J. W., Anand, A. and Kai, T. (2012). Tudor domain proteins in development. Development 139, 2255-2266.
89. Rangan, P., DeGennaro, M., Jaime-Bustamante, K., Coux, R.-X., Martinho, R. G. and Lehmann, R. (2009). Temporal and spatial control of germ-plasm RNAs. Curr. Biol. 19, 72-77.
90. Richardson, B. E. and Lehmann, R. (2010). Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat. Rev. Mol. Cell Biol. 11, 37-49.
91. Richter, J. D. and Lasko, P. (2011). Translational control in oocyte development. Cold Spring Harb. Perspect. Biol. 3, a002758.
92. Rocak, S. and Linder, P. (2004). DEAD-box proteins: the driving forces behind RNA metabolism. Nat. Rev. Mol. Cell Biol. 5, 232-241.
93. Roonwal, M. L. (1937). Studies on the embryology of the african migratory locust, Locusta migratoria migratoides Reiche and Frm. (Orthoptera, Acrididae). II. Organogeny. Philos. Trans. R. Soc. B 227, 175-244.
94. Salinas, L. S., Maldonado, E., Macías-Silva, M., Blackwell, T. K. and Navarro, R. E. (2007). The DEAD box RNA helicase VBH-1 is required for germ cell function in C. elegans. Genesis 45, 533-546.
95. Salinas, L. S., Franco-Cea, A., Láscarez-Lagunas, L. I., Villanueva-Chimal, E., Maldonado, E. and Navarro, R. E. (2012). Germ cell survival in C. elegans and C. remanei is affected when the DEAD box RNA helicases VBH-1 or Cre-VBH-1 are silenced. Genesis 50, 801-818.
96. Sander, K. and Mirza, M. B. (1956). The Early Embryology Of Pyrilla Perpusilla Walker (Homoptera), Including Some Observations On The Later Development (On Indian Insect Types, no. 4), p. 61. Aligarh: Aligarh Muslim University Publications.
97. Sasaki, J. and Nakashima, N. (2000). Methionine-independent initiation of translation in the capsid protein of an insect RNA virus. Proc. Natl. Acad. Sci. USA 97, 1512-1515.
98. Schmidt, E. D. and Dorn, A. (2004). Structural polarity and dynamics of male germline stem cells in the milkweed bug (Oncopeltus fasciatus). Cell Tissue Res. 318, 383-394.
99. Schröder, R. (2006). vasa mRNA accumulates at the posterior pole during blastoderm formation in the flour beetle Tribolium castaneum. Dev. Genes Evol. 216, 277-283.
100. Schüpbach, T. and Wieschaus, E. (1986). Maternal-effect mutations altering the anterior-posterior pattern of the Drosophila embryo. Roux. Arch. Dev. Biol. 195, 302-317.
101. Schüpbach, T. and Wieschaus, E. (1991). Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 129, 1119-1136.
102. Schwalm, F. E. (1965). Zell - und mitosenmuster der normalen und nach rötgenbestrahlung regulierenden keimanlage von Gryllus domesticus. Zeitschrift für Morphologie und Ökologie der Tiere 55, 915-1023.
103. Seidel, F. (1924). Die geschlechtsorgane in der embryonalentwicklung von pyrrhocoris apterus L. Zeitschrift für Morphologie und Ökologie der Tiere 1, 429-506.
104. Sengupta, M. S. and Boag, P. R. (2012). Germ granules and the control of mRNA translation. IUBMB Life 64, 586-594.
105. Shah, C., Vangompel, M. J. W., Naeem, V., Chen, Y., Lee, T., Angeloni, N., Wang, Y. and Xu, E. Y. (2010). Widespread presence of human BOULE homologs among animals and conservation of their ancient reproductive function. PLoS Genet. 6, e1001022.
106. Spike, C., Meyer, N., Racen, E., Orsborn, A., Kirchner, J., Kuznicki, K., Yee, C., Bennett, K. and Strome, S. (2008). Genetic analysis of the Caenorhabditis elegans GLH family of P-granule proteins. Genetics 178, 1973-1987.
107. Stebbings, H. and Hunt, C. (1987). The translocation of mitochondria along insect ovarian microtubules from isolated nutritive tubes: a simple reactivated model. J. Cell Sci. 88, 641-648.
108. Stebbings, H., Sharma, K. and Hunt, C. (1985). Protein turnover in the cytoplasmic transport system within an insect ovary - a clue to the mechanism of microtubule associated transport. FEBS Lett. 193, 22-26.
