Tokens of love: Functions and regulation of Drosophila male accessory gland products

Insect Biochemistry and Molecular Biology

Volumn 27, Issue 3, 1997, Pages 179-192

  Wolfner, Mariana F ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Accessory glands; Drosophila; Egg laying; Hormones; Life span; Receptivity; Reproduction; Seminal fluid; Sperm storage

Indexed keywords

GLYCOPROTEIN; HORMONE PRECURSOR; INSECT HORMONE;

ACCESSORY SEX GLAND; ANIMAL; DROSOPHILA; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HORMONAL REGULATION; MALE; MALE GENITAL SYSTEM; MATING; NONHUMAN; PHYSIOLOGY; REPRODUCTION; REVIEW; SEMINAL PLASMA; SEXUAL BEHAVIOR; SPERM;

ANIMALIA; DROSOPHILA MELANOGASTER; HEXAPODA; INSECTA; MELANOGASTER;

EID: 0031105559     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0965-1748(96)00084-7     Document Type: Short Survey

References (102)

1. Aguadé M., Miyashita N. and Langley C. (1992) Polymorphism and divergence in the Mst26A male accessory gland gene region in Drosophila. Genetics 132, 755-770.
2. Aigaki T., Fleischmann I., Chen P. S. and Kubli E. (1991) Ectopic expression of sex peptide alters reproductive behavior of female D. melanogaster. Neuron 7, 557-563.
3. Antony C. and Jallon J. (1982) The chemical basis of sex recognition in Drosophila melanogaster. J. Insect Physiol. 28, 873-880.
4. Bairati A. (1968) Structure and ultrastructure of the male reproductive system of Drosophila melanogaster Meig. 2. The genital duct and accessory glands. Monit. Zool. Ital. 2, 105-182.
5. Bastock M. and Manning A. (1955) The courtship of Drosophila melanogaster. Behav. 8, 85-111.
6. Baumann H. (1974) The isolation, partial characterization, and biosynthesis of paragonial substances, PS-1 and PS-2 of Drosophila funebris. J. Ins. Physiol. 20, 2181-2194.
7. Belote J. M. and Baker B. S. (1982) Sex determination in Drosophila melanogaster: Analysis of transformer-2, a sex-transforming locus. Proc. Natl. Acad. Sci., USA 79, 1568-1572.
8. Benoit R., Ling N. and Esch T. (1987) A new prosomatostatin-derived peptide reveals a pattern for prohormone cleavage at monobasic sites. Science 238, 1126-1129.
9. Bertram M., Akerkar G. A., Ard R. L., Gonzalez C. and Wolfner M. F. (1992) Cell type specific gene expression in the Drosophila melanogaster male accessory gland. Mechs. Dev. 38, 33-40.
10. Bertram M. J. (1994) Cell type-specific gene expression in the Drosophila melanogaster male accessory gland and the characterization of an accessory gland protein. Ph.D. thesis, Cornell University, Ithaca, NY, USA.
11. Bertram M. J., Neubaum D. M. and Wolfner M. F. (1996) Localization of the Drosophila accessory gland protein Acp36DE in the mated female suggests a role in sperm storage. Insect Biochem. Mol. Biol. 26, 971-980.
12. Boulétreau-Merle J. (1974) Stimulation de l'ovogenèse par la copulation chez les femelles de Drosophila melanogaster privée de leur complexe endocrine rétrocérebrale. J. Insect Physiol. 20, 2035-2041.
13. Boulétreau-Merle J. (1976) Déstruction de la pars intercerebralis chez Drosophila melanogaster: effet sur la fécondité et sur sa stimulation par l'accouplement. J. Insect Physiol. 22, 933-940.
14. Cavener D. R. and MacIntyre R. J. (1983) Biphasic expression and function of glucose dehydrogenase in Drosophila melanogaster. Proc. Natl. Acad. Sci., USA 80, 6286-6288.
15. Chapman K. B. and Wolfner M. F. (1988) Determination of male-specific gene expression in Drosophila accessory glands. Dev. Biol. 126, 195-202.
