Sperm of the wasted mutant are wasted when females utilize the stored spermin Drosophila melanogaster

Genes and Genetic Systems

Volumn 86, Issue 2, 2011, Pages 97-108

  Ohsako, Takashi ^a   Yamamoto, Masa Toshi ^a  

^a KYOTO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Drosophila melanogaster; Fertilization; Male sterile mutation; Sperm storage; Sperm utilization

Indexed keywords

ARTICLE; CONTROLLED STUDY; COPULATION; DROSOPHILA MELANOGASTER; EJACULATION; FEMALE; FERTILIZATION; GENE; GENE MUTATION; MALE; MUTANT; NONHUMAN; OVULATION; PRONUCLEUS; SPERM; SPERMATHECA; WILD TYPE; WST GENE;

ANIMALS; CHROMOSOME MAPPING; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; FERTILITY; GREEN FLUORESCENT PROTEINS; MALE; SEXUAL BEHAVIOR, ANIMAL; SPERM CAPACITATION; SPERMATOZOA;

ANIMALIA; DROSOPHILA MELANOGASTER;

EID: 79959212475     PISSN: 13417568     EISSN: 18805779     Source Type: Journal    
DOI: 10.1266/ggs.86.97     Document Type: Article

References (52)

1. Allen, A. K., and Spradling, A. C. (2008) The Sf1-related nuclear hormone receptor Hr39 regulates Drosophila female reproductive tract development and function. Development 135, 311-321.
2. Anderson, R. C. (1945) A study of the factors affecting fertility of lozenge females of Drosophila melanogaster. Genetics 30, 280-296.
3. Avila, F. W., Ravi Ram, K., Bloch Qazi, M. C., and Wolfner, M. F. (2010) Sex peptide is required for the efficient release of stored sperm in mated Drosophila females. Genetics 186, 595-600.
4. Bertram, M. J., Neubaum, D. M., and Wolfner, M. F. (1996) Localization of the Drosophila male accessory gland protein Acp36DE in the mated female suggests a role in sperm storage. Insect Biochem. Mol. Biol. 26, 971-980.
5. Bloch Qazi, M. C., and Wolfner, M. F. (2003) An early role for the Drosophila melanogaster male seminal protein Acp36DE in female sperm storage. J. Exp. Biol. 206, 3521-3528.
6. Bloch Qazi, M. C., Heifetz, Y., and Wolfner, M. F. (2003) The developments between gametogenesis and fertilization: ovulation and female sperm storage in Drosophila melanogaster. Dev. Biol. 256, 195-211.
7. Boulétreau-Merle, J. (1977) Role des spermatheques dans l'utilization du sperme et la stimulation de l'ovogenese chez Drosophila melanogaster. J. Insect Physiol. 23, 1099-1104.
8. Callaini, G., and Riparbell, M. G. (1996) Fertilization in Drosophila melanogaster: centrosome inheritance and organization of the first mitotic spindle. Dev. Biol. 176, 199-208.
9. Castrillon, D. H., Gonczy, P., Alexander, S., Rawson, R., Eberhart, C. G., Viswanathan, S., DiNardo, S., and Wasserman, S. A. (1993) Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single Pelement mutagenesis. Genetics 135, 489-505.
10. Cattaneo, F., Pasini, M. E., and Perotti, M.-E. (1997) Glycosidases are present on the surface of Drosophila melanogasterspermatozoa. Mol. Reprod. Dev. 48, 276-281.
11. Chapman, T., Bangham, J., Vinti, G., Seifried, B., Lung, O., Wolfner, M. F., Smith, H. K., and Partridge, L. (2003) The sex-peptide of Drosophila melanogaster: female post-mating responses analyzed by using RNA interference. Proc. Natl. Acad. Sci. USA 100, 9923-9928.
12. Chen, P. S., Stumm-Zollinger, E., Aigaki, T., Balmer, J., Bienz, M., and Böhlen, P. (1988) A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell 54, 291-298.