109. Stephen, S., Talbot, N. J. and Stebbings, H. (1999). Poly(A) mRNA is attached to insect ovarian microtubules in vivo in a nucleotide-sensitive manner. Cell Motil. Cytoskeleton 43, 159-166.
110. Stern, D. L. and Orgogozo, V. (2008). The loci of evolution: how predictable is genetic evolution? Evolution 62, 2155-2177.
111. Styhler, S., Nakamura, A., Swan, A., Suter, B. and Lasko, P. (1998). vasa is required for GURKEN accumulation in the oocyte, and is involved in oocyte differentiation and germline cyst development. Development 125, 1569-1578.
112. Sunanaga, T., Watanabe, A. and Kawamura, K. (2007). Involvement of vasa homolog in germline recruitment from coelomic stem cells in budding tunicates. Dev. Genes Evol. 217, 1-11.
113. Tanaka, S. S., Toyooka, Y., Akasu, R., Katoh-Fukui, Y., Nakahara, Y., Suzuki, R., Yokoyama, M. and Noce, T. (2000). The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev. 14, 841-853.
114. Tomancak, P., Guichet, A., Zavorszky, P. and Ephrussi, A. (1998). Oocyte polarity depends on regulation of gurken by Vasa. Development 125, 1723-1732.
115. Tomancak, P., Beaton, A., Weiszmann, R., Kwan, E., Shu, S., Lewis, S. E., Richards, S., Ashburner, M., Hartenstein, V., Celniker, S. E. et al. (2002). Systematic determination of patterns of gene expression during Drosophila embryogenesis. Genome Biol. 3, research0088.1-research0088.14.
116. Tomancak, P., Berman, B. P., Beaton, A., Weiszmann, R., Kwan, E., Hartenstein, V., Celniker, S. E. and Rubin, G. M. (2007). Global analysis of patterns of gene expression during Drosophila embryogenesis. Genome Biol. 8, R145.
117. Tsunekawa, N., Naito, M., Sakai, Y., Nishida, T. and Noce, T. (2000). Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development 127, 2741-2750.
118. Wang, C. and Lehmann, R. (1991). Nanos is the localized posterior determinant in Drosophila. Cell 66, 637-647.
119. Webster, P. J., Liang, L., Berg, C. A., Lasko, P. and Macdonald, P. M. (1997). Translational repressor bruno plays multiple roles in development and is widely conserved. Genes Dev. 11, 2510-2521.
120. Wheeler, W. M. (1893). A contribution to insect embryology. J. Morphol. 8, 1-161.
121. Will, L. (1888). Entwicklungsgeschichte der viviparen aphiden. Zoologische Jahrbücher 3, 201-280.
122. Witlaczil, E. (1884). Entwicklungsgeschichte der aphiden. Z. Wiss. Zool. 40, 559-696.
123. Wu, H.-R., Chen, Y.-T., Su, Y.-H., Luo, Y.-J., Holland, L. Z. and Yu, J.-K. (2011). Asymmetric localization of germline markers Vasa and Nanos during early development in the amphioxus Branchiostoma floridae. Dev. Biol. 353, 147-159.
124. Yajima, M. and Wessel, G. M. (2011). The multiple hats of Vasa: its functions in the germline and in cell cycle progression. Mol. Reprod. Dev. 78, 861-867.
125. Yeates, D. K., Cameron, S. L. and Trautwein, M. (2012). A view from the edge of the forest: recent progress in understanding the relationships of the insect orders. Aust. J. Entomol. 51, 79-87.
126. Ying, M. and Chen, D. (2012). Tudor domain-containing proteins of Drosophila melanogaster. Dev. Growth Differ. 54, 32-43.
127. Yoon, C., Kawakami, K. and Hopkins, N. (1997). Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124, 3157-3165.
128. Zeng, V. and Extavour, C. G. (2012). ASGARD: an open-access database of annotated transcriptomes for emerging model arthropod species. Database 2012, bas048.
129. Zhao, G., Chen, K., Yao, Q., Wang, W., Wang, Y., Mu, R., Chen, H., Yang, H. and Zhou, H. (2008). The nanos gene of Bombyx mori and its expression patterns in developmental embryos and larvae tissues. Gene Expr. Patterns 8, 254-260.
130. Zhurov, V., Terzin, T. and Grbić, M. (2004). Early blastomere determines embryo proliferation and caste fate in a polyembryonic wasp. Nature 432, 764-769.