16. Chapman T. (1992) A cost of mating with males that do not transfer sperm in female Drosophila melanogaster. J. Insect Physiol. 38, 223-227.
17. Chapman T., Hutchings J. and Partridge L. (1993) No reduction in the cost of mating for Drosophila melanogaster females mating with spermless males. Proc. R. Soc. Lond. B 253, 211-217.
18. Chapman T., Liddle L. F., Kalb J. M., Wolfner M. F. and Partridge L. (1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373, 241-244.
19. Chapman T. and Partridge L. (1996) Sexual conflict as fuel for evolution. Nature 381, 189-190.
20. Chen P. S. (1984) The functional morphology and biochemistry of insect male accessory glands and their secretions. Ann. Rev. Entomol. 29, 233-255.
21. Chen P. S. (1991) Biochemistry and molecular regulation of the male accessory gland secretions in Drosophila (Diptera). Annls. Soc. ent. Fr. 27, 231-244.
22. Chen P. S. (1996) The accessory gland proteins in male Drosophila: structural, reproductive and evolutionary aspects. Experientia 52, 503-510.
23. Chen P. S. and Balmer J. (1989) Secretory proteins and sex peptides of the male accessory gland in Drosophila sechellia. J. Insect Physiol. 35, 759-764.
24. Chen P. S., Stumm-Zollinger E., Aigaki T., Balmer J., Bienz M. and Bohlen P. (1988) A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell 54, 291-298.
25. Clark A. G., Silveria S., Meyers W. and Langley C. H. (1994) Nature screen: An efficient method for screening natural populations of Drosophila for targeted P-element insertions. Proc. Natl. Acad. Sci. USA 91, 719-722.
26. Clark A. G., Aguadé M., Prout T., Harshman L. G. and Langley C. H. (1995) Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. Genetics 139, 189-201.
27. Coleman S., Drahn B., Petersen G., Stolorov J. and Kraus K. (1995) A Drosophila male accessory gland protein that is a member of the serpin superfamily of proteinase inhibitors is transferred to females during mating. Insect Biochem. Mol. Biol. 25, 203-207.
28. Connolly K. and Cook R. (1973) Rejection responses by female Drosophila melanogaster: their ontogeny, causality and effects upon the behavior of the courting male. Behav. 44, 142-166.
29. Cook R. and Cook A. (1975) The attractiveness to males of female Drosophila melanogaster: effects of mating, age and diet. Anim. Behav. 23, 521-526.
30. Del Solar E. and Palomino H. (1966) Choice of oviposition sites in D. melanogaster. Am. Nat. 100, 123-133.
31. DiBenedetto A. J., Harada H. A. and Wolfner M. F. (1990) Structure, cell-specific expression, and mating-induced regulation of a Drosophila melanogaster male accessory gland gene. Dev. Biol. 139, 134-148.
32. DiBenedetto A. J., Lakich D. M., Kruger W. D., Belote J. M., Baker B. S. and Wolfner M. F. (1987) Sequences expressed sex-specifically in Drosophila melanogaster adults. Dev. Biol. 119, 242-251.
33. Eguchi Y., Itoh T. and Tomizawa J. I. (1991) Antisense RNA. Ann. Rev. Biochem. 60, 631-652.
34. Epper F. and Bryant P. J. (1983) Sex-specific control of growth and differentiation in the Drosophila genital disc, studied using a temperature-sensitive transformer-2 mutation. Dev. Biol. 100, 294-307.
35. Fowler K. and Partridge L. (1989) A cost of mating in female fruitflies. Nature 338, 760-761.
36. Fuller M. T. (1993) Spermatogenesis. In The Development of Drosophila melanogaster. (Edited by M. Bate and A. Martinez Arias), pp. 71-147. Cold Spring Harbor Press, New York.
37. Fuyama Y. (1983) Species specificity of paragonial substances as an isolating mechanism in Drosophila. Experientia 39, 190-192.