13. de Lamirande, E., Leclerc, P., and Gagnon, C. (1997) Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol. Hum. Reprod. 3, 175-194.
14. Fitch, K. R., and Wakimoto, B. T. (1998) The paternal effect gene ms(3)sneaky is required for sperm activation and the initiation of embryogenesis in Drosophila melanogaster. Dev. Biol. 197, 270-282.
15. Fowler, G. L. (1973) Some aspects of the reproductive biology of Drosophila: sperm transfer, sperm storage, and sperm utilization. Adv. Genet. 17, 293-360.
16. Fraser, L. R. (1998) Fertilization promoting peptide: an important regulator of sperm function in vivo? Rev. Reprod. 3, 151-154.
17. Gao, Z. D., Ruden, M., and Lu, X. (2003) PKD2 cation channel is required for directional sperm movement and male fertility. Curr. Biol. 13, 2175-2178.
18. Gilbert, D. G. (1981) Ejaculate esterase 6 and initial sperm use by female Drosophila melanogaster. J. Insect Physiol. 27, 641-650.
19. Graner, M., Stupka, K., and Karr, T. L. (1994) Biochemical and cytological characterization of DPRO-1: A widely distributed proteoglycan in Drosophila. Insect Biochem. Mol. Biol. 24, 557-567.
20. Heifetz, Y., Tram, U., and Wolfner, M. F. (2001) Male contributions to egg production: the role of accessory gland products and sperm in Drosophila melanogaster. Proc. R. Soc. Lond. B 268, 175-180.
21. Hirai, K., Toyohira, S., Ohsako, T., and Yamamoto, M-T. (2004) Isolation and cytogenetic characterization of male meiotic mutants of Drosophila melanogaster. Genetics 166, 1795-1806.
22. Iida, K., and Cavener, D. R. (2004) Glucose dehydrogenase is required for normal sperm storage and utilization in female Drosophila melanogaster. J. Exp. Biol. 207, 675-681.
23. 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.
24. Karr, T. L. (1991) Intracellular sperm/egg interactions in Drosophila: a three-dimensional structural analysis of a paternal product in the developing egg. Mech. Dev. 34, 101-112.
25. Lefevre, G., and Jonsson, U. B. (1962) Sperm transfer, storage, displacement, and utilization in Drosophila melanogaster. Genetics 47, 1719-1736.
26. Lindsley, D. L., and Zimm, G. (1992) The Genome of Drosophila melanogaster. Academic Press, San Diego.
27. Liu, H., and Kubli, E. (2003) Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 100, 9929-9933.
28. Manning, A. (1962) A sperm factor affecting the receptivity of Drosophila melanogaster females. Nature 194, 252-253.
29. Manning, A. (1967) The control of sexual receptivity in female Drosophila. Anim. Behav. 15, 239-250.
30. Miller, A. (1950) The internal anatomy and histology of the imago of Drosophila melanogaster. In: The Biology of Drosophila (ed.: M. Demerec), pp. 421-534. John Wiley & Sons, New York.
31. Neubaum, D. M., and Wolfner, M. F. (1999a) Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently. Genetics 153, 845-857.
32. Neubaum, D. M., and Wolfner, M. F. (1999b) Wise, winsome, or weird? Mechanisms of sperm storage in female animals. Curr. Top. Dev. Biol. 41, 67-97.
33. Ohsako, T., Hirai, K., and Yamamoto, M-T. (2003) The Drosophila misfire gene has an essential role in sperm activation during fertilization. Genes Genet. Sys. 78, 253-266.
34. Pasini, M. E., Cattaneo, F., Pinto, M. R., De Santis, R., and Perotti, M.-E. (1999) Plasma membrane association and preliminary characterization of Drosophila sperm surface glycosidases. Mol. Reprod. Dev. 52, 166-173.