38. Garcia-Bellido A. (1964) Das Sekret der Paragonien als Stimulus der Fekundität bei Weibchen von Drosophila melanogaster. Z. Naturforsch. 19b, 491-495.
39. Gilbert D. G. (1981) Ejaculate esterase and initial sperm use by female Drosophila melanogaster. J. Insect Physiol. 27, 641-650.
40. Gilbert D. G., Richmond R. C. and Sheehan K. B. (1981) Studies of esterase 6 in Drosophila melanogaster. V. Progeny production and sperm use in females inseminated by males having active or null alleles. Evolution 35, 21-37.
41. Gromko M. H., Gilbert D. G. and Richmond R. C. (1984) Sperm transfer and use in the multiple mating system of Drosophila. In Sperm competition and the evolution of mating systems. (Edited by Smith, R. L.), pp. 371-426. Academic Press, New York.
42. Hall J. C. (1994) The mating of a fly. Science 264, 1702-1714.
43. Harshman L. G. and Prout T. (1994) Sperm displacement without sperm transfer in Drosophila melanogaster. Evolution 48, 758-766.
44. Herndon L. A. and Wolfner M. F. (1995) A Drosophila seminal fluid protein, Acp26Aa, stimulates egg-laying in females for one day following mating. Proc. Natl. Acad. Sci. USA 92, 10114-10118.
45. Hihara F. (1981) Effects of the male accessory gland secretion on oviposition and remating in females of Drosophila melanogaster. Zool. Mag. 90, 303-316.
46. Jallon J. (1984) A few chemical words exchanged by Drosophila during courtship and mating. Behav. Genet. 14, 441-478.
47. Kalb J. M., DiBenedetto A. J. and Wolfner M. F. (1993) Probing the function of Drosophila melanogaster accessory glands by directed cell ablation. Proc. Natl. Acad. Sci. USA 90, 8093-8097.
48. Kaldany R.-R. J., Nambu J. R. and Scheller R. H. (1985) Neuropeptides in identified Aplysia neurons. Ann. Rev. Neurosci. 8, 431-455.
49. Kaplan W. D., Tinderholt V. E. and Gugler D. H. (1962) The number of sperm present in reproductive tracts of D. melanogaster females. Dros. Inf. Serv. 36, 82.
50. Keller L. (1995) All's fair when love is war. Nature 373, 190-191.
51. Kornfeld R. and Kornfeld S. (1985) Assembly of asparagine-linked oligosaccharides. Ann. Rev. Biochem. 54, 631-664.
52. Kubli E. (1992) My favorite molecule: the sex peptide. Bioessays 14, 779-784.
53. Kubli E. (1996) The Drosophila sex-peptide: a peptide pheromone involved in reproduction. Adv. Devel. Biochem. 4, 99-128.
54. Lasko P. F. (1994) Molecular genetics of Drosophila oogenesis. R. G. Landes Company, Austin, TX.
55. Lefevre G. and Jonsson V. B. (1962) Sperm transfer, storage, displacement and utilization in Drosophila melanogaster. Genetics 47, 1719-1736.
56. Ludwig M. Z., Uspensky I. I., Ivanov A. I., Kopantseva M. R., Dianov C. M., Tamarina N. A. and Korchin L. I. (1991) Genetic control and expression of the major ejaculatory bulb protein PEB-me in Drosophila melanogaster. Bioch. Genet. 29, 215-240.
57. Manning A. (1962) A sperm factor affecting the receptivity of Drosophila melanogaster females. Nature 194, 252-253.
58. Manning A. (1967) The control of sexual receptivity in female Drosophila. Anim. Behav. 15, 239-250.
59. Meikle D. B., Sheehan K. B., Phillis D. M. and Richmond R. C. (1990) Localization and longevity of seminal-fluid esterase 6 in mated female Drosophila melanogaster. J. Insect Physiol. 14, 1159-1168.
60. Merle J. (1968) Fonctionnement ovarien et réçeptivité sexuelle de Drosophila melanogaster après implantation de fragments de l'appareil génital male. J. Insect Physiol. 14, 1159-1168.
61. Monsma S. A. (1990) Structure and expression of two Drosophila melanogaster male accessory gland genes, and the fate of their products after transfer to the female fly during mating. Ph.D. thesis, Cornell University, Ithaca. NY, USA.
62. Monsma S. A., Harada H. A. and Wolfner M. F. (1990) Synthesis of two Drosophila male accessory gland proteins and their fate after transfer to the female during mating. Dev. Biol. 142, 465-475.
63. Monsma S. A. and Wolfner M. F. (1988) Structure and expression of a Drosophila male accessory gland gene whose product resembles a peptide pheromone precursor. Genes Dev. 2, 1063-1073.
64. Moshitzky P., Fleischmann I., Chaimov N., Saudan P., Klauser S., Kubli E. and Applebaum S. W. (1996) Sex-peptide activates juvenile hormone biosynthesis in the Drosophila melanogaster corpus allatum. Arch. Ins. Bioch. Physiol. 32, 363-374.
65. Nakayama K., Watanabe T., Nakagawa T., Kim W. S., Nagahama M., Hosaka M., Hatsuzawa K., Kondoh-Hashiba K. and Murakami K. (1992) Consensus sequence for precursor processing of mono-arginyl sites: evidence for the involvement of a kex2-like endoprotease in precursor cleavages at both dibasic and mono-arginyl sites. J. Biol. Chem. 267, 16335-16340.
66. Nöthiger R., Dubendorfer A. and Epper F. (1977) Gynandromorphs reveal two separate primordia for male and female genitalia in Drosophila melanogaster. Wilh. Roux's Arch. 181, 367-373.
67. Obara Y., Tateda H. and Kuwabara M. (1975) Mating behavior of the cabbage white butterfly, Pieris rapae crucivora Boisduval.: V. Copulatory stimuli inducing changes of female response patterns. Zool. Mag. 84, 71-76.
68. Ohashi Y. Y., Hamo-Fukushima K. and Fuyama Y. (1991) Purification and characterization of an ovulation stimulating substance from the male accessory glands of Drosophila suzukii. Insect Biochem. 21, 413-419.
69. Pappenheimer A. M. (1977) Diphtheria toxin. Ann. Rev. Biochem. 46, 69-94.
70. Park M. and Wolfner M. F. (1995) Male and female cooperate in the processing of a Drosophila melanogaster seminal fluid protein. Dev. Biol. 171, 694-702.
71. Partridge L. and Fowler K. (1990) Non-mating costs of exposure to males in female Drosophila melanogaster. J. Insect Physiol. 36, 419-425.
72. Partridge L., Green A. and Fowler K. (1987) Effects of egg-production and of exposure to males on female survival in Drosophila melanogasler. J. Insect Phsiol. 10, 745-749.
73. Prout T. and Bundgaard J. (1977) Population genetics of sperm displacement. Genetics 85, 95-124.
74. Rice W. R. (1996) Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381, 232-234.
75. Riddiford L. M. (1993) Hormones and Drosophila development. In The Development of Drosophila melanogaster (Edited by M. Bate and A. Martinez Arias), pp. 899-940. Cold Spring Harbor Press, New York.
76. Schäfer U. (1986) Genes for male-specific transcripts in Drosophila melanogaster. Mol. Gen. Genet. 202, 219-225.
77. Scheller R. H., Jackson J. F., McAlister L. B., Rothman B. S., Mayeri E. and Axel R. (1983) A single gene encodes multiple neuropeptides mediating a stereotyped behavior. Cell 32, 7-22.
78. Schmidt T., Choffat Y., Klauser S. and Kubli E. (1993a) The Drosophila melanogaster sex-peptide: a molecular analysis of structure-function relationships. J. Insect Physiol. 39, 361-368.
79. Schmidt T., Choffat Y., Schneider M., Hunziker P., Fuyama Y. and Kubli E. (1993b) Drosophila suzukii contains a peptide homolo-gous to the Drosophila melanogaster sex peptide and functional in both species. Insect Biochem. Mol. Biol. 23, 571-579.
80. Schmidt T., Stumm-Zollinger E. and Chen P. S. (1985) Protein metabolism of Drosophila melanogaster male accessory glands - III. Stimulation of protein synthesis following copulation. Insect Biochem. 15, 391-401.