35. Peacock, W. J., and Erickson, J. (1965) Segregation-distortion and regularly nonfunctional products of spermatogenesis in Drosophila melanogaster. Genetics 51, 313-328.
36. Peng, J., Chen, S., Büsser, S., Liu, H., Honegger, T., and Kubli, E. (2005) Gradual release of sperm bound Sex-Peptide controls female postmating behavior in Drosophila. Curr. Biol. 15, 207-213.
37. Perotti, M.-E. (1975) Ultrastructural aspects of fertilization in Drosophila. In: The Functional Anatomy of the Spermatozoon (ed.: B. A. Afzelius), pp. 57-68. Pergamon Press, Oxford and New York.
38. Perotti, M.-E., Cattaneo, F., Pasini, M. E., Verní, F., and Hackstein, J. P. H. (2001) Male sterile mutant casanovagives clues to mechanisms of sperm-egg interactions in Drosophila melanogaster. Mol. Reprod. Dev. 60, 248-259.
39. Pitnick, S., Markow, T., and Spicer, G. S. (1999) Evolution of multiple kinds of female sperm-storage organ in Drosophila. Evolution 53, 1804-1822.
40. Ravi Ram, K., and Wolfner, M. F. (2007) Sustained post-mating response in Drosophila melanogaster requires multiple seminal fluid proteins. PLoS Genet. 3, e238.
41. Ren, D., Navarro, B., Prez, G., Jackson, A. C., Hsu, S. Shi, Q., Tilly, J. L., and Clapham, D. E. (2001) A sperm ion channel required for sperm motility and male fertility. Nature 413, 603-609.
42. Richmond, R. C., and Senior, A. (1981) Esterase 6 of Drosophila melanogaster: kinetics of transfer to females, decay in females and male recovery. J. Insect Physiol. 27, 849-853.
43. Santel, A., Winhauer, T., Blumer, N., and Renkawitz-Pohl, R. (1997) The Drosophila don juan (dj) gene encodes a novel sperm specific protein component characterized by an unusual domain of a repetitive amino acid motif. Mech. Dev. 64, 19-30.
44. Schiff, N. M., Feng, Y., Quine, J. A., Krasney, P. A., and Cavener, D. R. (1992) Evolution of the expression of the Gldgene in the reproductive tract of Drosophila. Mol. Biol. Evol. 9, 1029-1049.
45. Smith, M. K., and Wakimoto, B. T. (2007) Complex regulation and multiple developmental functions of misfire, the Drosophila melanogaster ferlin gene. BMC Dev. Biol. 7, 21.
46. Tram, U., and Wolfner, M. F. (1999) Male seminal fluid proteins are essential for sperm storage in Drosophila melanogaster. Genetics 153, 837-844.
47. Tweedie, S., Ashburner, M., Falls, K., Leyland, P., McQuilton, P., Marygold, S., Millburn, G., Osumi-Sutherland, D., Schroeder, A., Seal, R., et al. (2009) FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res. 37, D555-D559.
48. Wakimoto, B. T., Lindsley, D. L., and Herrera, C. (2004) Toward a comprehensive genetic analysis of male fertility in Drosophila melanogaster. Genetics 167, 207-216.
49. Watnick, T. J., Jin, Y., Matunis, E., Kernan, M. J., and Montell, C. (2003) A flagellar polycystin-2 homolog required for male fertility in Drosophila. Curr. Biol. 13, 2179-2184.
50. Wilson, K. L., Fitch, K. R., Bafus, B. T., and Wakimoto, B. T. (2006) Sperm plasma membrane breakdown during Drosophila fertilization requires Sneaky, an acrosomal membrane protein. Development 133, 4871-4879.
51. Wong, A., Albright, S. N., Giebel, J. D., Ravi Ram, K., Ji, S., Fiumera, A. C., and Wolfner M. F. (2008) A role for Acp29AB, a predicted seminal fluid lectin, in female sperm storage in Drosophila melanogaster. Genetics 180, 921-931.
52. Zimmering, S., and Fowler, G. L. (1968) Progeny: sperm ratios and non-functional sperm in Drosophila melanogaster. Genet. Res. 12, 359-363.