81. Schmidt T., Stumm-Zollinger E. and Chen P. S. (1989) A male accessory gland peptide with protease inhibitory activity in Drosophila funebris. J. Biol. Chem. 264, 9745-9749.
82. Schwartz T. W. (1986) The processing of peptide precursors: proline-directed arginyl cleavage and other monobasic processing mechanisms. FEBS Lett. 200, 1-10.
83. Scott D. (1986) Sexual mimicry regulates the attractiveness of mated Drosophila melanogaster females. Proc. Natl. Acad. Sci. USA 83, 8429-8433.
84. Scott D. (1987) The timing of the sperm effect on female Drosophila melanogaster receptivity. Anim. Behav. 35, 142-149.
85. Scott D. and Richmond R. C. (1985) An effect of mate fertility on the attractiveness and oviposition rates of mated Drosophila melanogaster females. Anim. Behav. 33, 817-824.
86. Scott D. and Richmond R. C. (1990) Sperm loss by remating Drosophila melanogaster females. J. Insect Physiol. 36, 451-456.
87. Scott D. and Williams E. (1993) Sperm displacement after remating in Drosophila melanogaster. J. Insect Physiol. 39, 201-206.
88. Simmerl E., Schäfer M. and Schäfer U. (1995) Structure and regulation of a gene cluster for male accessory gland transcripts in Drosophila melanogaster. Insect Biochem. Mol. Biol. 25, 127-137.
89. Simmons L. W. and Parker G. A. (1989) Nuptial feeding in insects: mating effort versus paternal investment. Ethology 81, 332-343.
90. Spradling A. C. (1993) Developmental genetics of oogenesis. In The Development of Drosophila melanogaster. (Edited by M. Bate and A. Martinez Arias), pp. 1-70. Cold Spring Harbor Press, New York.
91. Styger D. (1992) Molukulare Analyse des Sexpeptidgens aus Drosophila melanogaster. Ph.D. thesis, University of Zürich, Switzerland
92. Szabad J. and Fajszi C. (1982) Control of female reproduction in o-sophila: Genetic dissection using gynandromorphs. Genetics 100, 61-78.
93. Tompkins L. (1984) Genetic analysis of sex appeal in Drosophila. Behav. Genet. 14, 411-440.
94. Tompkins L., Gross A. C., Hall J. C., Gailey D. A. and Siegel R. W. (1982) The role of female movement in the sexual behavior of Drosophila melanogaster. Behav. Genet. 12, 295-307.
95. Tompkins L. and Hall J. C. (1981) The different effects on courtship of volatile compounds from mated and virgin Drosophila females. J. Insect Physiol. 27, 17-21.
96. Tompkins L. and Hall J. C. (1983) Identification of brain sites controlling female receptivity in mosaics of Drosophila melanogaster. Genetics 103, 179-195.
97. Tompkins L., Siegel R., Gailey D. and Hall J. (1983) Conditioned courtship in Drosophila and its mediation by chemical cues. Behav. Genet. 13, 565-578.
98. Von Heijne G. (1983) Patterns of amino acids near signal sequence cleavage sites. Eur. J. Biochem. 135, 17-21.
99. Wilson B. A., Reich K. A., Weinstein B. R. and Collier R. J. (1990) Active-site mutations of diphtheria toxin: effects of replacing glutamic acid-148 with aspartic acid, glutamine or serine. Biochem. 29, 8643-8651.
100. Wolfner M. F., Harada H. A., Bertram M. J., Stelick T. J., Kraus K. W., Kalb J. M., Lung Y. O., Neubaum D. M., Park M., and Tram U. (in preparation) Peptide genes expressed specifically in the Drosophila melanogaster male accessory gland.
101. Yamaizumi M., Mekada E., Uchida T. and Okada Y. (1978) One molecule of diphtheria toxin fragment A introduced into a cell can kill the cell. Cell 15, 245-250.
102. Yamamoto K., Chadarevian A. and Pellegrini M. (1988) Juvenile hormone action mediated in male accessory glands of Drosophila by calcium and kinase C. Science 239, 916-919.